Escolar Documentos
Profissional Documentos
Cultura Documentos
Deeper Understanding cloud parameterization—by using a model that spectral ellipsometry with the high spatial reso-
allows direct coupling of atmospheric circulation lution of near-field microscopy. They used this
of the MJO and clouds to simulate an MJO event. Their method to study the metal-insulator transition in
The Madden-Julian Oscillation (MJO) is a large- results show that MJO predictions extending VO2 and identified an inhomogeneous state with
scale (1000-kilometer) atmospheric disturbance 1 month into the future soon may be possible. metallic and insulating regions near the transi-
that propagates slowly eastward through the tion regime. Within the metallic regions, they
tropics from the Indian Ocean to the western observed a divergent electron mass, an effect
Pacific during the course of 30 to 60 days. The Storing Light in Optic Fiber predicted by one of the competing scenarios of
MJO affects precipitation over the tropical mon- Communication with optical pulses is fast, but the transition in which correlation effects play a
soon regions and has been implicated as a trig- direct storage of optical signals for later process- dominant role.
ger of El Niño–Southern Oscillation events. It is ing is challenging. There are routes for stopping
coupled with the upper ocean through its effects and storing light that make use of quantum
on surface fluxes of solar radiation caused by gases, but the wavelengths that can be used are A Magnesium(I) Dimer
changes in cloudiness, and on evaporation from fixed by the excitation levels of the atoms or ions The partially reduced +1 state has rarely been
the ocean surface caused by surface wind speed of the gas. Zhu et al. (p. 1748; see the news observed for magnesium or any of its
changes, which can heat or cool the ocean mixed story by Cho) show that stimulated Brillouin heavier alkaline-earth congeners,
layer by up to 1°C during a strong MJO event. scattering can be used to write a sequence of calcium, strontium, and barium.
Nonetheless, important aspects of the MJO still optical pulses as an acoustic signal in a fiber and Green et al. (p. 1754, published
are unclear, such as how deep into the ocean its retrieve the signal on demand with a read pulse. online 8 November) used potassium
influence extends, in part because the range of Thus, variable delays can be achieved with com- metal to reduce a
scales of the processes it involves have made it monly used components. The induced time pair of Mg(II)
difficult to simulate in models (see the Perspec- delays are limited by the lifetime of the acoustic compounds and
tive by Hartmann and Hendon). Matthews et al. signal, but can be on the order of several thereby isolate and
(p. 1765) used a data set of unprecedented size nanoseconds. The authors also show that a small crystallographi-
CREDITS (TOP TO BOTTOM): LAUREN O’MALLEY; GREEN ET AL.
obtained from autonomous, free-drifting instru- number of pulses can be stored simultaneously cally characterize
ments, called Argo floats, to show that the sur- within the optic fiber. stable dimers in which two
face wind stress associated with the MJO can Mg(I) centers are connected by a single bond.
force eastward-propagating oceanic Kelvin waves Coordination of bulky bidentate nitrogen-based
that extend to a depth of 1500 meters and that
have amplitudes of as much as six times those of
Close-Ups of ligands helped stabilize these unusual complexes.
cent conditions of offshore and deeper water environments. However, it is difficult to reconstruct the com-
plex processes of mud deposition in the laboratory, such as the clumping of particles into floccules. Using
flume experiments, Schieber et al. (p. 1760; see the Perspective by Macquaker and Bohacs) investi-
gated the transport and deposition of clay floccules and find that this process occurs at flow velocities that
transport and deposit sand. Floccules form and are deposited over a wide range of experimental condi-
tions. The floccules form ripples that develop into mud beds and appear laminated after compaction.
These results bear not only on interpretations of paleoenvironments that mudstones record, but also on
current problems such as hydrocarbon exploration and the management of sediment accumulation.
taking serious steps to mitigate carbon dioxide emissions: the root cause of global warming
and the reef problem. Experience suggests that for this, we might have to await an election.
– Donald Kennedy
10.1126/science.1153230
infected ants almost immediately reduced their interaction with ant larvae in the brood cham-
ber, apparently helping to protect the most valuable or susceptible individuals in a colony. The
Disturbing Patterns
absence of aggression by uninfected worker ants toward afflicted individuals suggests that such Forest habitats around the world vary widely in
standoffishness may be due to self-restraint. Second, the uninfected workers increased their the nature of the influence that humans have
brood-care activities, primarily via grooming to remove spores from the infected individuals. had on them. Some forests are primary (more or
Rather than increasing their own incidence of infection, the naïve ants acquired a higher level less undisturbed), others are secondary (regrown
of resistance to the fungus—providing a form of “social prophylaxis.” — GR after human disturbance), and some are entirely
Curr. Biol. 17, 1967 (2007). artificial (plantations). In our era, the balance of
forested area tilts ever more to the secondary
and managed end of the spectrum. In this con-
text, Barlow et al. assessed the conservation
M AT E R I A L S S C I E N C E and the other half below the initial starting plane. value of primary, secondary, and plantation
They then electroplated a nanocrystalline alloy of forests in the tropics by comparing the species
Extra-Strong Sleeves nickel and iron to form a sleeve around the struts richness of major invertebrate, vertebrate, and
The sponge-like structure of metallic foams (up to and nodes of the plant taxa across replicated sites in
80% void fraction) has fostered applications in trusses, with the Amazonia. A range of patterns
impact-absorbing materials, acoustic insulation, thickness controlled was observed. A few taxa (scav-
and lightweight structural materials. More recent over a 75- to 400- enger flies, moths, and grasshop-
attention has focused on periodic cellular materi- µm range by the pers) appeared to be more
als (PCMs), wherein the remaining mass exclu- deposition time. The species-rich in the secondary and
sively forms load-bearing trusses that are loaded loading stiffness plantation forests; unsurprisingly,
in tension or compression rather than bending. more than doubled at the other extreme, amphibians,
A second design strategy for strengthening metals and the peak birds, and woody plants were far
is to reduce grain size to the nanometer scale and strength increased better represented in the undis-
thereby localize a larger number of atoms at grain 10-fold. The specific turbed forest; small mammals, orchid
boundaries, reducing their mobility. Suralvo et al. strength, which accounts for changes in density, bees, and fruit flies appeared to be relatively
created a PCM by stretching a square punched also increased almost threefold. — MSL unaffected by habitat type. These data help to
aluminum sheet to displace half the nodes above Scripta Mater. 58, 247 (2008). Continued on page 1699
Tiger tracked to Sale of Rare is one of only eight such instruments known to
this 2002 poster. exist in the world, the culture department says.
Astrolabe Halted A horizon line positioned at 52° N shows that it
This 14th century brass astrolabe probably was made for use in southern England.
belonged to an educated gentleman about
1388, the time Geoffrey Chaucer was writing
The Canterbury Tales. Now the owner wants to Dehydrated DNA
sell it to a foreigner, and the U.K. government Here’s a new item for your family album: your
is moving to keep it in Britain. genes. For $175, DNA Direct, a clinical genetic
Found in 2005 under the floors of a testing outfit in San Francisco, California, will
17th century inn just outside provide a kit you can use to swab your
Flat Cat: Act II Canterbury, the pocket- cheek and mail in a sample. A week or
Suspicions about purported photographs of a sized instrument, val- two later, you’ll receive three vials
presumed-extinct South China tiger (Science, ued at about £350,000, containing your air-dried and chemically
9 November, p. 893) were confirmed last has been in the posses- stabilized DNA, which can be stored
month when a netizen found the apparent sion of the landowner. indefinitely at room temperature and
source of the image: a 2002 Chinese lunar The name of the purchaser reactivated with a few drops of water.
New Year poster. But China’s obsession is confidential, according The samples have more than senti-
with the issue has continued. The China to a spokesperson for the mental value. The company sug-
Photographers Association convened a team Department for Culture, Media, and gests they might come in handy for
including biologists and forensic scientists Sports. The department has put a temporary genealogy, family medical histories,
who met in Beijing for 5 days pondering ban on the astrolabe’s export to give U.K. insti- settling inheritance suits, determining paternity
40 digital photos of the beast. On 2 December, tutions time to raise money to buy it. in the face of an elusive male, or—in a pinch—
they noted, among other things, that the Used for timekeeping, surveying, and per- identifying your remains should some dire
tiger was in exactly the same position in all forming astronomical calculations, this quadrant mishap render them unrecognizable.
the photos and that its eyes did not reflect
the camera’s flash.
Both the photographer and the State
Forestry Administration (SFA), however,
Oh, to Live in Iceland
continue to maintain that a tiger exists Iceland has the most well-developed humans of any country on Earth, according to the
in the mountains of Zhengping County. 2007/2008 United Nations Human Development Index, which rates life expectancy, income,
At a 4 December press conference, an SFA and education in 177 countries and regions. The land of geysers and glaciers displaced Norway,
spokesperson reiterated that the agency which has led the ranking for 6 years. Although not first in any category, Iceland ranked third in
plans to look for it. After the first snowfall, life expectancy (81.5 years), 13th in combined school and college enrollment (95.4%), and
10 large-carnivore experts will comb a fifth in per capita gross domestic product (U.S. $36,510). Australia, Canada, and Ireland round
200,000-hectare forested region for signs out the top 5, with the United States slipping from eighth to 12th. All 22 countries in the Low
of tigers, leopards, and bears. As for the Human Development category are in Africa.
photos, an SFA official offered this logic: Demographer Elwood “Woody” Carlson of Florida State University, Tallahassee, notes that
CREDITS (TOP TO BOTTOM): WWW.YWXINLONG.COM; COURTESY OF MLA; JENS NIETH/CORBIS
“There are a lot of photographs of the Loch it’s not fair to compare small countries to the United States. “We probably should be compar-
Ness monster [in Scotland]. … People care ing Iceland to Connecticut or something. … If you average together all the European countries,
about the existence of the monster rather the continent as a whole doesn’t look much different from the U.S.A.”
than the authenticity of the photos.”
Enjoying longevity in the
Blue Lagoon, hot springs
MIT: Completely Online near Reykjavik.
It took 5 years, but the Massachusetts Institute of
Technology in Cambridge has put all its courses
online. Free materials for all 1800 courses
are available at ocw.mit.edu—everything
from full video talks about aerospace engineer-
ing to anthropology lecture notes about
“Intersubjectivity, Phenomenology, Emotion,
and Embodiment.” The site has drawn 35 million
visitors since 2002, most from outside North
America, says MIT’s Stephen Carson. “It’s
unprecedented to have all the courses available
at a university this deeply and openly available
on the Web. … It’s an extension of the public-
service function of the university.”
1710 1711
Hot property. The much-coveted site behind the
British Public Library and next to the St. Pancras
railway station may house 1500 scientists by 2013.
and world medical science,” says UCL Vice- wanted to strengthen NIMR’s efforts in transla- LRI Director Richard Treisman, noting that
Provost Edward Byrne. tional medicine by marrying it to a research Cancer Research UK needs to have a visible
Although there’s no guarantee the proj- university and hospitals. In 2005, it announced presence, as it depends on public donations.
▲
1712
British Nobel laureate Paul Nurse, presi- those at NIMR now and that NIMR’s World UCL. Yet MRC, they note, hasn’t said how
dent of Rockefeller University in New York Influenza Centre will be part of the project, many NIMR labs will be eliminated. Given the
City, heads a committee that will develop sci- but it has made no assurances to other labs. potential uncertainty during the next 7 years,
ence plans for the project by next year. “The “Not everyone will relocate. That’s clear,” they worry that colleagues will simply leave.
aim of this group is to be as ambitious as pos- says Winterton. Some even wonder whether the institute’s name
sible,” says Byrne. What to incorporate from Although not agreeing that relocation is will live on at the new facility. “I don’t know if
NIMR will likely be the stickiest topic Nurse needed, several NIMR scientists who talked to this will mean the real end of NIMR,” says
faces. MRC has said that the new site will Science acknowledge that the new proposal has Jonathan Stoye, a virologist at the institute.
have animal research facilities comparable to much more appeal than the smaller union with –JOHN TRAVIS
SPACE SCIENCE
moon’s origins and composition (Science, were chipping away at it. In the
31 August, p. 1163). “Beautiful Science” forum of
Launched on 24 October, Chang’e-1 People Net, one anonymous indi-
maneuvered into a polar orbit, 200 kilome- vidual drew attention to a tiny
ters above the surface, on 7 November, Picture perfect. Chinese Premier Wen Jiabao unveils the rectangular shadow and asked,
according to the Beijing Aerospace Com- Chang’e-1 composite at a 26 November press conference. facetiously, whether it is the
▲
tion, longitudes converge at the poles and CCD camera to help determine a landing site affect NASA’s ability to put the first piece of the
latitudes are parallel. A low-resolution for the planned 2012 lander mission. A deci- Japanese Kibo module into orbit in February. A
image is available from the CNSA Web site sion on the payload and launch date of the sec- short delay is no big deal for European and
(www.cnsa.gov.cn/n615708/n620172/ ond probe is expected in early 2008, Wu says. Japanese scientists, who have been waiting
n677078/n751578/images/1798046.jpg). –HAO XIN AND RICHARD STONE since 2004. –ANDREW LAWLER
Rosiek came to a similar conclusion after With reporting by Andrew Lawler.
DEPLOYMENT
Coal carbon capture
Baucus (D–MT) during the $15.7 billion shake,” he told Science.
panel’s 5 December markup Just what is fair, however, is a key unre-
of the bill. “This is it.” Renewable energy solved question. Sanders had criticized an
So far, the debate about cli- Assistance, training, $15.7 billion earlier version that would have forced renew-
mate legislation has focused and adaption ables to compete for deployment funds
▲
on who should pay as the $55.8 billion Advanced vehicles
United States overhauls its $7.6 billion
Making allowances. Proceeds from a carbon credit
energy system. The question Cellulosic biomass auction would be distributed among a number of
of how to allocate the vast * Based on estimated outlays in 2030. $3.8 billion programs. The amounts assume a carbon dioxide
sums that a federally managed equivalent price of $49 per ton.
RESEARCH POLICY
At a meeting of the advisory committee time around, which happens most of the the usual 15 or 20 members to as many as 80,
to the NIH director on NIH’s Bethesda, time. But the appeals, Zerhouni said at the to accommodate the increasingly special-
Maryland, campus last week, leaders of this meeting, have created a “traffic jam” and a ized science being proposed. Sending appli-
review highlighted the recommendations system that “penalizes the new entrant to a cations containing certain technical details
they may deliver to Zerhouni in February. very extreme degree.” to outside experts, who would consider those
No final decisions have been made, how- Yamamoto thinks reviewers ought to elements alone and report back to the study
ever, and the committees are weighing assess applications first for their scientific section, is one way to slim study sections
everything, including shortening grant impact and, in cases that seem hopeless, down. Shorter grant proposals, meanwhile,
applications to seven pages from the current communicate that unequivocally to the could allow each one to be evaluated by four
25 pages and recommending an “editorial applicant without allowing resubmissions. people instead of the usual two.
fare as well, because with shorter applica- choose to go into a career where you begin to dom have announced that they may pull out of
tions, name recognition could carry more be independent when you’re 45?” the project. –ADRIAN CHO
weight. The NIH system cannot allow such a –JENNIFER COUZIN
▲
PHYSICS
CREDITS (TOP TO BOTTOM): B. STEVENS ET AL., CELL 131, 1–15 (14 DECEMBER 2007) 2007 ELSEVIER INC.; PETER HOEY
physicists report a simpler way to hit the the University of Rochester, New York, opted Gauthier says. The atomic and resonator tech-
brakes: They convert light in an optical for an optical fiber. They fed a “data” pulse in niques generally work at one frequency.
f iber into a slow-moving vibration and one end and a short, intense “write” pulse in the The conversion doesn’t depend on quan-
then back into light. other. When the two collided, the data pulse tum mechanics, notes Lene Hau, a physicist
“This has the enormous advantage of disappeared and was replaced by a vibration at Harvard University and one of the first to
simplicity,” says Stephen Harris, an applied crawling along at just 1/40,000 stop light. That should make the effect more
physicist at Stanford University in Palo the speed of light in a fiber. robust but rules out truly bizarre embellish-
Alto, California, and a pioneer of To convert the vibration ments. For example, Hau and colleagues
the atomic techniques. have encoded a light pulse in one cloud of
“Conversely, it can’t do atoms and revived it in another cloud by let-
some things that the ting a few atoms drift between the two, as
other techniques can.” Shake it up! The new technique they reported 8 February in Nature. Such a
To store a pulse of turns light into motion in an feat would be impossible with the fiber tech-
laser light in a cloud of optical fiber. nique. Still, Hau says, “it’s very important to
atoms, researchers shine a try different systems.”
second laser into the cloud at back to light, the researchers The atomic systems might someday pro-
the same time. The overlapping light hit it with a “read” pulse vide the memory for quantum computers,
fields interact with the atoms in a way identical to the write pulse. Harris says. Gauthier sees more immediate
that greatly decreases the light’s speed. The fiber vibrates because uses for the fiber-optic approach. For exam-
The light also nudges each atom into a the light makes it contract ple, it might be used to measure the correla-
strange quantum-mechanical condition in in the spots where the light is most intense. tions between signals in optical networks. But
which it spins in two different directions at To make the conversion efficient, the team first researchers must increase the storage
once. The precise spin mixture varies from tuned the frequency of light in the read pulse time and reduce the power in the read and
point to point in the cloud, effectively freezing slightly lower than that in the data pulse. The write pulse from a walloping 100 watts. That’s
the light pulse into the atoms when the refer- two had to differ by the frequency of the enough to shake up anybody. –ADRIAN CHO
at puny, immature-looking synapses in the thought just functioned in the immune sys- Compared to normal adult mice, adult glau-
developing nervous system. tem, it disrupts a very specific event that we coma mice exhibited elevated C1q levels:
When the researchers examined the think is involved in making the precise, final The protein accumulates at retinal synapses
brains of mice lacking a functional C1q connections in the developing visual sys- early in the disease, even before synapses
gene, they found that development had gone tem.” Many questions remain, however. disappear and neurons die off.
awry in the lateral geniculate nucleus, a Barres suspects that complement proteins Synapse loss precedes cell death in
relay station in the brain that receives synap- mark unwanted synapses for removal by Alzheimer’s and other neurodegenerative
tic inputs directly from retinal neurons. In microglia, immune cells in the brain. More diseases, Barres notes. He speculates that
normal mice, geniculate neurons initially work is needed to demonstrate that, drugs that block the complement cascade
receive inputs from both eyes and then prune Boulanger says, and to figure out why only may forestall neurodegeneration in a num-
them so that they only receive input from certain synapses are flagged for removal. ber of disorders. It’s an exciting idea, says
one eye or the other. In the mutant mice, Finally, Barres and colleagues collabo- Monica Vetter, a neurobiologist at the Uni-
geniculate neurons maintained extraneous rated with Simon John’s group at the Jack- versity of Utah in Salt Lake City: “There’s
inputs from both eyes into adulthood. son Laboratory in Bar Harbor, Maine, to good evidence that these complement com-
That’s a striking finding, Boulanger says: investigate whether C1q might have a role in ponents are upregulated in other diseases.”
“When you get rid of these proteins that we synapse loss in a mouse model of glaucoma. –GREG MILLER
ECOLOGY
fish farms in British Columbia. The situation from the Canadian fisheries agency on the abundance, including fluctuations in ocean
was alarming because young pink salmon are number of salmon in seven rivers that flow nutrients. But fisheries biologist Ray Hilborn
more vulnerable to damage from lice than into marine channels with fish farms. They of the University of Washington, Seattle, says
adult salmon are. also looked at 64 rivers from which migrating it is too risky to farm fish in open pens near
Graduate student Martin Krko sek of the
v
salmon do not pass by fish farms. Using a wild relatives: “The bigger concern is that
University of Alberta, Edmonton, started standard model, they calculated that pink [sea lice] are just one of many pathogens.
studying the problem in 2003. In previous salmon not exposed to fish farms showed the There could be other things out there that we
papers, he and colleagues calculated that same range of population size for all 35 years, don’t know about.” –ERIK STOKSTAD
Time to spawn
Until recently, catching corals in the act has
been more art than science. Spawn-chasers
must contend with bad weather, miscalculated
spawning times, problems with permits to
transport live corals, and a host of unknowns
about conditions conducive to survival of
young coral (see sidebar, p. 1715). Woesik, an ecologist at the Florida Institute of equinoxes, when the amount of insolation,
Although coral clones form the bulk of the Technology in Melbourne. “The problem for or sunlight hitting any one spot, is highest.
pillars and billowing mounds of healthy reefs, decades has been that we have been study- A literature review revealed that spawning
after a few years’ growth, individuals in the ing coral spawning at mid-latitudes,” he schedules in the Great Barrier Reef and off
colonies become sexually active. Most explains. In the tropics, water temperatures Japan also track insolation.
species spew gametes into the water in a milky vary by only about 3°C—not much of a cue, Van Woesik and his colleagues next looked
frenzy of fertilization en masse. For many he contends. At higher latitudes, corals off at spawning in the Caribbean. They combed
corals, this is a once-a-year event. Thus, western Australia spawn in late summer, the literature and got timing information for
“spawning together is a biological impera- whereas those off the east coast spawn in 12 species, including elkhorn, brain, and star
tive,” says Miller. spring, even though water temperatures peak corals, from Venezuela to Bermuda. Again,
To ensure sufficient concentrations of egg in both regions in summer. insolation seemed to set the spawning clocks.
and sperm for fertilization, corals need to From September 2002 until February It could be that insolation fluctuations affect
know the right month, the right day, even the 2003, van Woesik and research fellow symbiont productivity, periodically fueling
right hour to release gametes. For decades, Lolita Penland kept tabs on two tropical gonad growth, van Woesik says.
researchers assumed that warming sea surface reefs in Palau. They discovered that multi- Some reef researchers are dubious. “We
temperatures stimulate the production and ple species spawned multiple times over the need experimental work to understand how
CREDIT: CINDY LEWIS
maturation of gametes, which burst forth a course of the year. Temperature didn’t seem these environmental cues are translated
few days after the full moon, at a precise time to matter. Rather, most of the time, spawn- into physiological change by the
after sunset. ing coincided with the spring and fall organisms,” says Guest. And
The role of temperature as the seasonal
cue never felt quite right to Robert van
Let the spawning begin. Pink egg and sperm bundles are released by Acropora digitifera polyps.
sively studied at the molecular level—will point to ways to minimize the guesthouse-cum-laboratory. The ground floor was covered with
global warming–inflicted damage to the 2000-kilometer-long Great baby baths, and tables strained under a mass of microscopes and chem-
Barrier Reef, which generates $4 billion a year in revenue. Diseases, icals. Ukani was chemically preserving 1-millimeter-diameter, pear-
most of them poorly understood (see sidebar, p. 1716), and urban runoff shaped white larvae for the genetic research.
are among the villains. A looming threat is acidification of the seawater “Tomorrow, they’ll start swimming,” Ukani says. After reaching this
from dissolved carbon dioxide (Science, 4 May, p. 678, and p. 1737 of stage out on the reef, some larvae corkscrew down to the bottom, look-
this issue). ing for a patch of sea floor that they will call home for the rest of their
To address these critical issues, four teams came to Magnetic Island lives—as long as 100 years. Other larvae drift for months, eventually
to raise larvae. There’s no magic formula. Some scientists filter and settling far away. That wanderlust, an evolutionary adaptation to cope
change water regularly, whereas others say this stunts larval growth. In with changing sea conditions, may be the key to survival for coral reefs
an even simpler approach, a team led by ecologist Andrew Baird of JCU as the planet warms. –CHERYL JONES
raises larvae in $1 buckets for studies about how temperature affects Cheryl Jones is a science writer based in Canberra, Australia.
▲
Marked for death. Caribbean
yellow-band disease ravages Barrier Reef—succumb to above-average
Montastraea faveolata in water temperatures.
Puerto Rico. Not every species is under siege. Even
where key reef-builders are in trouble,
“weedy” corals, such as mustard hill coral
(Porites astreoides) and lettuce coral
(Agaricia agaricites), are doing okay. Most
of these corals brood their young, and
Szmant hopes to zero in on differences that
gird brooders against environmental forces
that hit spawners hard.
And there is plenty of geographic variabil-
ity. In the Caribbean, for example, the prog-
nosis is not bleak for every reef. Larvae seem
to settle just fine near Bonaire and Curaçao,
WHITER SHADES OF PALE even where development has resulted in pol-
lution and high sediment loads. Szmant and
Disease is an unsung villain in the global degradation of coral reefs. Here are a few of the nastiest Miller are panning for clues to these reefs’
plagues that experts are keeping an eye on. All are expected to worsen as global warming nudges up secrets to success.
average ocean temperatures. In the Florida Keys, Miller has teamed up
Caribbean yellow-band disease is hitting reefs hard. “In Puerto Rico, some of the reefs that I with molecular ecologist Iliana Baums of
have been studying for 8 years have lost 60% of their live coral tissue,” says Ernesto Weil of the Uni- Pennsylvania State University in State College
versity of Puerto Rico. The disease has struck large, old colonies of Montastraea, or star coral, the to probe whether survival depends on having
main reef builder in the region. Scientists have not pinned down the pathogen that leaves yellow the right parents. In 2005, Baums developed a
rings as it chews through a colony, nor do they know if it targets the coral or its algal symbionts. Out- genetic test that distinguishes individual
breaks, once confined to summer, are now “permanent,” says Weil, and assaults have been quicker elkhorn corals. The test uses short bits of vari-
and deadlier than in the late 1990s, when the disease first appeared. The increased ferocity seems able DNA called microsatellites. Last summer,
to be correlated with a rise in average minimum water temperatures, Weil says. Miller and Baums collected egg and sperm
The Caribbean white diseases are a group of bacterial diseases that show up as bands or from elkhorn and mountainous star coral,
patches of bare white skeleton. In the early 1980s, white-band disease wiped out as much as looked at their microsatellite makeup, and
95% of the acroporid corals throughout the Caribbean. White plague first struck in the late cross-fertilized gametes from a number of
1970s in Florida. Since then, it has appeared regularly across the Caribbean, afflicting 42 of the individuals. They tallied how many larvae of
region’s 60 coral species. The disease advances and retreats in sync with each cross settled on plates coated with various
seasonal changes in water temperature. Although white plague communities of microbes and algae. “We saw
remains “a major concern,” Weil says, yellow band is emerging incredible differences in the performance of
as a bigger threat. different crosses,” says Baums. Some
Aspergillosis, caused by the soil fungus Aspergillus crosses yielded few offspring, whereas
sydowii, exacted a heavy toll on Caribbean sea-fan corals in others were prolific. Reef restoration may
the mid-1990s. The disease is now entrenched but at low lev- depend on collecting gametes from the
els, says C. Drew Harvell of Cornell University. Studies sug- hardiest parent colonies, says Baums.
gest that the pathogen will thrive in warming oceans, she
says. One glimmer of hope is that the sea fans are fighting Matchmaking
back. They are “resilient,” says Harvell, “and may have Larvae lucky enough to find turf to colo-
evolved increased resistance.” nize can’t go it alone: They must latch onto
White syndrome is a single disease—or a suite of dis- a symbiont. They tend to be picky about
eases—that was first spotted about 10 years ago on the Great which microscopic zooxanthellae algae will
Barrier Reef and later detected in the Marshall and Hawaiian get a cozy intracellular home in return for
islands and in Palau. It can wipe out entire colonies in weeks or Denuded. White plague generating a stable food supply. Mary Alice
months. Although the causes are unknown, there is evidence for afflicts Dichocoenia stokesii. Coffroth, a marine biologist at the University
both bacterial infections and runaway cell death. A 6-year study of at Buffalo, New York, and her colleagues have
CREDITS (TOP TO BOTTOM): ERNESTO WEIL
48 reefs spanning 1500 kilometers of the Great Barrier Reef linked outbreaks to rises in sea sur- been teasing out the molecular signals that
face temperatures and to coral density, says Bette Willis of James Cook University in Townsville, underlie a successful match.
Australia. Global warming is likely to trigger more outbreaks, she says. Researchers suspect that larvae recruit algal
Scientists are warily eyeing Montipora white syndrome, which is attacking one of the three main partners from the water column. Coffroth and
coral genera in the Hawaiian Islands. “Changes in disease levels are starting to concern us,” says Greta others are showing that larvae are selective but
Aeby of the Hawaii Institute of Marine Biology in Kaneohe. She and others suspect that urban runoff, not dead set on particular species. Coffroth
especially in Oahu’s south Kaneohe Bay, is fueling a slow but sure advance of the disease, the cause evaluated the potential of free-living Symbio-
of which is eluding scientists. Says Aeby, “This is one disease we expect will get worse.” –C.J. dinium to join forces with young corals called
octocorals by suspending trays of newly settled
larvae 20 meters above a reef. At the beginning In 2001, Dirk Petersen and Michael Last year, SECORE researchers and
of the experiment, none of the larvae had algae, Laterveer of the Rotterdam Zoo in the Nether- aquarists netted 900,000 elkhorn larvae in
but by the end, Coffroth and her colleagues lands set up SECORE to encourage aquarists to Puerto Rico. Each night during the spawning
found that just three of the many Symbiodinium bring coral reproduction in-house rather than season that August, divers collected gametes
varieties in the water had taken up residence in depend on harvesting coral from the sea. Work- and quickly returned them to shore or boat,
coral polyps. They found a similar pattern with ing with larvae of two species, Atlantic brain where others would mix gametes from differ-
algae from reef rubble and other bottom sur- coral and boulder star coral (Montastraea annu-ent spots, gently rocking coolers to encourage
faces where octocoral colonies live, they laris) from Curaçao, Petersen figured out how fertilization. “The whole crew had to work in
reported in the 5 December 2006 issue of to gather and fertilize gametes and raise larvae.
2-hour shifts, 24 hours a day for 4 days,”
Current Biology. Petersen recalls.
It remains a mystery how They wound up with far more
corals and zooxanthellae strike up larvae than they could handle.
a relationship. To eavesdrop on the Convention on International Trade
molecular signals of courtship, in Endangered Species of Wild
Mónica Medina, a geneticist at Fauna and Flora permits did not
the University of California, come through in time for the Euro-
Merced, and her colleagues have pean participants. And there were
collected larvae, extracted DNA, fresh hassles. Previously, Petersen
and pulled out bits of genes called had transported larvae in carry-on
expressed sequence tags (ESTs), luggage. But last year, new secu-
which allow researchers to study rity rules relegated corals to bag-
genes without knowing the full gage, and 100,000 larvae destined
sequence. So far they have 10,000 for the Columbus Zoo and Aquar-
ESTs for each of two coral species ium in Ohio got lost in transit for
and about 900 zooxanthellae 2 days and perished. Months later,
genes represented. They are put- only corals under the care of Mitch
ting the DNA to work on chips Carl of the Henry Doorly Zoo in
that can monitor changes in Omaha, Nebraska, had survived.
expression in thousands of genes He distributed many to other
at a time. In 2006, Medina and SECORE members, and 821
others collected eggs and sperm of colonies are now thriving.
elkhorn and mountainous star The second time around,
coral from a Florida reef, then last August, Henley and other
used DNA chips to monitor gene SECORE colleagues each took
expression after fertilization. home about 10,000 lar vae.
When they expose larvae to Once again, only Carl had the
zooxanthellae, “the corals go magic touch: He is raising some
wild,” says Medina, switching on 900 incipient colonies. “I’ll be
scads of genes. happy if I have one colony left
Virginia Weis, a cell biologist after 1 year,” says Henley.
at Oregon State University in Cor- Likewise, Szmant and Miller
vallis, has some ideas about which have little to show for their
genes are important. In studies of efforts to collect and fertilize
the sea anemone, a coral cousin gametes during spawning expe-
that also has symbionts, she dis- ditions. They release some larvae
covered that a nascent relationship right away and put others on the
hinges on run-of-the-mill genes reef after these have settled on
involved in programmed cell ceramic plates in the lab. “We
death and cell division. have been trying various things
to increase survivorship, but no
Planned parenthood major breakthrough yet,” says
CREDITS (TOP TO BOTTOM): DIRK PETERSEN
Life on the Mean Reefs How can so many predators live off so
few prey? Because prey reproduce and
grow much faster than predators do. “It’s
The short, nasty existence for reef-dwelling fish at two primeval atolls suggests that like your lawn,” says Friedlander. “The
intensive fishing elsewhere has skewed predator-prey dynamics more you mow it, the faster and thicker it
grows.” At Kingman, half-pints like sur-
Imagine an atoll in the time of Eden. It findings are in review at two publications. geonf ish, wrasses, and damself ish live
would be teeming with fish, a few big ones To begin to understand the future of reefs about half as long as counterparts at Christ-
and a lot of little ones swarming among the in a warming world, it’s not only important to mas, where the average prey is 20% bigger.
coral reefs. unravel the mysteries of coral but also essen- Still, life is literally no picnic at the top of
Think again, says a group of marine tial to work out the dynamics of reef commu- the food chain. Examining predators’ stom-
biologists who have been studying the Line nities. The more researchers learn, the more achs, the scientists found them mostly empty.
Islands south of Hawaii. Led by researchers acutely they feel the need to restore reefs to a “Kingman has shown us that unlike mam-
at the Scripps Institution of Oceanography state resembling primeval Kingman and mals, fish can survive with very little food.
in San Diego, California, they are compar- Palmyra. “If we don’t protect these places, it They simply grow slower,” Sandin says.
ing Kingman and neighboring Palmyra— will be the end of true natural selection in the And they don’t turn on each other, he
U.S. possessions that are among a handful oceans,” says Alan Friedlander of the s ay s , because they don’t want to risk
of Pacif ic atolls virtually untouched by injury. Nowhere else has Sandin
humans—with Fanning and Christmas, observed the voracious scrutiny
which belong to Kiribati and respectively that spearing elicits at Kingman
have some 3000 and 6000 residents. and Palmyra. “Your buddy shoots
To their surprise, the scientists found his spear against a rock—ping!—
that life at Kingman is anything but idyllic. and you notice that all the preda-
The ecosystem is dominated by large pred- tors in the neighborhood turn
ators to an extraordinary degree: About around. He shoots a fish and they
CREDITS (TOP TO BOTTOM): JENNIFER SMITH; STUART WESTMORLAND/CORBIS
85% of the estimated mass of all f ish is all come closer. If the fish gets
made up of apex predators such as sharks, away with an injury, it will be
large jacks, and snappers. For the prey fish, eaten within a minute,” he says.
life in the real Edens of Kingman and Desperation has made the preda-
Palmyra is just as the English philosopher tors fearless. “They nip at any-
Thomas Hobbes had described it for thing that moves: ears, ponytails,
humankind without society: “Nasty, When the cat’s away … Fewer predators near Fiji mean hordes of even pencils,” Sandin says.
brutish, and short.” small fish out and about, like these fairy basslets—but less total Such primeval reefs need not
“Inverted pyramids have been documented fish mass than at Kingman and Palmyra. be kept in pristine isolation: They
in plankton but never within a community of could be a test bed for sustainable
large animals,” says Scripps’s Stuart Sandin, National Oceanic and Atmospheric Admin- approaches to fishing, researchers say. “We
the project’s coordinator. “The intensity of istration’s biogeography branch in Hawaii. need to study more pristine reefs to see how
predation is new.” The more familiar pyra- Seen underwater, Kingman, a mostly much you can fish without reducing the fish
mid occurs at Christmas Island, where sharks sunken atoll 15 kilometers long, “looks like stocks,” Sandin says. “That’s the key question
have been fished for their fins and jacks and a small town at the start of a classic Western we need to answer.”
snappers for food. There, apex predators movie,” Friedlander says. “There’s nobody –CHRISTOPHER PALA
make up only 15% of the biomass. Their out on the street except for a few big bul- Christopher Pala is a writer based in Honolulu.
LETTERS
7. R. A. Butler, “Is the Amazon more valuable for carbon off-
edited by Jennifer Sills sets than cattle or soy?” (mongabay.com, 17 October
2007); http://news.mongabay.com/2007/1017-
amazon.html.
8. D. C. Morton et al., Proc. Nat. Acad. Sci. U.S.A. 103,
Switch to Corn Promotes Amazon Deforestation 14637 (2006).
9. D. C. Nepstad et al., Conserv. Biol. 20, 1595 (2006).
10. D. L. Hard, in Protein Sources for the Animal Feed
THE UNITED STATES IS THE WORLD’S LEADING PRODUCER OF SOY. HOWEVER, MANY U.S. FARMERS Industry (Animal and Production Health Proceedings,
FAO, Rome, 2002), pp. 125–140.
are shifting from soy to corn (maize) in order to qualify for generous government subsidies 11. W. F. Laurance et al., Science 291, 438 (2001).
intended to promote biofuel production (1); since 2006, U.S. corn production has risen 19% 12. P. M. Fearnside, Environ. Conserv. 28, 23 (2001).
while soy production has fallen by 15% (2). This in turn is helping to drive a major increase in
global soy prices (3), which have nearly doubled in the past 14 months.
The rising price for soy has important consequences for Amazonian forests and savanna- NASA Funding Slow, Not
woodlands (4). In Brazil, the world’s second-leading soy producer, deforestation rates (5) and
especially fire incidence (6) have increased sharply in recent months in the main soy- and beef-
Steady, After Space Race
producing states in Amazonia (and not in states with little soy production). Although dry weather AFTER READING D. KENNEDY’S EDITORIAL
is a contributing factor, these increases are widely attributed to rising soy and beef prices (5, 7), and “Sputnik nostalgia” (5 October, p. 17), I find
studies suggest a strong link between Amazonian myself in a state I did not expect—one of dis-
deforestation and soy demand (8, 9). appointment. Kennedy writes about the posi-
Some Amazonian forests are directly tive effects the launch of Sputnik had on edu-
cleared for soy farms (8). Farmers also pur- cation and the nation’s educational commu-
chase large expanses of cattle pasture for soy nity. These improvements resulted largely
production, effectively pushing the ranchers from an increase in federal sponsorship that
farther into the Amazonian frontier or onto came as part of the backlash from Sputnik.
lands unsuitable for soy production (9). In Yet, there lies within this seemingly fine out-
addition, higher soy costs tend to raise global come an issue that needs to be addressed.
beef prices because soy-based livestock feeds The National Aeronautics and Space
become more expensive (10), creating an indi- Administration (NASA) was formed along
rect incentive for forest conversion to pasture. with a dramatic increase in federal funding for
Deforestation. The aftermath of forest burning in Finally, the powerful Brazilian soy lobby is a science and science education in response to
central Amazonia. key driving force behind initiatives to expand the former Soviet Union’s incredible achieve-
Amazonian highways and transportation net- ment (1). When Neil Armstrong became the
works in order to transport soybeans to market, and this is greatly increasing access to forests first person to set foot on the moon, the gov-
for ranchers, loggers, and land speculators (11, 12). ernment’s interest in science dropped almost
In a globalized world, the impacts of local decisions about crop preferences can have far- immediately. Because of the sudden lack of
reaching implications. As illustrated by an apparent “corn connection” to Amazonian deforesta- funding, the Apollo program was discontin-
tion, the environmental benefits of corn-based biofuel might be considerably reduced when its ued just 6 years after Apollo 11 landed in the
full and indirect costs are considered. Sea of Tranquility, in order to save funds for
WILLIAM F. LAURANCE the shuttle and Skylab programs (2). Lately,
Smithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Ancón, Panama. E-mail: laurancew@si.edu NASA has received additional funding to
attempt a second series of missions to the
References and Notes moon as part of the Constellation Program (3),
1. P. C. Westcott, “U.S. ethanol expansion driving changes throughout the agricultural sector”
(www.ers.usda.gov/amberwaves/september07/features/ethanol.htm).
but the long-awaited increase is the bitter-
2. National Agricultural Statistics Service Acreage Report, U.S. Department of Agriculture sweet result of an imaginary space race (4).
It seems that only when faced with the
CREDIT: WILLIAM F. LAURANCE
(www.usda.gov/nass/PUBS/TODAYRPT/acrg0607.pdf).
3. USDA-ERS (www.ers.usda.gov/data/priceforecast/data/futmodsoybeans.xls). Growing global demands for soy for edible oil,
livestock feed, and biodiesel are also contributing to high soy prices.
threat of looking stupid or coming in second
4. The corn-soy-deforestation link was evidently first noted by D. C. Nepstad et al., The Amazon in a Changing Climate: Large- place does our government open its wallet to
Scale Reductions of Carbon Emissions from Deforestation and Forest Impoverishment [Amazon Institute for Environmental science (1, 4).
Research (IPAM), 2006]. MICHAEL J. GOLDSTEIN
5. C. Angelo, Desmatamento cresce 8% na Amazonia, Folha de São Paulo Online (www1.folha.uol.com.br/
folha/ambiente/ult10007u337678.shtml). Department of Biology, Rutgers University, Camden, NJ
6. ImazonGeo (http://imazongeo.org.br/alerta2.php). 08102, USA.
PTSD. In responding, we need to consider been reported beyond 6 months. Further- Research Article. Perhaps all of these findings
complexities in the treatment of these disor- more, because PTSD research lacks rigorous explain why it may be necessary to revisit an
ders that we could only briefly allude to in our randomized clinical trials, “responder” lev- emotionally distressing memory before it can
Research Article (13 July, p. 215) (1). els have been overreported (3). We believe, be controlled via suppression. In any case,
First, Holmes et al. note that PTSD therefore, that conceptualization and testing such processes may provide part of the biolog-
patients who characteristically avoid their of complementary therapeutic approaches ical basis for exposure and restructuring
traumatic memories have a poorer prognosis. is needed. CBT methods.
However, unsystematic avoidance by a patient Some forms of CBT may tap into the BRENDAN E. DEPUE,1,2* TIM CURRAN,1,2,3
is not the same as a systematic therapeutic brain mechanisms underlying suppression. MARIE T. BANICH1,2,3,4
process of directed suppression, which Research suggests that cognitive restructuring 1Department of Psychology, University of Colorado,
involves the acquisition of neural suppression could benefit sufferers of PTSD (4). Cog- Boulder, CO 80309, USA. 2Center for Neuroscience,
University of Colorado, Boulder, CO 80309, USA. 3Institute
over a number of trials. Second, we do not nitive restructuring processes may involve of Cognitive Science, University of Colorado, Boulder, CO
advocate suppression as a sole means of treat- attaching a new emotional significance to a 80309, USA. 4Department of Psychiatry, University of
ment for PTSD, but rather as a complemen- negative memory or cognition, as well as less- Denver Health Sciences, Denver, CO 80208, USA.
tary treatment with other methods. For exam- ening physiological arousal (5, 6). Further- *To whom correspondence should be addressed. E-mail:
ple, it may be necessary to revisit an emotion- more, new responses paired with an original depue@colorado.edu
ally distressing memory before it can be con- conditioned stimulus may have inhibitory
trolled [our Research Article and (1)]. influences over the amygdala via a pathway References
1. B. E. Depue, T. Curran, M. T. Banich, Psychol. Sci. 17,
Currently, only about 30 to 70% of PTSD from the medial prefrontal cortex to the baso- 441 (2006).
patients respond successfully to exposure lateral amygdala to the central amygdala (7, 2. R. Bradley et al., Am. J. Psychiatr. 162, 214 (2005).
therapy alone. Even these “responders” are 8). In addition, research examining the cogni- 3. G. Harvey, R. A. Bryant, N. Tarrier, Clin. Psychol. Rev. 23,
501 (2003).
only classified as such because they experi- tive manipulation of emotional significance, 4. B. Nemeroff et al., J. Psychiatr. Res. 40, 1 (2006).
ence reductions in just one or two key symp- known as reappraisal, has shown increased 5. J. Debiec, V. Doyere, K. Nader, J. E. Ledoux, Proc. Natl.
toms (2). Other symptoms may still be vivid, activation in areas of the middle and inferior Acad. Sci. U.S.A. 103, 3428 (2006).
6. I. Izquierdo, M. Cammarota, Science 304, 829 (2004).
and patients may suffer from relapses. frontal gyri and decreased activation in the 7. G. J. Quirk et al., J. Neurosci. 23, 8800 (2003).
Few long-term comprehensive studies of amygdala (9). These are the specific pre- 8. M. R. Milad, G. J. Quirk, Nature 420, 70 (2002).
the relapse rate of PTSD symptoms have frontal areas involved in suppression in our 9. N. Ochsner et al., J. Cognit. Neurosci. 14, 1215 (2002).
Driven by Rare Cancer Stem Cells” leukemia but not others. Interestingly, however,
the reported phenotypes of the mouse leukemo-
genic subpopulations are variable and more
Jerry M. Adams,1* Priscilla N. Kelly,1,2 Aleksandar Dakic,1,2 Stephen L. Nutt,1 Andreas Strasser1* similar to relatively mature cells than hemato-
poietic stem cells (11–13).
A critical issue for cancer biology and therapy is whether most tumor cells or only rare “cancer stem The evidence for cancer stem cells in solid
cells” sustain tumor growth. Although the latter model seems supported by the minute proportion tumors is less advanced than for AML (1) and
of human leukemia cells that can grow in immunodeficient mice, evidence that more than 10% of is subject to the same reservations regarding
cells in many mouse leukemias and lymphomas are transplantable challenges its generality. xenotransplantation. The cancer-propagating
cells are often found within subpopulations
key unresolved issue for cancer biology were tumorigenic (7), it used a less sensitive, (e.g., CD133+) that can contain up to 20% of
I
n What Makes a Terrorist: Economics and What, then, are the root Roots of Terrorism patterns in the data. Occasion-
the Roots of Terrorism, Alan Krueger (a causes of terror? Krueger sug- ally, Krueger acknowledges
by Alan B. Krueger
professor of economics and public policy gests two. First, across coun- such concerns. Often, however,
at Princeton University and adviser to the U.S. tries, the absence of political Princeton University Press, he seems overly confident of his
National Counterterrorism Center) addresses a freedom is positively corre- Princeton, NJ, 2007. 192 pp. conclusions, given the evidence.
key question in the academic and policy lated with terror attacks. Thus, $24.95, £14.95. One example relates to
ISBN 9780691134383.
debates sparked by 9/11: What are the individ- Krueger argues, “a lack of civil Krueger’s argument that democ-
ual and societal causes of terrorism? The liberties seems to be a main racies suffer more terrorist
book’s great strength is its focus on new cause of terrorism around the world.” attacks than autocracies because democratic
sources of data examined in new ways. Second, democracies are more often the vic- leaders are more responsive to terrorism, mak-
Somewhat less satisfying are the conclusions tims of terrorism than autocracies. The reason, ing democracies attractive targets. Other
drawn from the evidence. Krueger seems Krueger suggests, is that democratic leaders scholars offer a different interpretation: the
overly confident that correlations in the data are more responsive than autocratic leaders to empirical relationship between regime type
have simple causal interpreta- and terrorism is spurious and actu-
tions. As a result, although the ally reflects systematic underre-
book makes real contributions porting of terrorist incidents in
to our understanding of the nondemocracies (2). If they are
empirical landscape of terror- correct, this calls Krueger’s theo-
ism, I remain skeptical of retical inference into question.
the author’s inferences and Critiques with more substantial
policy conclusions. policy implications can be made of
The most compelling analy- other of Krueger’s arguments. As
sis in the book is of biographi- I have discussed elsewhere (3),
cal information on operatives Krueger’s important observation
from Hezbollah and Hamas. that terrorist operatives are neither
This is a substantial contribu- poor nor poorly educated does not
tion, offering insight into who justify his conclusion that socio-
becomes a terrorist and, as economic factors are irrelevant for
important, pushing terrorism terrorist mobilization. As Krueger
studies in a productive new Terror in the streets. This depiction of a bomb exploding on Paris’s Avenue de la himself notes, terrorist organiza-
direction, toward microlevel Republique appeared in the February 1905 issue of Le Petit Journal. tions screen potential recruits,
data. Not surprisingly, these preferring educated candidates
data yield Krueger’s most provocative results: public opinion, making terrorism—a tactic because they are more effective in carrying out
Terrorist operatives are neither poor nor poorly designed to create mass panic—more effective difficult assignments (4). To see the problem
educated. Rather, their economic and educa- in democracies. this creates for Krueger’s logic, suppose that
tional statuses tend to lie around, or even Krueger concludes that alleviating poverty terrorist organizations accept recruits only
slightly exceed, the averages in their societies. is unlikely to reduce terrorism and that coun- over some competence threshold and that, as
Moreover, terrorists are not especially likely to terterrorism operations that violate civil liber- suggested by the data, competence is posi-
emerge from the world’s poorest countries. ties may be counterproductive. “The impor- tively correlated with income or education.
Following 9/11, many policy-makers took tance of guaranteeing civil liberties has been Suppose, further, that economic downturns
as self-evident that poverty and ignorance underemphasized as a means of prosecuting increase mobilization (perhaps by decreasing
were at the root of terrorism. Krueger quotes the war on terrorism and the war in Iraq,” he opportunity costs). In such a world, because of
President Bush: “We fight against poverty argues. Krueger also suggests that terrorism screening, the terrorists actually observed will
because hope is an answer to terror.” The “only matters in a big way if we let it matter.” be neither poor nor poorly educated, just as in
book provides a valuable service in dispelling If the media and the government minimize the Krueger’s data. Yet, Krueger’s conclusion will
the stereotype of the poor, ignorant terrorist. public panic that terrorist attacks engender, not be true: the supply of acceptable operatives
And Krueger takes the argument one step fur- the negative consequences of such attacks and, therefore, the expected level of violence
CREDIT: STEFANO BIANCHETTI/CORBIS
ther, concluding, “A wealth of evidence now will be diminished. will be affected by economic factors. Of
shows that any effect of education and There are good reasons to be skeptical of course, this theoretical argument does not
poverty on terrorism is indirect, complicated, Krueger’s interpretations of his findings establish that poverty causes terrorism. But it
and probably quite weak.” and, ultimately, of his policy conclusions. does suggest that the data Krueger presents on
Ironically, most of the grounds for skepticism the socioeconomic status of terrorists do
revolve around lessons that many social scien- not entail his inference that “there is not
The reviewer is at the Harris School of Public Policy Studies,
University of Chicago, 1155 East 60th Street, Suite 108, tists learned from Krueger himself, in his path- much question that poverty has little to do
Chicago, IL 60637, USA. E-mail: bdm@uchicago.edu breaking work in labor economics on how to with terrorism.”
For similar reasons, I am not as convinced with the discovery of tion in microbial ecology
as Krueger that the data show that limited the Archaea—a fun- that continues to reverberate.
political freedoms are a root cause of terror. damental discovery Friend himself appar-
The negative correlation between political that challenged the ently developed a taste for
freedom and terrorism could be due to causal paradigm that life exploring the world of
forces that run in either direction—repression splits neatly into two microbes and quit his job as
could spark violence or violence could lead a distinct groups, one a science journalist for USA
government to repress (a point that arises in the prokaryotic and the Today in order to devote his
question-and-answer section at the end of the other eukaryotic. As full attention to the Archaea.
book). This causal uncertainty is important. In Friend so deftly ex- The book offers readers
many conflict situations, counterterrorism plains, instead there excursions through Yellow-
operations necessitate an infringement on the are three primary line- stone National Park to scuba
rights and interests of civilians. As a result, ages (or domains) of dive for hyperthermophilic
sometimes civil liberties cannot be increased evolutionary descent: microbes, into Costa Rican
in the presence of a terrorist threat without a Bacteria, Eukarya, and rainforests to collect ter-
concomitant security trade-off. Before reach- Archaea. mites that house a microbial
ing strong conclusions about how to balance The journey begins community in their gut that
such concerns, we should seek more com- in the 1960s at the may be the world’s best
pelling evidence of the causal link between University of Illinois, Hot home for extremophiles. Velikan bioreactor for degrading
political freedom and political violence. where Carl Woese, (“Giant”) geyser survived the 3 June 2007 cellulose, and on a heli-
driven by a vision of landslide that seriously damaged Kamchatka’s copter-assisted foray into
References the tremendous value Valley of the Geysers. Russia’s Valley of the Geysers.
1. S. D. Levitt, S. J. Dubner, Freakonomics: A Rogue
Economist Explores the Hidden Side of Everything that would be derived Along the way, we learn of
(Morrow, New York, 2005). from a phylogenetic tree encompassing all biotechnological applications that stem from
2. K. Drakos, A Gofas, J. Conflict Resolut. 50, 714 (2006). forms of life, developed the means to assess the these exotic microbes, including the potentials
3. E. Bueno de Mesquita, Am. J. Polit. Sci. 49, 515 (2005).
4. E. Benmelech, C. Berrebi, J. Econ. Perspect. 21(3), 223 evolutionary relatedness of microbes. (Friend to minimize our reliance on fossil fuels and to
(2007). gained an insider’s historical perspective remediate some rather nasty chemical dumps.
through conversations with many of the scien- These travelogues are sprinkled with
10.1126/science.1151192 tists featured in the book, including Woese.) We primers in microbiology and chemistry that are
learn of the combination of insight and persist- needed to fully appreciate life’s third domain.
ence that led to Woese’s discovery of the For example, while riding a submersible to
MICROBIOLOGY Archaea. Perhaps not surprisingly, serendipity view the microbial assault under way on the
played a part as well: Ralph Wolfe—the world Titanic’s hull, Friend takes the opportunity to
Life in the Really expert on methane-producing “bacteria”— explain how the vast diversity of microbes in
occupied a lab just down the hall the world’s ocean is being cataloged and how
Hard Places The Third Domain from Woese and suggested that genomic methods revealed a previously unrec-
he take a look at these unusual ognized type of photosynthesis in the seas. He
The Untold Story of
Tom Schmidt Archaea and the Future
microbes. Those methanogens also weaves into the adventure stories relevant
of Biotechnology
offered the first evidence that vignettes from the history of microbiology that
I
n the classic Microbe there was more to life than bac- set the stage for the archaeal revolution.
Hunters (1), microbiolo- by Tim Friend teria and eukaryotes. As in any It is easy to be swept along with Friend’s
gist Paul de Kruif provided Joseph Henry Press, engaging history of science, it is wild ride through the world of microbes. In his
an enthralling account of scien- Washington, DC, 2007. not just the discovery that is exuberance for explaining the pivotal roles of
CREDIT: IGOR SHPILENOK/RUSSIAN NATURE PHOTOGRAPHY/WWW.SHPILENOK.COM
tists who had devoted their 312 pp. $27.95, C$32.95. recounted; in addition, readers microbes on Earth, there are some minor
careers to pursuing the unseen ISBN 9780309102377. are offered a view into the poli- errors in details (as there would be in the first
world of microbes. His tales of tics of science. We find that edition of any textbook that tackles complex
their difficult but rewarding work that identi- Woese’s discovery of the Archaea was greeted topics), but these are easy to overlook and
fied bacteria and viruses as the causative with skepticism by many and ridicule by others, do not interrupt the excitement of the hunt for
agents of many of the medical scourges including some very influential scientists. new forms of life.
plaguing humanity inspired many current Along the way, readers meet some of the The Third Domain brings deserved ac-
researchers in the field. The Third Domain has researchers who recognized early on the dra- claim to the discovery of the Archaea as one
the potential to similarly enthrall readers and matic consequences of Woese’s discovery. of the 20th century’s most dramatic develop-
inspire future generations of microbiologists. These include the swashbuckling Karl Stetter, ments in biology. I suspect many readers
Rather than recounting discoveries about the hunter extraordinaire of microbes that prefer will be persuaded to join Friend in his
relatively few microbes that cause disease, Tim life in boiling, sulfide-rich waters, and Norman recently acquired fondness for these spectac-
Friend takes readers on a journey that begins Pace, who combined molecular phylogenetics ular microbes.
with strategies to cull DNA sequences directly
from natural communities of microbes. Pace’s Reference
The reviewer is at the Department of Microbiology and approach to exploring the microbial world 1. P. de Kruif, Microbe Hunters (Harcourt, Brace, New York,
Molecular Genetics, 6180 Biomedical and Physical 1926).
Sciences Building, Michigan State University, East Lansing, without requiring that the organisms of interest
MI 48824, USA. E-mail: tschmidt@msu.edu be maintained in cultures unleashed a revolu- 10.1126/science.1150506
W
e face a formidable gap between health care in low-income coun-
innovations in health (including tries, recent billion-dollar increases
vaccines, drugs, and strategies for in budgets for global health have
care) and their delivery to communities in the provided only limited support for
developing world. As a result, nearly 14,000 studies needed to ensure maxi-
people in sub-Saharan Africa and South Asia mum impact (9). Instead, planners
die daily from HIV, malaria, and diarrheal dis- often assume that clinical research
ease (1), even though scientific advances have findings can be immediately trans-
enabled prevention, treatment, and, in some lated into public health impact,
cases, elimination of these diseases in devel- simply by issuing “one-size-fits-
oped countries. all” clinical guidelines or best prac-
Many evidence-based innovations fail to tices without engaging in system-
produce results when transferred to commu- atic study of how health outcomes
nities in the global south, largely because vary across community settings.
their implementation is untested, unsuitable,
or incomplete. For example, rigorous studies A Framework for Research
have shown that appropriate use of insecti- Translation
cide-treated bed nets can prevent malaria (2), Realizing the need for a quantita-
yet, in 2002, fewer than 10% of children in 28 tive, scientific framework to guide
sub-Saharan African countries regularly slept health-care scale-up in developing
with this protection (3). Newer studies have countries, researchers in health,
shown that malaria incidence is decreased by engineering, and business are build-
distribution of free nets, but further ing interest in implementation
research is needed to promote cost-effective, science (10–14). Unlike routine
A doctor seeing a patient through Progresa, Mexico’s incen-
sustained access—particularly for the poor tive-based development program that targets the very poor. applied (or operations) research,
living in rural areas (4). By improving children’s growth and nutrition, it has especially which may identify and address
The same is true of strategies to prevent benefited those who lack health care. Its success in improving barriers related to performance of
mother-to-child transmission of HIV. Al- health outcomes depends on rigorous, scientific studies that specific projects, implementation
though interventions like prophylactic anti- established the effectiveness of new strategies. science creates generalizable know-
retroviral therapy and replacement feeding ledge that can be applied across set-
have worked well in hospitals and clinics, research agenda. Although randomized, con- tings and contexts to answer central questions.
increasing coverage in rural areas (where trolled experiments are the gold standard for Why do established programs lose effective-
women have limited access to clean water and testing safety and efficacy of pharmaceuti- ness over days, weeks, or months? Why do
formal health care) may require testing of cals, health delivery schemes are less likely to tested programs sometimes exhibit unintended
novel approaches, such as self-administration be subject to rigorous scientific analysis. effects when transferred to a new setting? How
of drugs (5, 6). Similarly, the scale-up of male Second, people living in poverty face a can multiple interventions be effectively pack-
circumcision, which has been shown to pro- bewildering constellation of social constraints aged to capture cost efficiencies and to reduce
tect against HIV transmission in recent clini- and health threats that make prevention and the splintering of health systems into disease-
cal trials (7), will require development of safe, treatment more difficult. They often have lim- specific programs? Answering questions like
culturally acceptable, and accessible methods ited knowledge of preventive health practices these will require analysis of biological, social,
for surgery and care (8). and insufficient or sporadic access to quality and environmental factors that impact imple-
care. Their health systems are underfinanced, mentation, both to develop and test communi-
The Implementation Research Gap underregulated, and crippled by health-worker tywide, multisector interventions that are not
Why is effective implementation, particularly shortages. Even for those with access to testable in clinical settings, and to identify how
CREDIT: INTERAMERICAN DEVELOPMENT BANK
in resource-poor countries, such an intractable care, health is routinely undermined by heavy proven clinical interventions should be modi-
problem? The reasons are complex. First, sci- pathogen loads, environmental exposures, fied to achieve sustained health improvements
entists have been slow to view implementa- inadequate sanitation infrastructure, and socio- in the “real world.” A few innovative studies
tion as a dynamic, adaptive, multiscale phe- economic barriers to behavior change. Faced have begun to appear (15).
nomenon that can be addressed through a with such challenges, it is not surprising that One example is the research program coor-
public-health professionals have found it dif- dinated with implementation of Mexico’s 1997
Division of Advanced Science and Policy Analysis, The John ficult to successfully adapt, implement, and reform of health and social services. Before
E. Fogarty International Center, U.S. National Institutes of sustain new interventions. reform, food subsidies and health care were
Health, Bethesda, MD 20892, USA. Although a few rigorous studies of imple- provided by the Mexican government, largely
*Author for correspondence. E-mail: hofmank@mail.nih. gov mentation could advance the delivery of without gains in public health and welfare.
Frustrated with poor outcomes, the govern- Emergency Plan for AIDS Relief (PEPFAR); A final imperative is for researchers to col-
ment worked with scientists to develop a multi- and the President’s Malaria Initiative. To date, laborate with developing country governments,
sector antipoverty program, Progresa, to help these programs have focused on trial-and-error nongovernmental organizations (NGOs), and
increase the uptake of existing nutrition and optimization of health services, using descrip- communities. For example, the George Wash-
health services. tive studies, process evaluations, and monitor- ington University School of Public Health and
The new initiative provided conditional ing to measure program outputs. More recently, Health Services recently announced a partner-
financial incentives for poor rural families, on they have expanded to include targeted evalua- ship with the Elizabeth Glaser Pediatric AIDS
the basis of their use of prenatal, child health, tions, which use comparison groups to infer the Foundation, to help capture opportunities
and nutritional services provided by local clin- likely impacts of interventions on community to integrate research into the delivery of
ics. Because researchers were involved in the health. Among the questions they need to HIV/AIDS prevention and treatment services
initial design, they were able to build a prospec- address are those relating to behavior change supported by the foundation (23).
tive, cluster-randomized experiment into the and HIV prevention; the effectiveness of Although implementation experiments and
program’s roll-out, revealing statistically sig- orphan care services; the risk of drug resistance computational modeling may be more com-
nificant improvements in child development as in the scale-up of antiretroviral and antimalarial plex—in terms of study design and data analy-
a result of the new initiative (16). Because these therapy; and the packaging together of inter- sis—than the monitoring and observational
and other quantitative studies showed sustained ventions for HIV/AIDS, tuberculosis, and studies currently funded by donors, any incon-
effectiveness (17), conditional cash transfers malaria. Questions that focus on health-care venience is outweighed by the profound ability
have enjoyed continuous support of the providers and systems include how pay-for- of scientifically rigorous findings to focus lim-
Mexican government, despite radical changes performance schemes impact quality and cost ited health resources and to save more lives.
in political leadership. Similar programs are of care, and how agent-based modeling of
being adopted by policy-makers throughout clinic and hospital operations can inform devel- References and Notes
Latin America. opment of human resources for health. 1. A. D. Lopez, C. D. Mathers, M. Ezzati, D. T. Jamison,
C. J. L. Murray, Eds., Global Burden of Disease and Risk
The West African Onchocerciasis Control Factors (Oxford Univ. Press, New York, 2006).
Programme (OCP) is another example of how Implementation Science for Global Health 2. C. Lengeler, “Insecticide-treated bednets and curtains for
rigorous implementation research can am- There are three additional imperatives facing preventing malaria” (Cochrane Review, update software,
plify the public health impact of proven inter- the research community. First, we must Cochrane Library, issue 4, Oxford, 2001).
3. R. Monasch et al., Am. J. Trop. Med. Hyg. 71 (suppl.), 232
ventions. This decades-long initiative has advance theoretical models and new analytic (2004).
used established vector elimination methods methods that apply to resource-poor settings. 4. A. M. Noor, A. A. Amin, W. S. Akhwale, R. W. Snow, PLoS
and communitywide drug treatment cam- This may include, for example, developing Med. 4, e255 (2007).
5. D. J. Jackson et al., AIDS 21, 509 (2007).
paigns to control the nematode parasite that frameworks for implementation that rely on 6. J. Kagaayi et al., J. Acquir. Immune Defic. Syndr. 39, 121
causes river blindness. However, the program existing social networks and markets for sus- (2005).
is unique in that it has, from the beginning, tained health-care delivery, rather than the 7. B. Auvert et al., PLoS Med. 2, e298 (2005).
8. T. C. Quinn, Curr. Opin. Infect. Dis. 20, 33 (2007).
integrated mathematical modeling into every training of health workers—a limited resource
9. W. D. Savedoff, R. Levine, N. Birdsall, When Will We Ever
aspect of implementation and ongoing opera- in most developing countries. Multiple disci- Learn? Improving Lives Through Impact Evaluation
tion (18). Modeling of strategies has enabled plines, from systems science and computer (Report of the Evaluation Gap Working Group, Center for
the OCP to package together tested interven- simulation to public health and behavioral eco- Global Development, Washington, DC, 2006).
10. M. P. Eccles, B. S. Mittman, Implement. Sci. 1, 1 (2006).
tions, without direct experimentation. It has nomics, need to be integrated. 11. D. Sanders, A. Haines, PLoS Med. 3, e186 (2006).
also helped optimize interventions to match The World Health Organization’s Special 12. D. L. Fixsen et al., Implementation Research: A Synthesis
field conditions and has enabled scientists to Programme for Research and Training in of the Literature [Florida Mental Health Institute (FMHI)
publ. no. 231, Louis de la Parte FHMI, University of South
better understand parasite transmission and Tropical Diseases (TDR) has begun to address Florida, The National Implementation Research Network,
host-vector interactions. this need, through support of collaborative Tampa, FL, 2005].
Many implementation experiments—par- research grants in implementation research 13. R. G. A. Feachem, Trop. Med. Int. Health 9, 1139 (2004).
ticularly cluster-randomized trials and agent- (19). For example, with funds from the Exxon- 14. E. A. McCarthy, M. E. O’Brien, W. R. Rodrigues, PLoS Med.
3, e304 (2006).
based models that compare the population- Mobil Foundation, TDR researchers are 15. P. Buekens, G. Keusch, J. Belizan, Z. A. Bhutta, JAMA 291,
level health impacts of different delivery currently testing the impacts of health-care 2639 (2004).
strategies—can be coupled with the planning franchising (based on a micro-enterprise busi- 16. E. Skoufias, PROGRESA and Its Impacts of the Welfare of
Rural Households in Mexico (Research report 139,
and roll-out of new programs by health min- ness model) on access to antimalarial drugs International Food Policy Research Institute, Washington,
istries, making the cost of research marginal. in Kenyan villages (20, 21). Programs like DC, 2005).
They can also be used to model the potential these should be expanded. The U.S. National 17. E. Gakidou et al., Lancet 368, 1920 (2006).
18. F. E. McKenzie, E. M. Samba, Am. J. Trop. Med. Hyg. 71
gains of health-system designs, policies, and Institutes of Health is actively soliciting inter-
(suppl.), 94 (2004).
multisector interventions that cannot be tested national research proposals for its ongoing 19. Special Programme for Research and Training in Tropical
experimentally. These approaches all require initiative in Dissemination and Implementation Diseases (TDR), www.who.int/tdr/topics/ir/default.htm.
the involvement of scientists in early planning Research in Health (22). 20. “Shopkeepers to deliver health to Africa? Trust the people,”
RealHealthNews (Global Forum for Health Research,
to ensure that research questions are incorpo- Second, we need to train a generation Geneva, May 2007).
rated into program design. of researchers who can effectively bridge the 21. Additional details re (20) available at www.cfwshops.org/
implementation gap. This will require new cur- news_exxon_mobil_foundation.html.
22. Announcement of request for proposals, http://grants.
Identifying New Research Opportunities ricula and interdisciplinary, systems-oriented nih.gov/grants/guide/pa-files/PAR-07-086.html.
Opportunities for learning about implementa- approaches. Because some features of imple- 23. Elizabeth Glaser Pediatric AIDS Foundation,
tion are particularly promising for initiatives mentation are context-specific, it also calls for www.pedaids.org/
like the Global Fund to Fight AIDS, Tuber- strengthening of research institutions in low-
culosis, and Malaria; the U.S. President’s income countries. 10.1126/science/1150009
PLANTS ANIMALS
M
ost organisms enhance and cADPR-dependent path-
fitness by coordinating PER ways are involved in gener-
PRRs
their development with ating circadian [Ca2+]i oscil-
CRY
daily environmental changes lation, do they interact with
through molecular timekeepers CCA1 each other? Dodd et al. found
CLOCK
known as circadian clocks. In that a pharmacological in-
LHY BMAL1
eukaryotes, these clocks com- hibitor (U73122 at 1 µM) of
prise interlocking loops of tran- IP3 production did not affect
scriptional feedback and protein TOC1 RORA daily [Ca2+]i oscillation.
turnover (1). This system of mul- Because IP3 concentrations
tiple connected loops increases GI? REV-ERBα were not analyzed, more
the clock’s robustness and pro- research is needed to under-
vides numerous points of input cADPR Heme stand the relative roles of
and output to the clock. Many both cADPR and IP3. In par-
Phosphoenolpyruvate carboxykinase
metabolic pathways are regulated 2+
Ca release Glucose 6-phosphatase
ticular, identification of the
by circadian clocks in plants and plant genes that encode the
animals (2, 3). Two papers in this Gluconeogenesis
enzymes that produce cADPR
Ca2+-regulated physiology
issue, Dodd et al. on page 1789 and the proteins that control
(4) and Yin et al. on page 1786 Metabolic feedback to clocks. (Left) The plant circadian clock comprises interlocking Ca2+ release by cADPR and
(5), provide evidence that clock loops of the clock components CIRCADIAN CLOCK ASSOCIATED 1 (CCA1), LATE ELON- IP3 are required to analyze
feedback mechanisms in plants GATED HYPOCOTYL (LHY), PSEUDO-RESPONSE REGULATORs (PRRs), TIMING OF CAB the functions of these sig-
EXPRESSION 1 (TOC1), and GIGANTEA (GI). The clock controls the concentration of
and animals incorporate small cADPR, which in turn regulates circadian oscillation in the cytosolic free Ca2+ concentra- naling molecules in plants.
metabolites and signaling mole- tion. (Right) In the mammalian clock, the CLOCK/BMAL1 heterodimer regulates expres- The circadian clock also
cules. This represents yet another sion of PERIOD (PER), CRYPTOCHROME (CRY), RORA, and REV-ERBα. REV-ERBα is a controls daily metabolic
complex layer of feedback regu- heme sensor that forms a transcriptional repressor complex. Heme provides feedback to homeostasis in mammals.
lation within circadian networks, the circadian clock and influences gluconeogenesis. Indeed, mice with a domi-
and how the clock maintains nant mutation in Clock, the
metabolic homeostasis in response to exter- Dodd et al. determined that cADPR gene that encodes a core clock component,
nal conditions. concentration peaks during the early hours of develop various metabolic syndromes (15).
In plant and animal cells, the concentration the day. This fluctuation was abolished in plants Many enzymes that catalyze diverse meta-
of intracellular free calcium ions ([Ca2+]i) with defective clock function, indicating that bolic reactions require heme as a cofactor.
shows a diurnal oscillation (6). Because Ca2+ the circadian clock regulates cADPR concen- The circadian clock regulates the heme meta-
is a signaling molecule in various physiologi- tration. cADPR is synthesized from nicoti- bolic pathway partly by controlling expres-
cal responses, its daily oscillation could namide adenine dinucleotide by the enzyme sion of 5-aminolevulinic acid synthase, the
encode circadian clock signaling information ADP ribosyl cyclase (10). Nicotinamide, at 10 rate-limiting enzyme in heme biosynthesis
(7, 8). Analyses in the model plant Arabi- to 50 mM concentrations, inhibited ADP ribo- (3). Yin et al. show that the circadian clock
dopsis thaliana suggest that the extracellular syl cyclase and weakened circadian [Ca2+]i may also monitor heme metabolism through
Ca2+-sensing receptor contributes to generat- oscillation in plant cells. Dodd et al. also found the clock component REV-ERBα. Heme
ing this oscillation. This pathway involves a correlation between the expression of circa- binds to REV-ERBα and regulates its function
inositol 1,4,5,-trisphosphate (IP3), which trig- dian- and cADPR-regulated genes. Moreover, by promoting its assembly with two proteins
gers Ca2+ release from intracellular stores (9). decreasing the cellular concentration of that repress transcription—nuclear receptor
In animal cells, cyclic adenosine diphosphate cADPR lengthened the period of circadian co-repressor and histone deacetylase 3 complex.
ribose (cADPR) is another signaling molecule gene expression. The authors suggest that cir- Heme suppresses the expression of genes
that induces Ca2+ release by binding to the cadian-regulated cADPR-derived Ca2+ signal- involved in gluconeogenesis in the liver.
ryanodine receptor present on intracellular ing may configure part of the feedback loop Yin et al. show that in the presence of heme,
stores (10). Although there is not yet an obvi- that controls the clock (see the figure). REV-ERBα decreased the expression of
ous ryanodine receptor counterpart in plant The results of Dodd et al. raise interesting genes encoding phosphoenolpyruvate car-
genomes, cADPR triggers [Ca2+]i increase in questions. The phytohormone abscisic acid, boxykinase and glucose 6-phosphatase, both
plants as well (11, 12). thought to lengthen the clock period (13), of which control glucose production, in
induces cADPR production (11), and cADPR human hepatoma cells. Heme also augmented
gene expression overlaps with that of genes transcriptional repression of the core clock
The authors are in the Division of Biological Sciences, controlled by abscisic acid (14). Does abscisic gene Bmal1 by REV-ERBα. Therefore, REV-
Section of Cell and Developmental Biology, University of
California, San Diego, La Jolla, CA 92093–0116, USA. acid affect the clock partly through cADPR- ERBα couples the circadian clock with glu-
E-mail: timaizumi@ucsd.edu derived signals? Also, assuming that both IP3- cose metabolism. It would be intriguing to
study whether REV-ERBα–dependent regu- provide feedback mechanisms between the 6. T. Imaizumi et al., Sci. STKE 2007, pe32 (2007).
7. C. H. Johnson et al., Science 269, 1863 (1995).
lation contributes to the transcriptional regula- circadian clock network and clock-controlled 8. J. Love et al., Plant Cell 16, 956 (2004).
tion of phosphoenolpyruvate carboxykinase metabolic pathways to maintain metabolic 9. R. H. Tang et al., Science 315, 1423 (2007).
and glucose 6-phosphatase genes in Rev- homeostasis. 10. H. C. Lee, Physiol. Rev. 77, 1133 (1997).
erbα–deficient mice. 11. Y. Wu et al., Science 278, 2126 (1997).
12. C. P. Leckie et al., Proc. Natl. Acad. Sci. U.S.A. 95, 15837
At first glance, the studies by Dodd et al. References
(1998).
1. H. Wijnen, M. W. Young, Annu. Rev. Genet. 40, 409
and Yin et al. appear unrelated. However, they (2006).
13. S. Hanano et al., Genes Cells 11, 1381 (2006).
propose that both plant and animal clocks pos- 14. J. P. Sanchez et al., Plant J. 38, 381 (2004).
2. S. L. Harmer et al., Science 290, 2110 (2000).
15. F. W. Turek et al., Science 308, 1043 (2005).
sess a mechanism for implementing cellular 3. S. Panda et al., Cell 109, 307 (2002).
4. A. N. Dodd et al., Science 318, 1789 (2007); published
signaling or redox status in the fine-tuning of Published online 15 November 2007;
online 15 November 2007 (10.1126/science.1146757).
daily transcriptional regulation. Thus, a com- 5. L. Yin et al., Science 318, 1786 (2007); published online 10.1126/science.1151360
mon theme emerges in which small molecules 15 November 2007 (10.1126/science.1150179). Include this information when citing this paper.
ATMOSPHERIC SCIENCE
Data and modeling are helping to explain what
I
n 1971, meteorologists Roland Madden oscillation. It is as yet unclear what effect this convective and planetary scales, it serves as
and Paul Julian studied weather data from has on the deep ocean. The MJO also influ- a probe into our ability to understand and
near-equatorial Pacific islands. To their ences the onset and intensity of El Niño events model the interaction of convection and
surprise, tropospheric winds, pressure, and and may underlie the very existence of the El clouds with climate. This interaction re-
rainfall oscillated with a period of about 40 to Niño–Southern Oscillation (7). mains one of the largest uncertainties in
50 days (1). The oscillation in clouds and pre- In climate models, the MJO is typically climate projections (11). The inability to
cipitation tends to be confined to the tropical weaker and moves faster than is observed. properly simulate the MJO indicates inaccu-
Indian and Pacific oceans, but the oscillation Weather prediction models cannot sustain rate treatment of the interaction between the
in winds and pressure is felt throughout the the MJO. Coupled ocean-atmosphere models scale of convection—perhaps 1 km or
tropics (see the figure). The search for a single tend to produce more real-
robust theory for this Madden-Julian Oscil- istic simulations, because
lation (MJO) continues today. the MJO interacts strongly
The MJO is not a true oscillation, in the with the upper ocean, but Suppressed convection
sense that its period varies and its appearance this coupling is not essen- EQUATOR
is episodic, but it is the largest source of trop- tial for the existence of the
Tropical cyclone
ical weather variability on subseasonal time oscillation (8, 9). Surface winds
scales, especially in the Indian and Pacific Observations show that Upward motion
oceans. On page 1765 of this issue, Matthews a wide range of scales Downward motion
et al. (2) use observations from the new Argos interact within the MJO,
system of profiling floats to reveal the deep- ranging from the scale of
ocean response to the MJO. Also in this issue, individual convective cells
Miura et al. on page 1763 report an advance in a few kilometers across and EQUATOR
modeling the MJO (3). a few hours in duration to Warm sea
Because of its large amplitude and long the 10,000-km planetary Cold sea
surface temperature
period, the MJO affects many people. It scale of the 40- to 50-day surface temperature
causes prolonged dry and wet episodes during variation (10). Similar to a
the Asian Summer Monsoon and modulates hurricane but on a much
the intensity, frequency, and location of tropi- larger scale, the release of
cal storms in the Indian, Pacific, and Atlantic latent heat in moist convec-
oceans (4, 5). The strong and persistent sur- tion drives the planetary-
face winds associated with the MJO drive scale wind variations of the EQUATOR
a large response in the upper ocean (6). MJO. The planetary wind
Matthews et al. have measured the deep ocean variations in turn provide Westerly wind burst
response to wind surges associated with the organization to the convec-
tive-scale phenomena, sup-
D. L. Hartmann is in the Department of Atmospheric pressing convection in some The Madden-Julian Oscillation. Precipitation first develops in the Indian
Sciences, University of Washington, Seattle, WA 98195, regions and enhancing it Ocean and moves eastward with a speed of about 5 m s–1. Surface winds
USA. H. H. Hendon is with the Centre for Australian in others.
Weather and Climate Research, Bureau of Meteorology, converge under the convection, and a burst of eastward surface winds fol-
Melbourne, 3001 Victoria, Australia. E-mail: dennis@ Because the MJO arises lows the passage of the heaviest rainfall. This burst is an important driver
atmos.washington.edu; h.hendon@bom.gov.au from the interaction of for ocean dynamics. Each panel is separated by ~15 days.
less—and the resolved scales of global mod- occur for grid spacing as large as 7 km, rather References
1. R. A. Madden, P. R. Julian, J. Atmos. Sci. 28, 702
els, which currently have grid points sepa- than 1 km. (1971).
rated by ~25 km for global weather forecast- Increasing the resolution of weather pre- 2. A. J. Matthews et al., Science 318, 1765 (2007).
3. H. Miura et al., Science 318, 1763 (2007).
ing models and ~100 km for climate models. diction models to 7 km would require an 4. B. Liebmann et al., J. Meteorol. Soc. Jpn. 72, 401 (1994).
Miura et al. use a global model in which increase in computing power of about a factor 5. E. D. Maloney, D. L. Hartmann, Science 287, 2002
the horizontal grid spacing is 7 km. To per- of 100, which might be achieved in less than a (2000).
6. M. C. Spillane et al., J. Phys. Oceanogr. 17, 313 (1987).
form their simulation they used the Earth decade. Thus, increasing the spatial resolution 7. M. J. McPhaden, Science 283, 950 (1999).
Simulator, a Japanese supercomputer devel- of operational models may provide a brute- 8. C. Zhang et al., Clim. Dyn. 27, 573 (2006).
9. J. L. Lin et al., J. Clim. 19, 2665 (2006).
oped for running more realistic global simula- force solution to a critical problem in weather 10. T. Nakazawa, J. Meteorol. Soc. Jpn. 66, 823 (1988).
tions (12). In the simulation, the MJO appears and climate research. In the near term, tools 11. D. Randall et al., Bull. Am. Meteorol. Soc. 84, 1547
to be sustained with realistic structure over a such as the Earth Simulator should be used to (2003).
12. See www.es.jamstec.go.jp/index.en.html.
period of 1 month. This result suggests that a better understand the scale interactions that
transition to more realistic behavior may underlie the MJO. 10.1126/science.1152502
MICROBIOLOGY
Genome sequence analyses and enzymatic
studies reveal a novel CO2 fixation cycle in
A Fifth Pathway of Carbon Fixation some autotrophic archaea.
Rudolf K. Thauer
1 Cyanobacteria
A
utotrophs are organisms that can (oxygenic photosynthesis) Autotrophic CO2 fixation pathways
grow using carbon dioxide (CO2) as 1 Calvin cycle
their sole source of carbon. Among Gram-positive bacteria 2 Reductive citric acid cycle
3 In strict anaerobes 3 Reductive acetyl-CoA pathway
them are plants, algae, cyanobacteria, purple Bacteria
4 3-Hydroxypropionate/malyl-CoA cycle
and green bacteria, and also some bacteria Proteobacteria 5 Novel 3-hydroxypropionate/4-hydroxybutyrate cycle
1 In aerobes and anaerobes
and archaea that do not obtain energy from 2 In microaerophiles and anaerobes
3 Only in strict anaerobes Crenarchaeota
light. Autotrophs generate the biomass 2 Thermoproteus (anaerobic)
on which all other organisms—including Planctomyces 5 Metallosphaera, Sulfolobus,
humans—thrive. They also play an important 3 In strict anaerobes Acidianus, Nitrosopumilus,
Archaea Crenarchaeum (microaerophilic)
role in Earth’s nitrogen and sulfur cycles. Four
2 Green sulfur bacteria ⬇ Euryarchaeota
mechanisms are known by which autotrophic (anaerobes) 3 Methanogenic archaea
organisms fix carbon (see the figure). On (strict anaerobes)
4 Green nonsulfur bacteria 3,5 Archaeoglobus
page 1782 of this issue, Berg et al. (1) de- (microaerophilic) (strict anaerobes)
scribe a fifth autotrophic CO2 fixation path-
way in archaea that may have been used by 2 Aquifex/hydrogenobacter Eukarya 1 Plants and algae (chloroplasts)
(microaerophilic) (oxygenic photosynthesis)
some of the earliest organisms on Earth.
The first autotrophic CO2 fixation path- A novel pathway of CO2 fixation found by Berg et al. (1) in Archaea. Four other pathways are known by
way was elucidated by Calvin about 50 years which autotrophic representatives of Bacteria, Archaea, and Eukarya fix carbon.
ago (2). In this pathway, CO2 reacts with a
five-carbon sugar, yielding two carboxylic this reductive citric acid cycle were worked The fourth pathway was discovered
acids, from which the sugar is regenerated in a out (5). The cycle also operates in several in the green nonsulfur bacterium Chloro-
cyclic process. The Calvin cycle operates in other groups of bacteria and archaea. flexus. Here, CO2 fixation starts with the
plants, algae, and cyanobacteria (which all Because it involves enzymes that are sensi- carboxylation of acetyl-CoA; the CO 2
perform oxygenic photosynthesis) and in tive to oxygen, this cycle is only found in acceptor is then regenerated in a cyclic
autotrophic proteobacteria, some of which do anaerobes or in organisms that tolerate oxy- process, with 3-hydroxypropionate and
not tolerate oxygen (anaerobes). The key gen only at levels below those found in air malyl-CoA as characteristic intermediates
enzyme of the cycle—RuBisCO (3)—is also (microaerophiles). At the beginning of the (7). The 3-hydroxypropionate/malyl-CoA
found in several other bacteria and some 1980s, a third pathway of autotrophic CO2 cycle appears to be restricted to Chloro-
archaea, but these either lack another enzyme fixation was found in certain Gram-positive flexus species. None of the enzymes in-
crucial for the cycle and/or there is no evi- bacteria and methane-forming archaea. In volved in this cycle are inherently sensitive
dence for autotrophic growth. these organisms, one CO2 molecule is toward oxygen; one of them is sensitive to
In 1966, Evans et al. proposed that the reduced to CO and one to methanol (bound ultraviolet-A light, which, however, does
green sulfur bacterium Chlorobium uses a to a carrier); subsequently, acetyl–coen- not reach the ecological niches in which the
second cycle for autotrophic CO2 fixation zyme A (CoA) is synthesized from CO and green bacteria thrive.
(4). It took until 1990 until all the details of methanol (6). This reductive acetyl-CoA The novel autotrophic CO2 fixation path-
pathway is also found in several other bacte- way described by Berg et al. has some of
ria and archaea. It involves one of the most the same intermediates as the 3-hydroxy-
The author is at the Max Planck Institute for Terrestrial
Microbiology, 35043 Marburg, Germany. E-mail: thauer@ oxygen-sensitive enzymes known and is propionate/malyl-CoA cycle. Succinyl-CoA
mpi-marburg.mpg.de thus only found in strict anaerobes. is also formed from acetate and 2 CO2 mol-
ecules via 3-hydroxypropionate. However, anaerobic archaea and bacteria (9, 10). After made it into the aerobic world of plants, one
the enzymes involved appear not to be phy- the emergence of oxygenic photosynthesis, reason being that it does not use enzymes
logenetically related, indicating convergent the atmospheric oxygen concentration that are inactivated by O2 or by light.
evolution. From succinyl-CoA on, the two increased slowly and the reductive acetyl-
pathways are different. CoA pathway could no longer operate in References
Berg et al. show that the novel cycle is most organisms due to the extreme oxygen 1. I. A. Berg et al., Science 318, 1782 (2007).
2. M. Calvin, Nature 192, 799 (1961).
operative in Metallosphaera growing on H2 sensitivity of one of its key enzymes. 3. RuBisCO stands for ribulose-1,5-bisphosphate carboxy-
and O2 as the energy source. The genes for Autotrophy thus had to be reinvented after lase-oxygenase.
this cycle are also present in other archaea. the major phyla had already evolved, leading 4. M. C. W. Evans, B. B. Buchanan, D. I. Arnon, Proc. Natl.
Acad. Sci. U.S.A. 55, 928 (1966).
All these organisms are either micro- to different pathways of autotrophic CO2 5. B. B. Buchanan, D. I. Arnon, Photosynth. Res. 24, 47
aerophiles or, as in the case of Archaeo- fixation in different organisms dependent on (1990).
globus, strict anaerobes. The cycle involves their genetic outfit and living conditions. 6. S. W. Ragsdale, Crit. Rev. Biochem. Mol. Biol. 26, 261
(1991).
4-hydroxybutyryl-CoA dehydratase, a radi- Lateral gene transfer helped to spread the 7. S. Herter et al., J. Biol. Chem. 277, 20277 (2002).
cal enzyme sensitive to oxygen (8). new inventions. Some were lost again. The 8. B. M. Martin et al., Proc. Natl. Acad. Sci. U.S.A. 44,
Why do different autotrophs use different reductive citric acid cycle and the 3-hydroxy- 15645 (2004).
9. G. Wächtershäuser, Chem. Biodivers. 4, 584
pathways of CO2 fixation? According to one propionate/4-hydroxybutyrate cycle could
(2007).
hypothesis, the first organisms on Earth only survive in organisms that live under 10. W. Martin, M. J. Russel, Philos. Trans. R. Soc. B 362,
were strict anaerobes and autotrophs that anaerobic or microaerophilic conditions due 1887 (2007).
used a reductive acetyl-CoA pathway very to the inherent oxygen sensitivity of the
similar to that found today in some strictly enzymes involved. Only the Calvin cycle 10.1126/science.1152209
ECOLOGY
An invading whitefly is successful because
invading males interfere with mating by native
Invasion of the Whiteflies males and invading females produce more
female offspring.
Stuart R. Reitz
I
nvasive alien species––organisms
that have become established and Asymmetric warfare. A successful invasion, such as accomplished by the B bio-
type of the sweet potato whitefly, reflects the completion of three contingent
so abundant in new geographic
stages: (i) the opportunity to enter a new geographic area, from which the
areas as to cause harm––are one of the invader (ii) must establish in the new habitat, and then (iii) spread exten-
most pressing global environmental sively enough to cause harm. Liu et al. address how biotype B of the whitefly,
concerns (1). As invasive alien species as shown here mating, has accomplished the second and third stages through
spread, they often displace indigenous interfering with mating by indigenous whitefly biotypes and increasing their
species, thus altering ecological commu- own female offspring in the presence of males of other biotypes.
nities and adversely affecting agricultural
pest management, human well-being, and The sweet potato white- success is mating interference and facilitation.
biodiversity. To successfully invade a new fly Bemisia tabaci consists of some 12 geneti- Biotype B males reduce the reproductive suc-
geographic area, a species must have the cally distinct subtypes (termed “biotypes”) dis- cess of indigenous whiteflies by readily court-
opportunity to enter that area, and then it must tributed throughout tropical and subtropical ing the indigenous females and by disrupting
become an established member of its new regions of the world (4), of which the B biotype courtships among the indigenous males and
community, from which it can spread over is considered one of the most invasive organ- females. In contrast, whereas biotype B
large geographic areas (see the figure). isms in the world (5). Although the question of females mate only with biotype B males, they
The routes for introductions of alien whether these biotypes are unique species has can facilitate their reproductive success by
species are fairly well understood. Most organ- been intensely debated (6, 7), it is clear that producing more female offspring in the pres-
isms achieve this first step in the invasion within just the past 20 years, biotype B has ence of multiple males, regardless of the addi-
CREDIT: TOM PERRING/UNIVERSITY OF CALIFORNIA, RIVERSIDE
process with the assistance of human move- become one of the world’s most damaging agri- tional males’ biotypes.
ment (2). Less well understood are the pro- cultural pests (8). As with other invasive alien Sexual interference by invaders has been
cesses enabling species to become established, species, biotype B has been transported by linked with displacements of other animal
spread, and displace indigenous species. On humans through the movement of agricultural species, such as between species of Aedes mos-
page 1769 of this issue, Liu et al. (3) provide products, which has given it the opportunity to quitoes or Hemidactylus geckos (9, 10), but
unique insights into how one subtype of the invade new areas. Yet this raises the question of mating facilitation by an indigenous species
sweet potato whitefly spread through China how this biotype has been so successful as had not previously been implicated in aiding
and Australia and displaced two indigenous an invader, even in areas with indigenous the success of an invader. Although the size of
subtypes of this species. whitefly biotypes. the invading “army” is important (11), Liu et al.
By combining DNA analyses to distinguish raise the interesting possibility that relatively
the biotypes, long-term field surveys, and con- small introductions of biotype B can succeed
The author is at the Agricultural Research Service, U.S.
Department of Agriculture, Tallahassee, FL 32308, USA. trolled experimentation, Liu et al. reach the by rapidly producing female offspring, and thus
E-mail: stuart.reitz@ars.usda.gov striking conclusion that the key to biotype B contribute to its overall invasiveness.
A valuable aspect of the study by Liu et al. is Liu et al. conclude that invasions bring come at tremendous environmental and eco-
that they documented the process of establish- about intense interactions between previously nomic costs, yet understanding interactions
ment and displacement as it occurred over time geographically isolated species. In such asym- between invaders and residents will continue
in different areas within China and Australia. metric interactions, the B biotype is competi- to be necessary for more effective control of
Rarely has this approach been possible or tively superior and indigenous biotypes suffer invasive species (9).
undertaken: Invasions and displacements often more from interactions with the B biotype than
References
are not detected or studied until they are wide- the B biotype suffers from interactions with 1. D. Pimentel, et al., Ecol. Econ. 52, 273 (2005).
spread and complete. Consequently, much of the indigenous types. It still would be of inter- 2. A. K. Sakai et al., Annu. Rev. Ecol. Syst. 32, 305 (2001).
our information on these historical events is est to compare invasive populations of biotype 3. S.-S. Liu et al., Science 318, 1769 (2007); published 8
November 2007 (10.1126/science.1149887).
derived from retrospective studies, which can be B with populations in its indigenous habitats of 4. L. M. Boykin et al., Mol. Phylogenet. Evol. 44, 1306 (2007).
confounded by rapid evolutionary changes in the Middle East and Asia Minor to determine 5. International Union for the Conservation of Nature and
both invading and indigenous populations (12). whether biotype B inherently has invasive Natural Resources (IUCN), Invasive Species Specialist
Group, “100 of the World’s Worst Invasive Alien Species”
In turn, these displacements should not be characteristics, or whether populations have (www.issg.org).
regarded as total victory for the invaders. been selected for through previous invasions. 6. T. M. Perring, Crop Prot. 20, 725 (2001).
Some authors argue that invasive competitors Such questions of how invasive populations 7. P. J. De Barro, J. W. H. Trueman, D. R. Frohlich, Bull.
Entomol. Res. 95, 193 (2005).
may cause local extinctions of indigenous compare with their original source populations 8. J. K. Brown et al., Annu. Rev. Entomol. 40, 511 (1995).
species but are unlikely to cause the complete are among the most pertinent in invasion bio- 9. E. A. Dame, K. Petren, Anim. Behav. 71, 1165 (2006).
extinction of indigenous species (13). Further, logy today (16). 10. S. R. Reitz, J. T. Trumble, Annu. Rev. Entomol. 47, 435
(2002).
some invasive populations have undergone Maintaining a long-term perspective is 11. J. M. Levine, Science 288, 852 (2000).
seemingly unexplained crashes, which open important, as the results of Liu et al. show. 12. S. Y. Strauss et al., Ecol. Lett. 9, 357 (2006).
opportunities for additional changes in in- Brief snapshots of the event may not have led 13. M. A. Davis, Bioscience 53, 481 (2003).
14. D. Simberloff, L. Gibbons, Biol. Invasions 6, 161 (2004).
vaded communities (14, 15). It remains to be to the same conclusions as did their longer- 15. D. L. Strayer et al., Trends Ecol. Evol. 21, 645 (2006).
seen whether remnant populations of the term study. Clearly, invasions provide oppor- 16. P. Alpert, Biol. Invasions 8, 1523 (2006).
indigenous biotypes exist and may respond tunities for dramatic ecological and evolution-
evolutionarily to the invasive biotype B. ary experimentation. Unfortunately, invasions 10.1126/science.1152124
GEOLOGY
Mudstones can be deposited under
more energetic conditions than widely
On the Accumulation of Mud assumed, requiring a reappraisal of many
geologic records.
Joe H. S. Macquaker and Kevin M. Bohacs
O
n page 1760 of this issue, Schieber et al.
(1) document a mechanism for de- tling (wavy vertical arrows) (top) and the advective
positing mud that is at odds with sediment transport processes close to the sedi-
perceived wisdom. Geoscientists tend to ~5 mm ment-water interface (wavy close-to-horizontal
arrows) identified by Schieber et al. (bottom).
assume that most mud accumulates directly
Bedding planes are indicated by solid lines, laminae
from suspension in the water column, that by dotted lines. The vertical scale is exaggerated
mud deposition requires quiet bottom-water relative to the horizontal scale. In mudstone
conditions, and that mudstones containing ~5 mm successions, the expression of these two very differ-
closely spaced, parallel laminae represent ent physical processes can only be distinguished by
continuous deposition (see the first figure, top ~200 mm detailed inspection of the textures present.
panel). In contrast, the authors show that mud
can accumulate as current ripples composed deposited under still waters. Such rocks are matter, remains of organisms, and chemical
of grain aggregates under currents that can widely used to infer past climates, ocean con- precipitates formed when the sediment was
transport very fine sand (see the first figure, ditions, and orbital variations. buried. Because of their very fine grain size,
bottom panel). Thus, a layer of muddy sedi- Fine-grained sedimentary rocks such as they appear homogeneous in hand specimens;
ment can be eroded and transported laterally shales or mudstones—with an average grain moreover, their high clay content makes them
without showing obvious signs of such distur- size of less than 62.5 µm—are by far the most very susceptible to weathering. Thus, they do
bance and may record surface-water condi- common sedimentary rocks preserved close not reward casual inspection and are poorly
tions elsewhere in the basin. The results call to Earth’s surface. Most were deposited on understood relative to other rock types.
for critical reappraisal of all mudstones previ- lake or ocean floors, where they provide a Researchers typically resort to analysis of
ously interpreted as having been continuously record of Earth’s history. These rocks also play attributes such as fossil content, chemical
an important part in the global carbon budget, composition, and electromagnetic character-
J. Macquaker is in the School of Earth, Atmospheric and groundwater flow, and landfill containment istics to deduce the conditions under which
Environmental Sciences, The University of Manchester, and contribute important resources such as the mudstone was deposited.
Manchester M13 9PL, UK. K. M. Bohacs is with the oil, shale gas, minerals, and metals. Patterns of change in these proxy data are
ExxonMobil Upstream Research Company, Houston, TX
77027, USA. E-mail: Joe.Macquaker@Manchester.ac. Mudstones typically consist of various typically attributed to variations in ocean cir-
uk; Kevin.M.Bohacs@exxonmobil.com materials, including clays, quartz, organic culation, water chemistry, plankton growth,
E
ukaryotic RNA polymerase II, the Chapman et al. on page 1780 (5) and by
The laboratory investigations reported by enzyme that converts DNA informa- Egloff et al. on page 1777 (6), provide evi-
Schieber et al. now provide direct evidence of tion into RNA, couples this transcrip- dence that expands the number of potential
advective sediment transport of mud-sized tional activity to both modifying the DNA CTD phosphorylation states, supporting the
material, using apparatus designed to main- template (chromatin) and to processing nas- notion of a CTD code. Together, the papers
tain the integrity of the floccules. In the exper- cent RNA transcripts into mature forms. show that CTD phosphorylation is more com-
iments, clay aggregates formed migrating rip- Proteins that carry out the latter two functions plicated than previously thought and link, for
ples that deposited sediment under much are tethered to the catalytic core of poly- the first time, expression of specific genes
higher current velocities than previously merase II by a flexible carboxyl-terminal with a distinct CTD phosphorylation pattern.
assumed. These floccule ripples have low domain (CTD) that harbors tandem repeats of CTD heptapeptides are tandemly repeated
crests (2 to 20 mm) and very long spacings the consensus amino acid sequence Tyr1-Ser2- from 17 to 52 times in different eukaryotes and
(300 to 400 mm); they deposit nonparallel Pro3-Thr4-Ser5-Pro6-Ser7 (1–3). Actively tran- these sequences are modified by phosphoryla-
inclined laminae that could be easily misinter- scribing polymerase II is phosphorylated on tion, glycosylation, and proline isomerization
preted as parallel-laminated. different sites within this heptapeptide (2, 3). In principle, CTD modification could
Together, these studies indicate that many sequence, and the pattern of phosphorylation dictate many aspects of polymerase II function
of our preconceptions about fine-grained has been proposed as a code that controls the including assembly of the multisubunit enzyme,
rocks are naïve. First, mud accumulation can binding of different regulatory factors to the its transport to the nucleus, its localization either
occur in higher-energy conditions than most enzyme (4). Two papers in this issue, by on the DNA template or within subnuclear
researchers had assumed. Second, Schieber domains, and its eventual destruction.
et al. suggest that advective traction currents Most work to date has focused on the role
The author is in the Department of Molecular Biology and
commonly erode, transport, and deposit sub- Genetics, Johns Hopkins Medical School, Baltimore, MD of CTD phosphorylation during transcription.
stantial volumes of fine-grained sediment; as a 21205, USA. E-mail: jcorden@jhmi.edu The pattern of phosphorylation is established
by the balanced activities of enzymes that tion of this serine to alanine does not reduce identified but is presumed to be part of the
phosphorylate (kinases) and dephosphorylate gene expression. In contrast, Egloff et al. show transcription complex that drives expression of
(phosphatases) the CTD (3). Earlier work that serine-7 is required for expression of the small nuclear RNA genes. The requirement for
showed that serine-2 and serine-5 are phospho- U2 small nuclear RNA gene in mammalian serine-7 phosphorylation is the first example
rylated (7). More recent studies have shown cells. These data are consistent with earlier of a specifically modified form of polymerase
that serine-5 is phosphorylated when the poly- work showing that distal CTD repeats—which II involved in expressing a particular type of
merase passes through the 5′ end of a gene, are degenerate and include lysine or threonine gene, and is the strongest evidence yet for a
whereas serine-2 phosphorylation is promi- at position 7 (1)—are less effective at directing gene-specific CTD code.
nent when the enzyme reaches the gene’s 3′ U2 processing relative to the proximal repeats The CTD may be more broadly involved in
end (8). When polymerase II is in the middle of (9). In the Egloff et al. study, mutation of ser- gene-specific regulation. For example, a large
a gene, both serine-2 and serine-5 are phos- ine-7 to alanine does not block recruitment of number of unexpressed human protein-coding
phorylated. Capping enzymes that modify the polymerase II to genes, but blocks the process- genes contain an engaged polymerase II at their
5′ end of nascent RNA polymerase II ing of nascent RNA transcripts. Moreover, the 5′ end (11). Although the state of CTD phos-
transcripts bind to phosphorylated serine-5 authors show that the integrator complex, phorylation at these inactive genes was not
repeats, whereas RNA cleavage and poly- which is required for 3′-end processing of determined, these genes showed evidence of
adenylation factors prefer phosphorylated ser- small nuclear RNAs (10), binds specifically to transcription initiation. It is possible that regu-
ine-2 repeats near the 3′ end of RNA (3). phosphorylated serine-7 in the CTD. The lation of CTD phosphorylation is required for
Chapman et al. created antibodies that rec- kinase that phosphorylates this residue when polymerase II to proceed along the DNA tem-
ognize these and other forms of phosphoryl- polymerase II is on the U2 gene has not been plate beyond a promoter-proximal block; poly-
ated CTD. The most surprising result indi- merase activation may occur through pro-
cates that serine-7 is phosphorylated on moter-specific recruitment of appropriate
actively transcribing polymerase II, increas- CTD kinases to act on the CTD. Another possibility
ing the number of possible heptapeptide ser- RNA polymerase is that the CTD code could in some cases be
II
ine-phosphorylation states from four to eight linked to the histone code, which also regulates
(see the figure). If each individual heptapep- (YSPTSPS)n gene expression. For example, when poly-
repeat unit
tide repeat is independently modified in merase II passes through the middle of a gene,
human cells, this could lead to nearly 852 dif- YSPTSPS the histone methyltransferase Set2 recognizes
ferent CTD serine phosphorylation patterns. YSPTSPS repeats in the CTD containing both phosphoryl-
How many different CTD serine phospho- YSPTSPS ated serine-2 and phosphorylated serine-5 (3).
YSPTSPS 8 possible patterns of
rylation patterns are present in cells, and are serine phosphorylation Set2 methylates histone H3, and this modifica-
YSPTSPS within the repeat unit
these phosphorylated isomers functionally dis- tion recruits a histone deacetylase. The result-
YSPTSPS
tinct? Given the similarity of multiple repeats, it YSPTSPS
ing histone hypoacetylation may alter DNA
seems unlikely that kinases and phosphatases YSPTSPS conformation such that polymerase II cannot
can discriminate sufficiently to independently initiate transcription at cryptic (and potentially
modify most repeats. The pattern of modified regulatory) promoters located within a gene.
8n
repeats is thus likely to be more uniform possible serine phosphorylation patterns The biological role of CTD phosphoryla-
depending on which kinase or phosphatase is within the CTD tion remains to be fully elucidated, but the
brought close to the CTD. Chapman et al. pro- More pattern complexity from other
emerging picture is that the pattern of CTD
vide evidence for at least two distinct popula- possible modifications in a repeat unit: phosphorylation changes during RNA synthe-
tions of polymerase II primarily phosphory- cis-trans isomerization of prolines sis, allowing dynamic modification of the
tyrosine phosphorylation
lated at either serine-2 or serine-5. What about glycosylation
DNA template and processing of the nascent
multiply phosphorylated repeats? Mutation of RNA transcript. The studies by Chapman et
serine-7 to alanine in multiple repeats reduces Higher-order pattern complexity al. and by Egloff et al. provide both the tools to
the abundance of a form of polymerase II that when multiple repeats are considered fully document CTD phosphorylation pat-
binds an antibody specific to phosphorylated terns and the best evidence to date that these
DNA
serine-5, suggesting that phosphorylation of Patterns control recruitment patterns constitute a code that intersects, at the
both residues may be linked. Intriguingly, ser- of regulatory factors most fundamental level, with the regulation of
that control polymerase activity
ine-7 mutations seem to have different effects different classes of eukaryotic genes.
on polymerase activity when they are located in
the proximal or distal repeats within the CTD, References
1. J. L. Corden, Trends Biochem. Sci. 15, 383 (1990).
suggesting that differential modification may CTD 2. A. Meinhart et al., Genes Dev. 19, 1401 (2005).
direct the functional specialization of different 3. H. P. Phatnani, A. L. Greenleaf, Genes Dev. 20, 2922
repeats within the CTD array. The antibody mRNA (2006).
4. S. Buratowski, Nat. Struct. Biol. 10, 679 (2003).
CREDIT: N. KEVITIYAGALA/SCIENCE
Fig. 1. (A) Linkages between the buildup of atmospheric CO2 and the slowing (25°C), and total alkalinity (2300 mmol kg−1). Further details of these
of coral calcification due to ocean acidification. Approximately 25% of the calculations are in the SOM. Acidity of the ocean varies by ± 0.1 pH units
CO2 emitted by humans in the period 2000 to 2006 (9) was taken up by the over the past 420,000 years (individual values not shown). The thresholds for
ocean where it combined with water to produce carbonic acid, which releases a major changes to coral communities are indicated for thermal stress (+2°C) and
proton that combines with a carbonate ion. This decreases the concentration of carbonate-ion concentrations ([carbonate] = 200 mmol kg−1, approximate
carbonate, making it unavailable to marine calcifiers such as corals. (B) Tem- aragonite saturation ~Waragonite = 3.3; [CO2]atm = 480 ppm). Coral Reef
perature, [CO2]atm, and carbonate-ion concentrations reconstructed for the past Scenarios CRS-A, CRS-B, and CRS-C are indicated as A, B, and C, respectively,
420,000 years. Carbonate concentrations were calculated (54) from CO2 atm and with analogs from extant reefs depicted in Fig. 5. Red arrows pointing
temperature deviations from today’s conditions with the Vostok Ice Core data set progressively toward the right-hand top square indicate the pathway that is
(5), assuming constant salinity (34 parts per trillion), mean sea temperature being followed toward [CO2]atm of more than 500 ppm.
exceeds 3.3 (10). Geological studies report a no- have deleterious consequences for reef ecosys- density. However, erosion could be promoted
table gap in the fossil record of calcified organisms, tems. First, the most direct response is a decreased by the activities of grazing animals such as
including reef-building corals (14) and calcare- linear extension rate and skeletal density of coral parrotfish, which prefer to remove carbonates
ous algae (15), during the early Triassic when colonies. The massive coral Porites on the Great from lower-density substrates. Increasingly
[CO2]atm increased dramatically and reached levels Barrier Reef has shown reductions in linear ex- brittle coral skeletons are also at greater risk
at least five times as high as today’s (16). Phylo- tension rate of 1.02% year−1 and in skeletal den- of storm damage (21); thus, if rates of erosion
genetic studies suggest that corals as a group sity of 0.36% year−1 during the past 16 years (20). outstrip calcification, then the structural com-
survived the Permian-Triassic extinction event (14) This is equivalent to a reduction of 1.29% year−1 plexity of coral reefs will diminish, reducing
but may have done so through forms lacking cal- or a 20.6% drop in growth rate (the product of habitat quality and diversity. A loss of struc-
cified skeletons (17, 18). Although Scleractinian linear extension rate and skeletal density) over the tural complexity will also affect the ability of
(modern) corals arose in the mid-Triassic and lived 16-year period. While at present it is not possible reefs to absorb wave energy and thereby impairs
under much higher [CO2]atm, there is no evidence to confidently attribute the observed decrease in coastal protection.
that they lived in waters with low-carbonate growth and calcification to ocean acidification, it Third, corals may maintain both skeletal growth
mineral saturation. Knoll et al. succinctly state that is consistent with changes reported in oceanic pH and density under reduced carbonate saturation
“it is the rapid, unbuffered increase in [CO2]atm and carbonate-ion concentrations. by investing greater energy in calcification. A
and not its absolute values that causes impor- Second, corals may maintain their physical likely side effect of this strategy is the diversion
tant associated changes such as reduced [CO32− ], extension or growth rate by reducing skeletal of resources from other essential processes, such
pH, and carbonate as reproduction, as
saturation of sea wa- Table 1. Rates of change in atmospheric CO2 concentration ([CO2 ]atm, ppm/100 years) and global temperature seen in chronic stress
ter” (19). The rate of (°C/100 years) calculated for the past 420,000 yr B.P. using the Vostok Ice Core data (5) and compared to changes (21), which could ul-
[CO2]atm change is over the last century and those projected by IPCC for low-emission (B1) and high-emission (A2) scenarios (8). Rates timately reduce the
were calculated for each successive pair of points in the Vostok Ice Core record by dividing the difference between two
critical given that larval output from
sequential values (ppm or °C) by the time interval between them. Rates were then standardized to the change seen
modern genotypes reefs and impair the
over 100 years. Ratios of each rate relative to the mean rate seen over the past 420,000 years are also calculated.
and phenotypes of potential for recolo-
corals do not appear [CO2]atm Ratio (relative to Temperature Ratio (relative to nization following
to have the capacity Period (ppm century−1) past 420,000 years) (°C century−1) past 420,000 years) disturbances.
to adapt fast enough
to sudden environ- Past 420,000 years (99% 0.07 + 0.223 1 0.01 + 0.017 1 Resilience and
confidence interval; n = 282) Tipping Points
mental change.
Reef-building Past 136 years (1870–2006) 73.53 1050 0.7 70
Maintaining ecologi-
corals may exhibit IPCC B1 scenario: 550 ppm 170 2429 1.8 180
cal resilience is the
at 2100
several responses central plank of any
to reduced calcifi- IPCC A2 scenario: 800 ppm 420 6000 3.4 420
strategy aiming to
at 2100
cation, all of which preserve coral reef
Fig. 3. Ecological feedback processes on a coral reef showing pathways of first factor has a negative (decreasing) influence on the box indicated. Green
disturbance caused by climate change. Impact points associated with ocean arrows denote positive (increasing) relationships. Over time, the levels of
acidification (e.g., reduced reef rugosity, coralline algae) are indicated by the factors in hexagonal boxes will increase, whereas those in rectangular boxes
blue arrows, and impact points from global warming (e.g., bleached and will decline. Boxes with dashed lines are amenable to local management
dead corals) by the red arrows. Boxes joined by red arrows denote that the intervention.
Fig. 5. Extant examples of reefs from the Great Barrier Reef that are used the locations photographed. (A) Reef slope communities at Heron Island.
as analogs for the ecological structures we anticipate for Coral Reef (B) Mixed algal and coral communities associated with inshore reefs
Scenarios CRS-A, CRS-B, and CRS-C (see text). The [CO2]atm and tem- around St. Bees Island near Mackay. (C) Inshore reef slope around the
perature increases shown are those for the scenarios and do not refer to Low Isles near Port Douglas. [Photos by O. Hoegh-Guldberg]
200 mmol kg−1 (aragonite saturation < 3.3) and sea coral reefs as we know them today would be ex- through their impact on coastal protection, fish-
temperatures above +2°C relative to today’s val- tremely rare at higher [CO2]atm. eries, and tourism. These consequences become
ues (Scenario CRS-C, Fig. 1). These changes will We recognize that physiological acclimation or successively worse as [CO2]atm increases, and un-
reduce coral reef ecosystems to crumbling frame- evolutionary mechanisms could delay the arrival of manageable for [CO2]atm above 500 ppm.
works with few calcareous corals (Fig. 5C). The some scenarios. However, evidence that corals and Although reefs with large communities of coral
continuously changing climate, which may not their symbionts can adapt rapidly to coral bleach- reef-related organisms persist under CRS-A and
stabilize for hundreds of years, is also likely to ing is equivocal or nonexistent. Reef-building CRS-B, they become nonfunctional under CRS-C,
impede migration and successful proliferation of corals have relatively long generation times and as will the reef services that currently underpin
alleles from tolerant populations owing to con- low genetic diversity, making for slow rates of human welfare. Climate change is likely to fun-
tinuously shifting adaptive pressure. Under these adaptation. Changes in species composition are damentally alter the attractiveness of coral reefs to
conditions, reefs will become rapidly eroding also possible but will have limited impact, as even tourists (compare Fig. 5, A and C), which is an
rubble banks such as those seen in some inshore the most thermally tolerant corals will only sustain important consideration for the many low-income
regions of the Great Barrier Reef, where dense temperature increases of 2° to 3°C above their coastal countries and developing small island states
populations of corals have vanished over the long-term solar maxima for short periods (24, 31). lying within coral reef regions. Under-resourced
past 50 to 100 years. Rapid changes in sea level However, such changes come at a loss of bio- and developing countries have the lowest capacity
(+23 to 51 cm by 2100, scenario A2) (8), diversity and the removal of important redundan- to respond to climate change, but many have
coupled with slow or nonexistent reef growth, cies from these complex ecosystems. Some studies tourism as their sole income earner and thus are at
may also lead to “drowned” reefs (36) in which have shown that corals may promote one variety risk economically if their coral reefs deteriorate
corals and the reefs they build fail to keep up of dinoflagellate symbiont over another in the (40). For instance, tourism is a major foreign ex-
with rising sea levels. relatively small number of symbioses that have change earner in the Caribbean basin and in some
The types of synergistic impacts on coral and significant proportions of multiple dinoflagellate countries accounts for up to half of the gross do-
reef-dependent organisms defined for Scenario types (38). These phenotypic changes extend the mestic product (40). Coral reefs in the United
CRS-B (Fig. 5B) will be magnified substantially plasticity of a symbiosis (e.g., by 1° to 2°C) (21) States and Australia may supply smaller compo-
for CRS-C (Fig. 5C), with probably half, and pos- but are unlikely to lead to novel, long-lived as- nents of the total economy, but still generate con-
sibly more, of coral-associated fauna becoming rare sociations that would result in higher thermal siderable income (many billions of U.S. $ per year)
or extinct given their dependence on living corals tolerances (39). The potential for acclimation even from reef visitors that are increasingly responsive
and reef rugosity (37). Macroalgae may dominate to current levels of ocean acidification is also low to the quality of reefs (41).
in some areas and phytoplankton blooms may be- given that, in the many studies done to date, coral Reef rugosity is an important element for the
come more frequent in others, as water quality de- calcification has consistently been shown to de- productivity of all reef-based fisheries, whether sub-
clines owing to the collateral impact of climate crease with decreasing pH and does not recover as sistence, industrial, or to supply the aquarium trade.
change on associated coastal areas, drying catch- long as conditions of higher acidity persist (13). The density of reef fish (32) is likely to decrease as
ments and causing episodic heavy rainfall that a result of increasing postsettlement mortality aris-
transports nutrients and sediments into coastal areas. Socioeconomic Impacts of Coral Reef Decline ing from a lack of hiding places and appropriate
Whether or not one defines the transition from The scenarios presented here are likely to have se- food for newly settled juveniles (42). Regardless of
CRS-B to CRS-C and [CO2]atm of 450 to 500 ppm rious consequences for subsistence-dependent so- future climate-change influences, the total landing
as the tipping point for coral reefs, it is clear that cieties, as well as on wider regional economies of coral reef fisheries is already 64% higher than
1
Department of Biophysics and Biophysical Chemistry,
Johns Hopkins University School of Medicine, Baltimore,
MD 21205, USA. 2Ludwig Center for Cancer Genetics and
Therapeutics, and Howard Hughes Medical Institute at the
Johns Hopkins Kimmel Cancer Center, Baltimore, MD
21231, USA. 3Graduate Program in Immunology, Johns
Hopkins University School of Medicine, Baltimore, MD
21205, USA.
Fig. 1. Overview of the p110a/niSH2 heterodimer. (A) Scheme of the domain organization. The same
*Present address: National Human Genome Research color coding is used throughout this article unless specified. Gray regions are linkers between domains.
Institute, National Institutes of Health, Bethesda, MD
The nSH2 domain of p85a, denoted by the region with orange stripes, was not traced in the final model
20892, USA.
†To whom correspondence should be addressed. E-mail: but its location in the complex was determined as described in the text. (B) Ribbon diagram of the
mamzel@jhmi.edu (L.M.A.); gabelli@jhmi.edu (S.B.G.); p110a/niSH2 heterodimer. The iSH2 ABD and iSH2 C2 contacts are boxed. (C) Ribbon diagram of the
vogelbe@jhmi.edu (B.V.) p110a/niSH2 heterodimer, alternate view.
Fig. 2. Mutations in PIK3CA identified in human cancers. (A) Distribution Asn345 mutation of C2 and the residues within iSH2 (Asp560 and Asn564)
of representative mutations within p110a. Residues mutated in cancers with which it may interact are shown. (D) Mutations in the helical domain
are shown as CPK models. The start of the cancer-associated truncation (Glu542, Glu545, and Gln546), located at the interface with nSH2 (orange
(residue 571 of p85) is shown by the red arrowhead. (B) Electron density surface). (E) Mutations of the kinase domain (Met1043 and His1047), lo-
map of Arg38 and Arg88 cancer mutations shown at the interface between cated near the C-terminal end of the activation loop, are shown in light
the ABD and the kinase domains. (C) Close-up view of the interface of the green. The part of the activation loop between residues 941 and 950
C2 domain of p110 with iSH2 of p85. The stick representation of the could not be traced (see text).
sequence identity between the two proteins (fig. but were later found not to be located at the interaction of the C2 domain with iSH2. This
S1 and fig. S3) (52). interface in a crystal structure of ABD in complex would presumably alter the regulatory effect of
Cancer-specific mutations. Cancer-associated with iSH2 (53). The effect of these mutations, p85 on p110a, rather than disrupt the interac-
mutations have been identified in the ABD, C2, however, was not evident from the structure of tion of p110a with the lipid membrane. It is
helical, and kinase domains of p110a (33). The ABD-iSH2 heterodimer. The structure of the intriguing that another mutation identified in can-
distribution of representative mutations within p110a/niSH2 reveals that both Arg38 and Arg88 cer, Glu453Gln, is also located at the interface
the p110a structure is shown in Fig. 2A. Several are located at a contact between the ABD and the between C2 and iSH2. The density for its side
of these mutations have been shown to result in kinase domains, within hydrogen-bonding dis- chain, however, is not defined well enough in the
enhanced enzymatic activity in vitro and in vivo tance (<3.2 Å) of Gln738, Asp743, and Asp746 of the structure to identify a direct interaction.
(33, 42, 43). Mutations located in different do- N-terminal lobe of the kinase domain (Fig. 2B). The helical domain contains two residues,
mains were thought to act through unrelated Mutations of Arg38 and Arg88 are likely to Glu542 and Glu545, that are frequently mutated in
mechanisms but this hypothesis was difficult to disrupt these interactions, resulting in a confor- cancers (“hot spots”). In the majority of cases,
prove in the absence of structural information. mational change of the kinase domain that alters these two residues are mutated to Lys, causing a
The structure presented here sheds light on the enzymatic activity. charge reversal. Glu542 and Glu545, as well as the
mechanisms through which these mutations may Mutations in the C2 domain were thought to less frequently mutated Gln546, are located on an
affect kinase activity. change the affinity of p110a for the lipid mem- exposed region of the helical domain (Fig. 2A).
The ABD domain mutations (in which, for brane (47). In the structure reported here, Asn345, Biochemical studies suggested that these residues
example, cysteine, histidine, and glutamine re- mutated to Lys in some cancers, is within interact with Lys379 and Arg340 of the p85 nSH2
place arginine at residue 38 and 88) Arg38Cys, hydrogen-bonding distance (2.8 Å and 3.0 Å) domain and that this interaction inhibited the ac-
Arg38His, and Arg88Gln were initially thought to of Asn564 and Asp560 of iSH2 (Fig. 2C). This tivity of the catalytic subunit (53, 55). Although
disrupt the interaction between ABD and iSH2, suggests that an Asn345 mutation may disrupt the nSH2 was included in our p110a/niSH2 protein
complex, it was not highly ordered in the crystal. (32, 56). In particular, a truncation mutant known is partly blocked from membrane interaction
A model of the complete p110a/niSH2 complex as p65 (eliminating all amino acids C-terminal to by iSH2, although it remains possible for the
was therefore created by placing the previously residue 571), leads to constitutively increased basic residues of its CBR loops (e.g. Arg349,
determined structure of the nSH2 domain of hu- PI3Ka activity. It has been proposed that residues Lys410, Arg412, Lys413, Lys416) to reach the mem-
man p85a (54) into the weak density of the final 581 to 593 constrain the location of the inhibitory brane. Further studies are required to elucidate
2Fobs – Fcalc map of p110a/niSH2, while taking nSH2 domain and that deletion of them removes the relative importance of iSH2 and C2 in lipid
into account the interactions identified biochem- such orienting constraints (57). On the basis of membrane interaction.
ically (53). In this model, nSH2 is placed close to the crystal structure of p110/niSH2, an alternative Ras activates PI3Ks by binding to the RBD of
the interface between the kinase and the helical possibility appears more likely: Truncation at their catalytic subunit. A model of Ras bound to
domain and interacts with both domains. This residue 571 might destabilize the iSH2 coiled- p110a/niSH2, built by aligning the structure of
model is fully consistent with the biochemical coil around residues 560 and 564 that make an the Ras-binding domain of p110a with the struc-
experiments of Miled et al. (53) demonstrating important contact with Asn345 of the C2 domain. ture of the p110g/Ras complex (50), shows the
that mutations at residues 542, 545, and 546 Thus, the effect of this truncation may be equiv- position of this activator protein in the complex
abrogate the inhibitory effect of nSH2 (Fig. 2D). alent to that of mutation of Asn345 of the C2 do- and its relation to the putative membrane
Two ways in which the effects of these mutations main discussed above. plane (Fig. 3B).
are communicated to the complex can be iden- Interaction with the lipid membrane. Upon The p110a/niSH2 crystal structure reveals
tified: Mutations may modify the orientation of activation, PI3Ks are recruited to the plasma the architecture of the complete catalytic sub-
nSH2 with respect to the helical and the kinase membrane, where the phosphatidylinositide sub- unit of a class IA PI3K, identifies a contact be-
domains, and by changing the interaction of the strates reside. A model of the interaction between tween the C2 domain of p110a and iSH2 domain
helical domain with nSH2, the mutations may p110g and the lipid membrane based on the of p85, and suggests a role for iSH2 in lipid
alter the relative positions of helices a11K and known location of the active site and the co- binding. It also sheds new light on the mecha-
a12K. crystal structure of p110g with Ras (50) has been nisms by which PIK3CA oncogenic mutations
His1047 in the kinase domain is another hot proposed. In this model, loops from the C2 and affect PI3Ka activity. Insights obtained from this
spot for somatic mutations in cancer. It is inter- kinase domains form the major contact sites with structure suggest new targets for the design of
esting that His1047 is mutated to Arg in the ma- the lipid membrane. When this assumed mem- isoform- or mutation-specific inhibitors for
jority of cases, yet arginine is normally present at brane plane is placed in the p110a/niSH2 struc- cancer therapeutics.
the homologous position in human p110g (fig. ture, the exposed surface of the coiled-coil of
S1). In the structure of the p110a/p85 complex, iSH2 (residues 447 to 561) forms a long rect- References and Notes
His1047 is located within helix a12K of the C- angular surface that contacts the putative plane of 1. B. Vanhaesebroeck, M. D. Waterfield, Exp. Cell Res. 253,
239 (1999).
terminal lobe of the kinase domain and is close to the membrane. This surface of iSH2, as well as 2. L. C. Cantley, Science 296, 1655 (2002).
the C-terminal end of the activation loop, possi- two loops from the kinase domain (residues 3. T. Maehama, J. E. Dixon, Trends Cell Biol. 9, 125 (1999).
bly forming a hydrogen bond with the main- 723 to 729 and 863 to 867) are rich in basic 4. B. Vanhaesebroeck, D. R. Alessi, Biochem. J. 346, 561
chain carbonyl of Leu956 within the activation residues (Lys 447, Lys 448, Arg 461, Arg 465, (2000).
loop (Fig. 2E). Mutations of His1047 most likely Arg472, Lys480, Lys530, Lys532, Arg523, Arg534, 5. B. T. Nave, M. Ouwens, D. J. Withers, D. R. Alessi,
P. R. Shepherd, Biochem. J. 344, 427 (1999).
have a direct effect on the conformation of the Arg543, Arg544, Lys551, and Lys561 of the iSH2 6. B. D. Manning, A. R. Tee, M. N. Logsdon, J. Blenis,
activation loop, changing its interaction with and Lys723, Lys729, Lys863, and Lys867 of the L. C. Cantley, Mol. Cell 10, 151 (2002).
phosphatidylinositide substrates. Another less fre- kinase domain) and are therefore well-suited for 7. S. R. Datta et al., Cell 91, 231 (1997).
quently observed mutation, Met1043Ile, is located interacting with negatively charged phospholipids 8. L. del Peso, M. González-Garcia, C. Page, R. Herrera,
G. Nuñez, Science 278, 687 (1997).
on the same helix, and we hypothesize that it (Fig. 3A). The region of iSH2 containing these 9. L. D. Mayo, D. B. Donner, Proc. Natl. Acad. Sci. U.S.A.
also exerts its effect through changes in the basic residues thus would appear to be the major 98, 11598 (2001).
activation loop. determinant of interaction with membranes, in 10. B. P. Zhou et al., Nat. Cell Biol. 3, 973 (2001).
Although alterations of p85a in cancers are agreement with the observation that iSH2 in- 11. M. A. Lawlor, P. Rotwein, Mol. Cell. Biol. 20, 8983 (2000).
12. L. Rossig et al., Mol. Cell. Biol. 21, 5644 (2001).
much less common than those of p110a, several teracts with phospholipids in vitro (58). In con- 13. M. H. Cardone et al., Science 282, 1318 (1998).
have been reported. Many of these are trunca- trast, the C2 domain, which had been thought 14. J. A. Romashkova, S. S. Makarov, Nature 401, 86 (1999).
tions or deletions starting at or near residue 571 to be the main lipid-interacting domain of p110, 15. A. Brunet et al., Cell 96, 857 (1999).
REPORTS
optical “write” pulse. After a controllable storage
Stored Light in an Optical Fiber via time, the acoustic excitation is converted back to
the optical domain by interaction with a “read”
Stimulated Brillouin Scattering pulse. The process is based on stimulated
Brillouin scattering (SBS) (13, 14) and works at
Zhaoming Zhu,1 Daniel J. Gauthier,1* Robert W. Boyd2 any wavelength where the fiber is transparent,
including the important telecommunication band
We describe a method for storing sequences of optical data pulses by converting them into long- in the near-infrared spectral region. The SBS
lived acoustic excitations in an optical fiber through the process of stimulated Brillouin scattering. process arises from electrostriction, in which a
These stored pulses can be retrieved later, after a time interval limited by the lifetime of the time-varying electric field creates a time-varying
acoustic excitation. In the experiment reported here, smooth 2-nanosecond-long pulses are stored change in density of the material system (i.e., an
for up to 12 nanoseconds with good readout efficiency: 29% at 4-nanosecond storage time and acoustic excitation). The acoustic wave modu-
2% at 12 nanoseconds. This method thus can potentially store data packets that are many bits lates the refractive index of the medium, which
long. It can be implemented at any wavelength where the fiber is transparent and can be incorporated induces both amplifying and absorbing reso-
into existing telecommunication networks because it operates using only commercially available nances in the vicinity of the applied laser
components at room temperature. frequencies. Our storage scheme relies on the
process of anti-Stokes absorption, which oc-
n information network consists of nodes degrees of freedom of a dense atomic ensemble curs efficiently when the carrier frequency
ε1 (ω = 50 cm-1)
can circumvent this limitation (9–11). Specifically,
2000 40 352
we probed coexisting phases in the vicinity of the
insulator-to-metal transition in vanadium dioxide 20 348
(VO2) at length scales down to 20 nm. This en- 0
346
1
Physics Department, University of California–San Diego,
La Jolla, CA 92093, USA. 2Abt. Molekulare Strukturbiolo-
gie, Max-Planck-Institut für Biochemie and Center for
NanoScience, 82152 Martinsried, München, Germany. 3IT
Convergence and Components Laboratory, Electronics and
Telecommunications Research Institute, Daejeon 305-350,
Korea. 4Theoretical Division and Center for Integrated
Nanotechnologies, MS B262, Los Alamos National Labora-
tory, Los Alamos, NM 87545, USA.
*To whom correspondence should be addressed. E-mail:
mumtaz@physics.ucsd.edu
Phase coexistence
5 T = 342 K B
10 Strongly correlated 8000 342.6
σ (ω ) Ω -1cm-1
Re sistance (Ω )
2
10 2000
1
A
10 0
341 342 343 344
T (K) 6000
C
Fig. 3. (A) The phase diagram of VO2 and the resistance-temperature curve
1/ τ ( ω ) cm -1
4
6
m *(ω )/m b
m*(ω
2
4
0
350 400 450 500 550
2 T (K)
0
0 1000 2000 3000 4000
Frequency (cm-1)
Fig. 4. Representations of (A) the HOMO (–4.75 eV) and (B) the LUMO (–0.722 eV) of the model system {Mg[(Ar'N)2C(NMe2)]}2 3 (Ar' is C6H3Me2-2,6).
tions (B3LYP and BP86) (25) were carried out poses of comparison with 1 and 3. In contrast to dination as judged by 1H or 13C{1H} NMR
on the model complex, {Mg[(Ar'N)2C(NMe2)]}2 those complexes, the optimized geometry of 4 ex- spectroscopy. However, a weak, transient coor-
3 (Ar' is C6H3Me2-2,6). The geometry of the op- hibits coplanar heterocycles, oriented nearly or- dination of THF cannot be ruled out in these ex-
timized structure was found to be in close agree- thogonal to the bridging, symmetrical Mg2H2 unit. periments on the basis of the results of the
ment with that in the crystal structure of 1 (i.e., Scans of the potential energy hypersurface of reaction of 2 with the carbodiimide CyNCNCy
with effectively orthogonal heterocycle planes) the less bulky model, {Mg[(HN)2C(NH2)](m-H)}2, (Cy is cyclohexyl) in toluene at –70°C (Fig. 1).
but with slightly underestimated Mg-Mg bond at density functional (B3LYP) and ab initio (MP2) This led to immediate loss of the yellow color of
lengths (with B3LYP, 2.828 Å; with BP86, levels of theory, show this conformation to be the 2 and the isolation of the magnesium magnesio-
2.839 Å) and slightly overestimated Mg-N distances global minimum (14). Moreover, there are no local amidinate complex, 5, after warming the reaction
(with B3LYP, mean = 2.102 Å; with BP86, mean = minima associated with any conformation of the mixture to 20°C (14). Presumably, this reaction
2.114 Å). Figure 4A depicts the highest occupied molecule in which the planes of the magnesium occurs via an initial coordination of one N-center
molecular orbital (HOMO) of the complex, which heterocycles are orthogonal or close to orthogonal of the carbodiimide at a magnesium center, fol-
largely comprises the metal-metal s-bonding inter- with each other. Surprisingly, the Mg...Mg sepa- lowed by a double reduction of the carbodiimide
action. The two lowest unoccupied orbitals, LUMO ration in 4 at 2.770 Å (Mg-H mean distance = and its concomitant insertion into the Mg-Mg
(Fig. 4B) and LUMO+1 (fig. S4), are almost de- 1.890 Å) is substantially shorter than in 3, despite bond of 2 (28, 29). The spectroscopic data for 5
generate (energy difference of 0.11 eV, 2.6 kcal a less pronounced metal-metal interaction (Wiberg are consistent with the solid-state structure deter-
mol−1) and predominantly encompass metal-metal bond index = 0.307). In this respect, previous the- mined by an x-ray crystallographic study (fig. S4).
p-bonding orbitals derived from metal px- and py- oretical studies have concluded that metal-metal In contrast to the nearly orthogonal Mg(Nacnac)
orbital overlaps respectively. A similar arrange- distances in hydride bridged complexes can be least squares planes in 2, these planes in 5 are
ment of frontier orbitals has been calculated for shorter than in corresponding hydride-free, metal- mutually parallel and orthogonal to the CyN-
[C6H3(C6H5)2-2,6]ZnZn[C6H3(C6H5)2-2,6] (26). metal bonded complexes (27). The results of all CNCy unit. Reaction of the carbodiimide with
The HOMO-LUMO gap in 3 (4.02 eV, 93.0 kcal calculations undertaken are fully consistent with the alternative hydride-bridged magnesium(II)
mol−1) is comparable with those calculated for both 1 (and by implication 2) being a magnesium(I) complex, [Mg(Nacnac)(m-H)]2, would not be ex-
(C5H5)MgMg(C5H5) (3.87 eV, 89.5 kcal mol−1) (5) dimer, not a hydride bridged magnesium(II) pected to give compound 5 but instead C=N bond
and [C6H3(C6H5)2-2,6]ZnZn[C6H3(C6H5)2-2,6] dimer. hydromagnesiation.
(4.25 eV, 97.6 kcal mol−1) (26). In addition, the Although 1 and 2 would be expected to be
results of a natural bonding orbital (NBO) analysis highly reducing, we have found that they do References and Notes
(B3LYP) of the Mg-Mg interaction in 3 indicate not react with dihydrogen or dinitrogen in 1. W. Kaim, B. Schwederski, Bioinorganic Chemistry:
Inorganic Elements in the Chemistry of Life - An
a high s-character, single covalent bond (93.2% toluene, even at elevated temperatures (80°C) Introduction and Guide (Wiley, Chichester, 1994),
s-, 6.0% p-, and 0.8% d-character; Wiberg bond or when irradiated with ultraviolet light (l = chapters 2 and 4.
index = 0.914), whereas the metal-ligand inter- 254 nm). The lack of reactivity of the com- 2. T. Nguyen et al., Science 310, 844 (2005); published
actions are predominantly ionic (natural charge plexes toward dihydrogen is not surprising online 22 September 2005 (10.1126/science.1116789).
3. I. Resa, E. Carmona, E. Gutierrez-Puebla, A. Monge,
for Mg, +0.82 mean, and for N, –0.97 mean). when it is considered that the closely related Science 305, 1136 (2004).
Accordingly, the molecule can be viewed as an addition of H2 to [(C5H5)MgMg(C5H5)] [to 4. Y. Xie, H. F. Schaefer III, E. D. Jemmis, Chem. Phys. Lett.
anion-stabilized Mg22+ unit, as has been dis- generate two molecules of (C5H5)MgH] has 402, 414 (2005).
cussed for other model RMgMgR systems (4–6). been calculated to be an endothermic process 5. A. Velazquez, I. Fernandez, G. Frenking, G. Merino,
Organometallics 26, 4731 (2007).
We were prompted to analyze the theoretical (4). Surprisingly, exposure of the three-coordinate 6. M. Westerhausen et al., Chem. Eur. J. 13, 6292 (2007).
hydride complex, {Mg[(Ar'N)2C(NMe2)](m-H)}2 magnesium centers in 1 and 2 to THF in C6D6 7. X. Wang, L. Andrews, J. Chem. Phys. A 108, 11511 (2004).
4, using DFT calculations (B3LYP) for pur- solutions does not lead to evidence of THF coor- 8. S. Petrie, Aust. J. Chem. 56, 259 (2003).
Activity of CeOx and TiOx that have attached a batch reactor (12) or have
capabilities for scanning tunneling microscopy
(STM) (13). High-resolution x-ray photoelectron
Nanoparticles Grown on Au(111) in the spectroscopy (XPS) spectra, probing only the
near-surface region in the oxide/gold systems
Water-Gas Shift Reaction (5, 14), were acquired at the U7A beamline of the
National Synchrotron Light Source. To prepare the
TiO2/Au(111) surfaces, Ti atoms were vapor de-
J. A. Rodriguez,1* S. Ma,1 P. Liu,2 J. Hrbek,1 J. Evans,3 M. Pérez3 posited on a gold substrate covered with NO2 at
100 K (15). The temperature was then raised to
The high performance of Au-CeO2 and Au-TiO2 catalysts in the water-gas shift (WGS) reaction 700 K and the TiNOx particles were transformed
(H2O + CO→H2 + CO2) relies heavily on the direct participation of the oxide in the catalytic process. into TiO2. STM images indicated that this meth-
Although clean Au(111) is not catalytically active for the WGS, gold surfaces that are 20 to 30% odology produces flat NPs of TiO2 exhibiting a
covered by ceria or titania nanoparticles have activities comparable to those of good WGS catalysts combination of rutile and anatase phases (15). The
such as Cu(111) or Cu(100). In TiO2-x/Au(111) and CeO2-x/Au(111), water dissociates on O NPs of ceria were prepared according to two dif-
vacancies of the oxide nanoparticles, CO adsorbs on Au sites located nearby, and subsequent ferent procedures. In the first one, labeled CeO2-I
reaction steps take place at the metal-oxide interface. In these inverse catalysts, the moderate here, alloys of CeAux/Au(111) were exposed to O2
chemical activity of bulk gold is coupled to that of a more reactive oxide. (~5 × 10−7 torr) at 500 to 700 K for 5 to 10 min
(13, 14). The CeO2 NPs grew dispersed on the
early 95% of the hydrogen supply is mechanism are still unclear. For example, the herringbone structure of Au(111) (Fig. 1A) and
TiO2/Au(111) model 0
catalysts. Transitions *CO+H2O* TS1 *CO+H*+*OH TS2
states are denoted as
TS1, TS2, and TS3. (B) HOCO*+H*
–2
Optimized structures for
the different steps of the Au(100)
WGS on TiO2/Au(111). TiO2 /Au(111)
Large yellow spheres, –4
Ti2O4 HCOO*+H*
Au; large gray spheres, HOCO*+H* TS3 *CO2+2H*
Ti; small red spheres, O;
+H TS1
3
O 2O
O 2O
*
*
2
O
2H
H
2O
TS
TS
2+
*C H
H
*C H
2+
+
*+
+
O
O
C
C
Indeed, experimental studies show that CO ad- gold substrate located nearby (bifunctional catalyst). properties of the oxide facilitate H2O dissociation,
sorbs and is chemically active on gold surfaces first All of the subsequent steps occur at an oxide-metal and we have found that this is the case for NPs of
covered with oxygen or other chemical species interface. The DF calculations show that the activa- CeO2-x, TiO2-x, MoO3-x, and ZnO1-x.
(26, 27). On a free Ti2O4 cluster or on a nonsup- tion energy for the dissociation of water on TiO2/ Previous studies indicate that overlayers of Au
ported TiO2 single chain, the dissociation of water Au(111), ~0.6 eV, is also much smaller than on can be catalytically active for the oxidation of CO,
is not difficult, and is even easier than on Cu(100) Cu(100), ~1.1 eV (11), so TiO2/Au(111) should if they are nanosized in one dimension or interact
(Fig. 4), but the reaction of the formed OH with be a better WGS catalyst than Au(100) and Cu(100), strongly with an oxide support (28). In contrast,
CO leads to the formation of a stable formate spe- as found above. The intermediate that precedes the the situation for the WGS on TiO2-x/Au(111) and
cies that prevents the production of H2 and CO2. formation of CO2 and H2 in the WGS process is a CeO2-x/Au(111) takes advantage of the moderate
The DFT calculations for the model TiO2/ HOCO species. COx species were observed experi- chemical activity of bulk gold by coupling it to
Au(111) catalyst show a system that can readily mentally on the surface of the catalysts after the that of a more reactive oxide material.
perform the WGS process (Fig. 4). The reaction WGS, and they could be simple spectators when
pathway with the minimum-energy barriers in- strongly bound to the oxide nanoparticles. References and Notes
1. J. J. Spivey, Catal. Today 100, 171 (2005).
volves the following steps: Our results imply that the high performance of 2. D. J. Suh, C. Kwak, J. H. Kim, S. Kwon, T. J. Park, J. Power
Au-CeO2 and Au-TiO2 catalysts in the WGS (4, 6) Sources 142, 70 (2005).
COgas → COads ð1Þ relies heavily on the direct participation of the 3. R. Burch, Phys. Chem. Chem. Phys. 8, 5483 (2006).
oxide-metal interface in the catalytic process. The 4. Q. Fu, H. Saltsburg, M. Flytzani-Stephanopoulos, Science
H2 Ogas → H2 Oads ð2Þ oxide helps in the dissociation of water, a reaction
301, 935 (2003).
5. X. Wang, J.A. Rodriguez, J.C. Hanson, M. Perez, J. Evans,
that extended surfaces and NPs of gold cannot J. Chem. Phys. 123, 221 101 (2005).
H2 Oads → OHads þ Hads ð3Þ
perform (11). Experiments in our laboratories have 6. J. A. Rodriguez, P. Liu, J. Hrbek, J. Evans, M. Perez,
verified that TiO2-x/Au(111) and CeO2-x/Au(111) Angew. Chem. Int. Ed. 46, 1329 (2007).
COads þ OHads → HOCOads ð4Þ 7. J. A. Rodriguez, M. Pérez, J. Evans, G. Liu, J. Hrbek,
easily dissociate water, and no decomposition of J. Chem. Phys. 122, 241101 (2005).
HOCOads → CO2,gas þ Hads ð5Þ this adsorbate is seen when no O vacancies exist 8. Q. Fu, W. Deng, H. Saltsburg, M. Flytzani-Stephanopoulos,
in the oxide nanoparticles (14). Exposure of small Appl. Catal. B: Environ. 56, 57 (2005).
9. S. Ricote et al., Appl. Catal. Gen. 303, 35 (2006).
2Hads → H2 ,gas ð6Þ coverages of TiO2 and CeO2 to CO at 575 K leads
10. T. Bunluesin, R. J. Gorte, G. W. Graham, Appl. Catal.
to the appearance of O vacancies in the oxide NPs, Environ. 15, 107 (1998).
The adsorption and dissociation of water take place and these systems become active for the dissoci- 11. P. Liu, J. A. Rodriguez, J. Chem. Phys. 126, 164705
on the oxide, whereas CO adsorbs on sites of the ation of water. For the WGS, it is critical that the (2007).
Accretion of Mudstone Beds from rent velocity and density of suspension) from tem-
porally and spatially very limited measurements in
the overlying water column (14–17). Such mea-
Migrating Floccule Ripples surements (e.g., flow velocity, sediment concen-
tration) in modern environments are commonly
Juergen Schieber,1* John Southard,2 Kevin Thaisen1 considered representative of depositional conditions
for the uppermost millimeters to decimeters of the
Mudstones make up the majority of the geological record. However, it is difficult to reconstruct the accumulating deposits. However, upon close exam-
complex processes of mud deposition in the laboratory, such as the clumping of particles into floccules. ination, modern sediments show considerable het-
Using flume experiments, we have investigated the bedload transport and deposition of clay erogeneity at the millimeter to centimeter scale
floccules and find that this occurs at flow velocities that transport and deposit sand. Deposition-prone (16), an indication that what we observe in sur-
floccules form over a wide range of experimental conditions, which suggests an underlying universal ficial sediments is not a direct response to mea-
process. Floccule ripples develop into low-angle foresets and mud beds that appear laminated after sured conditions in the overlying water column.
postdepositional compaction, but the layers retain signs of floccule ripple bedding that would be To improve on this situation, it is essential to
detectable in the rock record. Because mudstones were long thought to record low-energy conditions of conduct experiments that replicate natural con-
offshore and deeper water environments, our results call for reevaluation of published interpretations of ditions and to compare the experimental sedi-
ancient mudstone successions and derived paleoceanographic conditions. ments to the rock record.
Here, we report experimental insights into the
century ago, Henry Clifton Sorby, one of equilibrium diameter that is related to the intensity sedimentology of mudstones. In past experimental
in limited domains (24, 25), GCRMs probably the western Pacific. The lifetime of an individ- 1
School of Environmental Sciences, University of East Anglia,
have the ability to respond to a given large-scale ual MJO event is between 30 and 60 days. Norwich NR4 7TJ, UK. 2School of Mathematics, University of
forcing and restore statistical equilibrium states in Dynamically, the MJO can be interpreted as a East Anglia, Norwich NR4 7TJ, UK.
a realistic time scale, even if a coarse horizontal moist atmospheric Kelvin-Rossby wave in the *To whom correspondence should be addressed. E-mail:
resolution is used. tropics (4) and a modified Rossby wave response a.j.matthews@uea.ac.uk
Depth (m)
face wind speed changes, both heat and cool the are at ±0.15°, 0.35°, and 400
ocean mixed layer by up to 1°C in a strong MJO 1.5°C (see scale bar). 600
event (6).
800
In addition, oceanic equatorial Kelvin waves
in the central and eastern Pacific are forced by 1000
MJO wind stress anomalies (9–12). A sequence 10S 5S EQ 5N 10N
of MJO events can force a train of eastward- –0.35 0.15 1.5
propagating equatorial Kelvin waves along the
–1.5 –0.15 0.35
thermocline in the Pacific, which can trigger an
El Niño event (13, 14) such as the event of 1997–
1998 (15, 16). The MJO has a direct impact on
the ocean biosphere: The MJO-forced oceanic scends to 2000 m, ascends to the surface, surface shortwave and latent heat fluxes. Neg-
Kelvin waves modulate the surface chlorophyll measuring a vertical profile of temperature and ative OLR anomalies imply more deep clouds, a
concentration through vertical entrainment, with salinity, then descends again to its parking depth. reduction in the downward surface shortwave
implications for the fishing industry (17). Argo data have already been used to study mid- flux, and a cooling of the ocean surface. Intra-
The upper tropical ocean component of the depth circulation at high latitudes (22) and seasonal latent heat flux (evaporation) anomalies
MJO has been well documented (6–8), but the seasonal temperature variation below the ther- are mainly controlled by changes in the total
data have not been available to examine whether mocline in the Pacific (23). The 10-day temporal (climatological mean plus anomalous) surface
there is a deep tropical ocean component. The resolution provides a new opportunity to study wind speed. West of the date line, westerly sur-
deepest MJO-linked observations in the tropical the spatial variability of the deep ocean on face wind anomalies reinforce the mean west-
ocean—from the Tropical Atmosphere Ocean intraseasonal time scales. erlies there (Fig. 1A). The total wind speed will
(TAO) moored buoy network in the tropical Here, we used Argo data to reveal the oceanic increase, increasing evaporation from the ocean
Pacific—extend down to only 500 m (9). A 50- component of the MJO downward into the deep surface and cooling it. East of the date line,
day oscillation has been observed in currents Pacific, in a case study of the December 2003– westerly anomalies partially cancel the mean
down to 3000 m depth in the Indian Ocean, February 2004 MJO event. Outgoing longwave easterlies, reducing the total wind speed and
consistent with a zonally propagating Rossby radiation (OLR) was used as a proxy for precip- evaporation and providing a warming anomaly
wave (18), but these limited data have not been itation (24), as low values of OLR are indicative to the ocean. The sea surface temperature (SST)
linked to the MJO or any atmospheric surface of deep clouds and precipitation in the tropics. In response to these changes in the surface fluxes
forcing. However, the MJO can influence the the uppermost panel of Fig. 1A, which shows the is lagged by approximately one-quarter of the
deep ocean in high latitudes (19). Argo data for 10 December 2003, the positive MJO cycle, or 1 to 2 weeks (6).
Therefore, it seems plausible that the MJO OLR anomalies over the western Pacific indicate The surface shortwave and latent heat flux
may influence the deep ocean in the tropics, but reduced precipitation (dry phase of MJO) with anomalies lead to changes in the equatorial
the limited hydrographic data that exist do not easterly surface wind anomalies, and the negative western Pacific SST throughout this particular
have the temporal resolution necessary for an OLR anomalies over the eastern Indian Ocean MJO event, as clearly illustrated by the gridded
analysis of intraseasonal variability. However, indicate enhanced precipitation (wet phase of Argo temperature anomalies (24). Initially, the
this situation has begun to change because of MJO) with equatorial westerly wind anomalies. positive SST anomalies in the equatorial western
the advent of the Argo ocean observing system A further region of positive OLR anomalies over Pacific on 10 December (Fig. 1B) are due to the
(20). Argo floats have been deployed since 2000 the central Indian Ocean indicates the next dry dry MJO phase and increased downward
and are at the core of current efforts to set up a phase of the MJO. These precipitation anomalies surface shortwave flux, as well as the reduction
global ocean observing system (21). Today al- then propagate slowly eastward. The 56-day in evaporation and upward latent heat flux from
most 3000 floats are operational, providing un- period shown in Fig. 1A covers slightly more the anomalous easterlies weakening the total
precedented global coverage of the world oceans. than one full cycle of the MJO. wind speed, over the previous week. These flux
Each float drifts at a typical parking depth of The MJO exerts a thermodynamical control anomalies are still present on 10 December, and
1000 m for ~10 days. In ~2 hours, it then de- on the ocean mixed layer via changes to the a week later, on 17 December, there are still
Asymmetric Mating Interactions Drive behavioral mechanisms (2). Closely related spe-
cies often have incompletely isolated mate rec-
ognition systems conducive to reproductive
Widespread Invasion and interactions and interference (3), but rarely have
such behavioral mechanisms been isolated and
Displacement in a Whitefly tested in an experimental setting to reveal their
contribution to invasion biology (1). Here, we
combined long-term field monitoring, caged pop-
Shu-Sheng Liu,1* P. J. De Barro,2 Jing Xu,1 Jun-Bo Luan,1 Lian-Sheng Zang,1 ulation studies, and detailed behavioral observa-
Yong-Ming Ruan,1 Fang-Hao Wan3 tions to investigate the mechanisms underlying
the widespread, rapid invasion by a genetic group
The role of behavioral mechanisms in animal invasions is poorly understood. We show that asymmetric of the whitefly Bemisia tabaci (Gennadius)
mating interactions between closely related but previously allopatric genetic groups of the whitefly (Hemiptera: Aleyrodidae).
Bemisia tabaci, a haplodiploid species, have been a driving force contributing to widespread invasion The whitefly B. tabaci, a haplodiploid species,
and displacement by alien populations. We conducted long-term field surveys, caged population is a genetically diverse group including many
experiments, and detailed behavioral observations in Zhejiang, China, and Queensland, Australia, to morphologically indistinguishable populations
investigate the invasion process and its underlying behavioral mechanisms. During invasion and that differ in biological characteristics but display
displacement, we found increased frequency of copulation leading to increased production of clear geographic distributions, with indigenous
female progeny among the invader, as well as reduced copulation and female production in the
indigenous genetic groups. Such asymmetric mating interactions may be critical to determining the 1
Institute of Insect Sciences, Zhejiang University, Hangzhou
capacity of a haplodiploid invader and the consequences for its closely related indigenous organisms. 310029, China. 2CSIRO Entomology, 120 Meiers Road, In-
dooropilly, Queensland 4068, Australia. 3Institute of Plant
Protection, Chinese Academy of Agricultural Sciences, Beijing
iological invasions threaten agricultural expense of indigenous, closely related orga-
B
100081, China.
and natural systems throughout the world nisms, and insight into the causes of animal in- *To whom correspondence should be addressed. E-mail:
(1). Invasive animals often thrive at the vasions often hinges on detailed assessments of shshliu@zju.edu.cn
Fig. 1. Changes of the mean proportions of the exotic B biotype and other six locations along the east coast, where transport of vegetables
indigenous biotypes of Bemisia tabaci after introduction of B. (A) ZHJ1 and ornamental plants is frequent. (B) AN versus B on Sonchus
versus B on cotton at seven locations in Zhejiang, China, from 2004 to oleraceus at 17 locations in Queensland, Australia, from 1995 to 2005.
2006. The map covers the area 122°E to 119°E from east to west and The map covers the area 153°30´E to 142°E from east to west and 34°S to
27°30´N to 30°N from south to north. Of the seven locations, Jiande is 14°40´S from south to north. Data from the other 17 locations are not
in a western mountainous area with less transport activity relative to the depicted because of space.
c and AN indicated that neither could interbreed to when B and ZHJ1 occurred together during dis-
60 d produce fertile female offspring (14, 19). placement (Fig. 2A and fig. S1). Similar differ-
40 In both regions, the process of invasion and ences in the sex ratio between AN and B when
20 displacement agrees in general with earlier cir- each of them occurred alone, as well as a similar
0
B biotype performance as ZHJ1 biotype performance as
affected by ZHJ1 males affected by B males
B AN biotype B biotype 14 14
Copulation events
Copulation events
100 12 A a 12 C
a a a
b 10 10
80 b
% females
c 8 b 8
60 d 6 6 a
a a
40 4 4 b
b
2 2
20
0 0
0
Before During invasion and After
invasion displacement by B displacement 100 100
% female progeny
% female progeny
B a a a D
80 ab 80
Phases of invasion by the B biotype b
ab a
ab
Fig. 2. Changes in mean sex ratios in field pop- 60 60 b
ulations of the exotic B biotype and indigenous 40 40 c
biotypes before, during, and after displacement of
20 20
the indigenous biotypes by B. (A) Female ratios of
ZHJ1 and B on cotton from 2004 to 2006; for 0 0
0 1B 1Z 3B 3Z 0 1Z 1B 3Z 3B
locations, see Fig. 1. The data set includes 13
No. of added to a pair of B B No. of added to a pair of ZHJ1 ZHJ1
samples for ZHJ1 before invasion, 26 samples for
ZHJ1 and B during invasion and displacement, Fig. 3. Changes in the mean number of copulation events during the first 72 hours after emergence
and 28 samples for B after displacement. (B) Fe- and production of progeny for the first 5 days after emergence when a pair of B biotype ♂×♀ was
male ratios of AN and B on spurge from 1995 to supplemented with one or three ♂ of the B or the indigenous ZHJ1 (Z) biotype (A and B), or when a
2005; for locations, see Fig. 1. The data set includes pair of ZHJ1 biotype ♂×♀ was supplemented with one or three ♂ of the ZHJ1 or B biotype (C and D).
74 samples for AN before invasion, 66 samples for We conducted 15 to 50 replicates for each of the treatments. One-way ANOVA and LSD tests were
AN and B during invasion and displacement, and applied to each of the four data sets, and the data in (B) and (D) were transformed by arcsine square
77 samples for B after displacement. One-way root before analysis. For (A), F4,106 = 5.67, P < 0.001; for (B), F4,199 = 3.02, P = 0.019; for (C), F4,95 =
analysis of variance (ANOVA) and Fisher protected 8.02, P < 0.001; and for (D), F4,201 = 15.28, P < 0.001. Means ± SEM of the number of progeny
least significant difference (LSD) tests were applied produced by B females in the five treatments in (B) were 20.8 ± 1.5, 24.1 ± 1.5, 20.3 ± 1.4, 18.4 ±
to each of the data sets, based on proportion data 1.3, and 19.1 ± 1.7, respectively, and the means did not differ significantly (F4,199 = 2.31, P = 0.059).
transformed by arcsine square root. For (A), F3,89 = Means ± SEM of the number of progeny produced by ZHJ1 females in the five treatments in (D) were
224.14, P < 0.001; for (B), F3,280 = 81.96, P < 19.6 ± 1.9, 22.7 ± 1.7, 17.5 ± 1.6, 18.1 ± 1.7, and 17.7 ± 1.5, respectively, and the means did not
0.001. Different letters above bars indicate differ significantly (F4,201 = 1.74, P = 0.143). Different letters above bars indicate significant
significant differences; error bars indicate SD. differences; error bars indicate SE.
a
Copulation events
a
10 10 males were similar to those of ZHJ1 interacting
8 8 with B (Fig. 4, C and D). Identification of the
b ab a progeny produced using nuclear DNA markers
6 6
b detected no hybrids, demonstrating reproductive
4 4
2 2
isolation between B and ZHJ1 and between B
and AN (18). These results showed that B inter-
0 0
acting with an indigenous biotype could increase
100 100 production of female progeny by increasing its
a a a
% female progeny
B D
% female progeny
1
Centre for Mathematical Biology, Department of Mathemat-
ical and Statistical Sciences, University of Alberta, Edmonton,
AB, Canada. 2Department of Biological Sciences, University
of Alberta, Edmonton, AB, Canada. 3Biology Department,
Dalhousie University, Halifax, NS, Canada. 4Salmon Coast Fig. 1. Study area in the Broughton Archipelago (boxed area in inset), depicting pink salmon populations
Field Station, Simoom Sound, BC, Canada. from unexposed rivers (numbered circles) and exposed rivers (directly labeled within the lower rectangular
*Deceased. frame). Inferred migration routes in the Broughton Archipelago are shown by the small arrows. Salmon
†To whom correspondence should be addressed. E-mail: farms are shown by black dots and sample sites by stars. Salmon farms south of Knight Inlet are not
mkrkosek@ualberta.ca shown. Identities of the numbered (unexposed) rivers are provided in data set S1 (28).
years. The time to reach sufficient temporal rep- 29. B. Dennis, P. L. Munholland, J. M. Scott, Ecol. Monogr. Research (with nonacademic participants including the
lication to support hierarchical mixed-effects mod- 61, 115 (1991). David Suzuki Foundation, Canadian Sablefish Association,
30. J. O. Lloyd-Smith et al., Trends Ecol. Evol. 20, 511 Wilderness Tourism Association, and Finest at Sea), the
eling, say 10 generations (which equals 20 years), (2005). National Geographic Society, Tides Canada, a University
greatly exceeds the predicted time to extinction. 31. C. M. Duarte, N. Marbá, M. Holmer, Science 316, 382 of Alberta Bill Shostak Wildlife Award, the Lenfest
That is, there is a major risk associated with (2007). Ocean Program, Census of Marine Life, and a Canada
waiting for large data sets to accumulate before 32. We dedicate this paper to our coauthor, Ransom Myers, Research Chair.
who passed away before the completion of this work. We
implementing conservation policy. Industrial aqua- thank J. Volpe, J. Reynolds, L. Dill, M. Wonham, Supporting Online Material
culture is rapidly expanding to new species, B. Connors, and A. Gottesfeld for helpful comments; www.sciencemag.org/cgi/content/full/318/58571772/DC1
regions, and habitats (31), which can create A. Park for assistance in preparing data and figures; and Materials and Methods
parasite outbreaks that contribute to the decline Fisheries and Oceans Canada stock assessment scientists Figs. S1 to S3
who collected and shared data. Funding came from the Tables S1 to S3
of ocean fisheries and ecosystems. Natural Science and Engineering Research Council of Dataset S1
Canada, the Canadian Mathematics of Information
References and Notes Technology and Complex Systems National Centre of 2 August 2007; accepted 2 November 2007
1. J. B. C. Jackson et al., Science 293, 629 (2001). Excellence Network on Biological Invasions and Dispersal 10.1126/science.1148744
2. R. A. Myers, B. Worm, Nature 423, 280 (2003).
3. R. L. Naylor et al., Nature 405, 1017 (2000).
4. R. Goldburg, R. Naylor, Front. Ecol. Environ. 3, 21
5.
(2005).
I. A. Fleming et al., Proc. R. Soc. London Ser. B 267,
Habitat Split and the Global
1517 (2000).
6. J. P. Volpe, B. R. Anholt, B. W. Glickman, Can. J. Fish.
Aquat. Sci. 58, 197 (2001).
Decline of Amphibians
7. M. Krkošek, M. A. Lewis, J. P. Volpe, Proc. R. Soc. London
Ser. B 272, 689 (2005). Carlos Guilherme Becker,1,2 Carlos Roberto Fonseca,2* Célio Fernando Baptista Haddad,3
8. M. Krkošek, M. A. Lewis, A. Morton, L. N. Frazer, Rômulo Fernandes Batista,4 Paulo Inácio Prado5
J. P. Volpe, Proc. Natl. Acad. Sci. U.S.A. 103, 15506
(2006).
9. A. H. McVicar, ICES J. Mar. Sci. 54, 1093 (1997). The worldwide decline in amphibians has been attributed to several causes, especially habitat loss
10. D. J. Noakes, R. J. Beamish, M. L. Kent, Aquaculture 183, and disease. We identified a further factor, namely “habitat split”—defined as human-induced
363 (2000). disconnection between habitats used by different life history stages of a species—which forces
11. A. H. McVicar, Aquac. Res. 35, 751 (2004).
12. R. Hilborn, Proc. Natl. Acad. Sci. U.S.A. 103, 15277 forest-associated amphibians with aquatic larvae to make risky breeding migrations between
(2006). suitable aquatic and terrestrial habitats. In the Brazilian Atlantic Forest, we found that habitat split
13. A. W. Pike, S. L. Wadsworth, Adv. Parasitol. 44, 233 (2000). negatively affects the richness of species with aquatic larvae but not the richness of species with
14. A. Morton, R. Routledge, C. Peet, A. Ladwig, Can. J. Fish. terrestrial development (the latter can complete their life cycle inside forest remnants). This
Aquat. Sci. 61, 147 (2004).
15. C. R. Peet, thesis, University of Victoria (2007).
mechanism helps to explain why species with aquatic larvae have the highest incidence of
16. M. Krkošek et al., Proc. R. Soc. London Ser. B 274, 3141 population decline. These findings reinforce the need for the conservation and restoration of
(2007). riparian vegetation.
17. C. Groot, L. Margolis, Eds. Pacific Salmon Life Histories
(UBC Press, Vancouver, 1991).
mphibian populations are declining tigated the role of a further factor, which we
18.
19.
20.
A. B. Morton, R. Williams, Can. Field Nat. 117, 634
(2003).
A. Morton, R. D. Routledge, R. Williams, N. Am. J. Fish.
Manage. 25, 811 (2005).
R. J. Beamish et al., ICES J. Mar. Sci. 63, 1326 (2006).
A worldwide (1, 2). Among the factors
determining the amphibian declines are
habitat loss and fragmentation, which affect am-
define as “habitat split.”
Amphibian species with aquatic larvae typ-
ically undergo a major ontogenetic niche shift,
21. W. R. Heard, in (17), pp. 119–230. phibians just as they affect any other organisms: whereby tadpoles and adults occupy two distinct
22. W. E. Ricker, J. Fish. Res. Board Can. 11, 559 (1954). through population isolation, inbreeding, and edge habitats (11). In pristine environments, the aquat-
23. B. Dennis, M. L. Taper, Ecol. Monogr. 64, 205 (1994). effects (3–5). Another important factor is the ic habitat of the tadpoles and the terrestrial hab-
24. R. A. Myers, K. G. Bowen, N. J. Barrowman, Can. J. Fish. fungus Batrachochytrium dendrobatidis, a high- itat of the postmetamorphics grade into each
Aquat. Sci. 56, 2404 (1999).
25. B. W. Brook, C. J. A. Bradshaw, Ecology 87, 1445 ly virulent pathogen that attacks many amphib- other. However, in landscapes occupied by hu-
(2006). ian species and has been responsible for the mans, land use has often resulted in a spatial
26. F. J. Mueter, R. M. Peterman, B. J. Pyper, Can. J. Fish. decline of many populations even in undisturbed separation between remnants of terrestrial hab-
Aquat. Sci. 59, 456 (2002). environments (6, 7). Amphibians can also be itat and breeding sites (12). Adults of species
27. J. C. Pinheiro, D. M. Bates, Mixed-Effects Models in S and
S-PLUS (Springer, New York, 2004).
threatened by climate shifts (7), ultraviolet-B with aquatic larvae, in order to breed, are obliged
28. Materials and methods are available as supporting radiation (8), introduction of exotic species (9), to abandon forest remnants to reach water bodies,
material on Science Online. and agrochemical contaminants (10). We inves- and at the end of the reproductive season, both
all of these metrics are calculated on a circular 2. T. J. C. Beebee, R. A. Griffiths, Biol. Conserv. 125, 271
landscape of 15-km diameter (19). (2005).
Across the Atlantic Forest biome, habitat split 3. S. A. Cushman, Biol. Conserv. 128, 231 (2006).
was the best predictor of the species richness of 10 4. R. H. MacArthur, E. O. Wilson, The Theory of Island
Biogeography (Princeton Univ. Press, Princeton, NJ,
leaf-litter forest amphibians [simple linear re- 1967).
gression: b = –0.140 ± 0.026 (SEM), F1,10 = 5. I. Hanski, Nature 396, 41 (1998).
29.040, P < 0.001, r2 = 0.744], followed by 5 6. K. R. Lips et al., Proc. Natl. Acad. Sci. U.S.A. 103, 3165
(2006).
1 7. J. A. Pounds et al., Nature 439, 161 (2006).
Departamento de Zoologia, Universidade Estadual de 8. A. R. Blaustein, P. T. Johnson, Front. Ecol. Environ. 1, 87
Campinas, 13083-970 Campinas SP, Brazil. 2Laboratório (2003).
de Interação Animal-Planta, Universidade do Vale do Rio
0
0 10 20 30 40 50 60 70 80 90 100 9. L. B. Kats, R. P. Ferrer, Divers. Distrib. 9, 99 (2003).
dos Sinos, 93022-970 São Leopoldo RS, Brazil. 3Departa- 10. R. A. Relyea, Ecol. Appl. 15, 1118 (2005).
mento de Zoologia, Universidade Estadual Paulista Júlio de
Habitat split (%)
11. E. E. Werner, J. F. Gilliam, Annu. Rev. Ecol. Syst. 15, 393
Mesquita Filho, Cx. Postal 199, 13506-900 Rio Claro SP, Fig. 1. Effect of habitat split on species richness (1984).
Brazil. 4Secretaria Estadual do Meio Ambiente e Desen-
of leaf-litter amphibians with aquatic larvae and 12. J. B. Dunning, B. J. Danielson, H. R. Pulliam, Oikos 65,
volvimento Sustentável do Amazonas, 69050-030 Manaus 169 (1992).
AM, Brazil. 5Departamento de Ecologia, Instituto de with terrestrial development across 12 Brazilian
13. M. J. Mazerolle, A. Desrochers, Can. J. Zool. 83, 455
Biociências, Universidade de São Paulo, 05508-900 São Atlantic Forest landscapes. Habitat split is
(2005).
Paulo SP, Brazil. calculated as the percentage of the total stream 14. IUCN, Conservation International, NatureServe, Global
*To whom correspondence should be addressed. E-mail: length that does not overlap with natural forest Amphibian Assessment (www.globalamphibians.org),
cfonseca@unisinos.br cover. Linear regression lines are shown. accessed 20 May 2007.
15. D. L. Silvano, M. V. Segalla, Conserv. Biol. 19, 653 24. J. M. Hero, S. E. Williams, W. E. Magnusson, J. Zool. 267, M. Hartmann, I. Martins, and C. Oliveira for performing
(2005). 221 (2005). some of the field surveys; and J. Giovanelli and U. Kubota
16. R. A. Mittermeier et al., Hotspots Revisited: Earth’s 25. J. Carolsfeld, B. Harvey, C. Ross, A. Baer, Eds., Migratory for assistance in spatial and statistical analyses. Supported
Biologically Richest and Most Endangered Terrestrial Fishes of South America: Biology, Fisheries and Conservation by a scholarship from the Fundação de Amparo à Pesquisa
Ecoregions (Univ. of Chicago Press, Chicago, 2005). Status (IDRC Press, Victoria, BC, Canada, 2004). do Estado de São Paulo (FAPESP: 04/13132-3) (C.G.B.),
17. P. C. Eterovick et al., Biotropica 37, 166 (2005). 26. J. M. Amezaga, L. Santamaria, A. J. Green, Acta Oecol. fellowships from the Conselho Nacional de Desenvolvimento
18. V. M. Viana, A. A. J. Tabanez, J. L. F. Batista, in Tropical Forest 23, 213 (2002). Científico e Tecnológico (CNPq: 305428/2005-5, 302512/
Remnants: Ecology, Management and Conservation of 27. J. R. Mendelson III et al., Science 313, 48 (2006). 2005-5) (C.R.F. and C.F.B.H.), Programa BIOTA/FAPESP
Fragmented Communities, W. F. Laurance, R. O. Bierregaard, 28. J. A. Pounds et al., Science 314, 1541 (2006). (01/13341-3, 02/08558-6), and Universidade do Vale do
Eds. (Univ. of Chicago Press, Chicago, 1997), pp. 347–365. 29. J. R. Mendelson III et al., Science 314, 1541 (2006). Rio dos Sinos.
19. See supporting material on Science Online. 30. B. Wuethrich, Science 315, 1070 (2007).
Supporting Online Material
20. A. D. Guerry, M. L. Hunter, Conserv. Biol. 16, 745 31. We thank K. Lips, A. Pounds, C. Gascon, T. Halliday,
www.sciencemag.org/cgi/content/full/318/5857/1775/DC1
(2002). J.-M. Hero, T. Gardner, M. Almeida-Neto, T. Grant,
Materials and Methods
21. T. A. G. Rittenhouse, R. D. Semlitsch, Wetlands 27, 153 P. Eterovick, R. Loyola, A. Freitas, E. G. F. Benya, and
Fig. S1
(2007). M. F. Kersch for critically reviewing previous versions of
Table S1
22. K. R. Lips, J. D. Reeve, L. R. Witters, Conserv. Biol. 17, the manuscript; S. Stuart, J. Chanson (World Conservation
References
1078 (2003). Union–Global Amphibian Assessment), T. Halliday, and
23. R. M. Bustamante, S. R. Ron, L. A. Coloma, Biotropica 37, J. Kauffman (Declining Amphibian Populations Task Force) 17 August 2007; accepted 6 November 2007
180 (2005). for providing updated versions of their database; M. Dixo, 10.1126/science.1149374
Serine-7 of the RNA Polymerase II elongation and 3′ end processing (5, 6). No role
has yet been ascribed to Ser7.
The mammalian Pol II CTD comprises 52
CTD Is Specifically Required for repeats, 25 of which deviate from the consen-
sus at position 7. The mainly consensus repeats
snRNA Gene Expression 1 to 25 activate snRNA 3′ end processing more
effectively than repeats 27 to 52, which have
few serines at position 7 (2). In contrast, both
Sylvain Egloff,1 Dawn O’Reilly,1 Rob D. Chapman,2 Alice Taylor,1 Katrin Tanzhaus,1 halves of the CTD are equally effective in ac-
Laura Pitts,1 Dirk Eick,2 Shona Murphy1* tivating polyadenylation (7). We have tested
the requirement for Ser7 for expression of
RNA polymerase II (Pol II) transcribes genes that encode proteins and noncoding small snRNA [U2–globin (U2G) (2)] and mRNA
nuclear RNAs (snRNAs). The carboxyl-terminal repeat domain (CTD) of the largest subunit of [cytomegalovirus promoter-driven heteroge-
mammalian RNA Pol II, comprising tandem repeats of the heptapeptide consensus Tyr1-Ser2-Pro3- neous nuclear ribonucleoprotein K (pCMV-
Thr4-Ser5-Pro6-Ser7, is required for expression of both gene types. We show that mutation of hnRNPK) (8)] templates in human embryonic
serine-7 to alanine causes a specific defect in snRNA gene expression. We also present evidence kidney (HEK) 293 cells by introducing muta-
that phosphorylation of serine-7 facilitates interaction with the snRNA gene–specific Integrator tions into consensus (Con) CTD repeats in an
complex. These findings assign a biological function to this amino acid and highlight a a-amanitin–resistant Pol II large subunit (Rpb1)
gene type–specific requirement for a residue within the CTD heptapeptide, supporting the (9) (Fig. 1A and fig. S1A). The large subunit
existence of a CTD code. of endogenous Pol II is very sensitive to in-
hibition by a-amanitin, facilitating comple-
uman snRNA genes transcribed by nylated snRNAs (2). Removal of the CTD of mentation studies (9). A CTD with at least 25
1
proximal and distal sequence elements (PSE structure composed of multiple repeats contain- Sir William Dunn School of Pathology, University of Oxford,
and DSE) (1). Rather than polyadenylation ing residues that undergo reversible phospho- South Parks Road, Oxford OX1 3RE, UK. 2Institute of Clinical
signals, 3′ box elements direct the cotranscrip- rylation during transcription (5). For example, Molecular Biology and Tumour Genetics, Gesellschaft fuer
Strahlung Forschung (GSF)-Research Centre of Environment
tional formation of the primary 3′ end of tran- phosphorylation of Ser 5 by cyclin-dependent and Health, Munich Center for Integrated Protein Science
scripts (2, 3). The 3′ end of these precursor kinase 7 (CDK7) facilitates promoter release (CiPSM), Marchioninistrasse 25, 81377 Munich, Germany.
snRNAs (pre-snRNAs) is further processed in and RNA capping, whereas Ser2 phosphoryl- *To whom correspondence should be addressed. E-mail:
the cytoplasm to yield mature nonpolyade- ation by CDK9 is associated with processive shona.murphy@path.ox.ac.uk
NADH+H+
22 A comparison of the proposed 3-hydrox-
1,3-diphosphoglycerate ypropionate/4-hydroxybutyrate cycle with the
ADP
21 Calvin-Bassham-Benson cycle reveals important
ATP
3-phosphoglycerate differences. The formation of one molecule of
20 glyceraldehyde 3-phosphate from three mole-
2-phosphoglycerate cules of CO2 follows the equation: 3 CO2 + 6
19 NAD(P)H + 9 ATP → 1 triosephosphate + 6
phosphoenolpyruvate NAD(P)+ + 9 adenosine diphosphate (ADP) + 8
18
AMP+Pi inorganic phosphate (Pi). This does not account
ATP
pyruvate for the loss of energy and reducing power from the
17
2Fdox+CoASH oxygenase activity of ribulose-1,5-bisphosphate
2Fdred CO2 carboxylase-oxygenase (RuBisCO). Triosephos-
CoAS phate formation via the proposed cycle (Fig. 1)
acetyl-CoA
O follows the equation: 2 bicarbonate + 1 CO2 + 5
HCO3
-
NAD(P)H + 2 reduced ferredoxin + 6 ATP →
16
16 CoAS 1
ADP+Pi
1 triosephosphate + 5 NAD(P)+ + 2 oxidized
acetoacetyl-CoA
CoAS CoASH
acetyl-CoA
O ATP malonyl-CoA ferredoxin + 3 ADP + 4 Pi + 3 AMP + 2
CoAS O
NADH+H+ NADPH+H+ inorganic pyrophosphate (PPi). Hence, in ener-
O O
NAD
+ 15 O OH 2 NADP++CoASH getic terms, the two processes are comparable
CoAS
malonate semialdehyde [because ATP cleavage to AMP is equivalent to
O OH O
3-hydroxybutyryl-CoA NADPH+H+
the loss of two energy-rich compounds, and
14
O OH 3
+
reduced ferredoxin has a stronger reduction
NADP
CoAS
3-hydroxypropionate O
potential than NAD(P)H], but oxygenase activ-
O ity of RuBisCO renders the Calvin-Bassham-
crotonyl-CoA OH OH
ATP+CoASH Benson cycle energetically inferior.
13 OH 4 The active “CO2” species is CO2 in the Calvin-
AMP+PPi
CoAS
3-hydroxypropionyl-CoA Bassham-Benson cycle, whereas it is bicarbonate
4-hydroxybutyryl-CoA O
O as cosubstrate for acetyl-CoA/propionyl-CoA carbo-
AMP+PPi OH SCoA xylase in the 3-hydroxypropionate/4-hydroxybutyrate
12 5
ATP+CoASH
OH cycle, with CO2 as cosubstrate for pyruvate synthase
HO acryloyl-CoA
4-hydroxybutyrate
O (Fig. 1). The turnover number of RuBisCO
O
+
SCoA (average: 5 s−1) reflects a low catalytic efficiency
NADP
11 O 6
NADPH+H+ that requires large amounts of enzyme (21, 22).
NADPH+H+
HO propionyl-CoA NADP+ M. sedula acetyl-CoA/propionyl-CoA carboxyl-
succinate semialdehyde O
O ATP
ase catalyzing both carboxylation reactions has a
+ O OH
SCoA turnover number at 65°C of 28 s−1 (19). The
NADP 10 O 7 -
NADPH+H +
HO
HCO3 Michaelis constant (Km) value of RuBisCO for
O ADP+Pi
SCoA 8 dissolved CO2 [the average value is 0.05 mM,
9
O succinyl-CoA SCoA
methylmalonyl-CoA but it may be as high as 0.34 mM in some marine
cyanobacteria (21)] is lower than or even
Fig. 1. Proposed autotrophic 3-hydroxypropionate/4-hydroxybutyrate cycle in M. sedula. Reactions comparable to the apparent Km value of archaeal
of the cycle are shown. Enzymes: 1, acetyl-CoA carboxylase; 2, malonyl-CoA reductase (NADPH); 3,
acetyl-CoA/propionyl-CoA carboxylase for bi-
malonate semialdehyde reductase (NADPH); 4, 3-hydroxypropionyl-CoA synthetase (AMP-forming); 5, 3-
hydroxypropionyl-CoA dehydratase; 6, acryloyl-CoA reductase (NADPH); 7, propionyl-CoA carboxylase; 8, carbonate [0.3 mM (19)]. However, the CO2
methylmalonyl-CoA epimerase; 9, methylmalonyl-CoA mutase; 10, succinyl-CoA reductase (NADPH); 11, concentration in water equilibrated with air (1
succinate semialdehyde reductase (NADPH); 12, 4-hydroxybutyryl-CoA synthetase (AMP-forming); 13, 4- atm pressure, 20°C, 370 parts per million CO2) is
hydroxybutyryl-CoA dehydratase; 14, crotonyl-CoA hydratase; 15, 3-hydroxybutyryl-CoA dehydrogenase 0.012 mM at pH 7.4 (which is the assumed
(NAD+); 16, acetoacetyl-CoA b-ketothiolase. The proposed pathway of glyceraldehyde 3-phosphate intracellular pH), and the bicarbonate concentra-
synthesis from acetyl-CoA and CO2 is also shown. Enzymes: 17, pyruvate synthase; 18, pyruvate, water tion under the same conditions is 0.26 mM. The
dikinase [phosphoenolpyruvate (PEP) synthase]; 19, enolase; 20, phosphoglycerate mutase; 21, 3- concentration of bicarbonate will be even higher
phosphoglycerate kinase; 22, glyceraldehyde 3-phosphate dehydrogenase. The activities of pyruvate at pH 7.8 to 8.2 of seawater (apparent dissociation
synthase and PEP synthase at 75°C were 10 to 25 nmol min−1 mg−1 protein (6) and 25 nmol min−1 mg−1 constant pKapp for CO2/HCO3– is 6.3, 20°C).
protein, respectively. Thus, the acetyl-CoA carboxylase affinity for the
active “CO2” species appears not to be inferior to cell. There is no additional clue from the genome although these genera lack the genes required for
that of RuBisCO. In addition, in volcanic gases as to how these Crenarchaeota protect one of part 1 of the proposed pathway. I. hospitalis forms
and in animal hosts, the CO2 concentration is their key enzymes of CO2 fixation from oxygen succinyl-CoA from acetyl-CoAvia pyruvate, phos-
much higher than in ambient air. Although 4- inactivation. phoenolpyruvate, and oxaloacetate (23) and may
hydroxybutyryl-CoA dehydratase is slowly in- The 4-hydroxybutyryl-CoA dehydratase gene use the second half of the 3-hydroxypropionate/4-
activated by oxygen, it may be sufficiently stable was not found in heterotrophic Crenarchaea, yet hydroxybutyrate cycle for the regeneration of
at low oxygen tensions to maintain activity, it is present in the genomes of autotrophic the CO2-acceptor acetyl-CoA from succinyl-CoA.
especially in the protected environment of the Ignicoccus and Pyrobaculum spp. (table S1), Pyrobaculum spp. use a reductive citric acid cycle
for CO2 fixation, which results in acetyl-CoA 4-Hydroxybutyryl-CoA dehydratase was orig- The number of identified 4-hydroxybutyryl-CoA
formation from citrate (6); however, pyruvate syn- inally described in a few strict anaerobes that use dehydratase gene sequences in the GOS database is
thase activity appears to be lacking in autotroph- it in fermentation (15, 25). These strictly anaer- comparable with that of the gene of RuBisCO large
ically grown cells (24). This enzyme is normally obic Bacteria form a separate “anaerobe cluster” subunit (344 specific genes, including 26 complete
responsible for the reductive carboxylation of in the 4-hydroxybutyryl-CoA dehydratase phy- genes and 318 fragments). This indicates that a
acetyl-CoA to pyruvate in autotrophic anaerobes. logenetic tree (Fig. 3). Two independent clusters group of abundant mesophilic autotrophic Crenar-
In the absence of pyruvate synthase, the second are formed by hyperthermophilic Crenarchaea that chaea in the sea (28–30) may use the proposed 3-
half of the proposed cycle may be used in the are unable to ferment, with type 1 being more com- hydroxypropionate/4-hydroxybutyrate pathway for
reverse direction to assimilate two molecules of mon than type 2. Another cluster is associated with CO2 fixation; yet, such comparisons depend on the
acetyl-CoA into succinyl-CoA, to give a modified mesophilic Crenarchaea such as Cenarchaeum sp., cloning efficiency of the required genes. Because
reductive citric acid cycle. Several heterotrophic a member of the “marine group”–1 Crenarchaeota, these Crenarchaea probably use ammonia as an elec-
Thermococcales and Halobacteriales harbor the as well as with many marine environmental meta- tron donor (12, 20, 30), their contribution to the
characteristic genes for the first part of the cycle but genomes from the Global Ocean Sampling (GOS) carbon cycle should be much lower than that of
lack those for the second part (table S1). Because database (26, 27). The Basic Local Alignment phototrophs [~1% of annual marine production (29)].
their genomes appear to lack the genes for isocitrate Search Tool (BLAST) search identified 189 specific It should be stressed that, in other Archaea,
lyase and malate synthase, which are key enzymes genes (18 complete genes and 171 fragments) of 4- not all individual reactions of the proposed cycle
of the glyoxylate cycle, these organisms may thus hydroxybutyryl-CoA dehydratase in the GOS data- may be catalyzed by the same kind of enzyme.
use the first part of the cycle for the assimilation of base, most of which (84%) group in the “marine For instance, various alcohol dehydrogenases,
acetyl-CoA, instead of the glyoxylate cycle, as well cluster”–1 (Fig. 3). It is unlikely that the bearers of aldehyde dehydrogenases, acyl-CoA synthetases,
as for propionate assimilation. this gene conduct fermentation in the oxic seawater. or enoyl-CoA hydratases may fulfill the same
C
Chromosoma 113, 103 (2004).
2. S. M. Reppert, D. R. Weaver, Annu. Rev. Physiol. 63, 647 daily rotation of the planet. In plants and ular clocks with multiple feedback loops (4–6).
(2001).
3. P. L. Lowrey, J. S. Takahashi, Annu. Rev. Genomics
cyanobacteria, benefits occur when the We tested the hypothesis that plant circadian os-
Hum. Genet. 5, 407 (2004). clock is resonant with the environment (1–3). cillators also incorporate cytosolic signaling mol-
4. A. Kohsaka, J. Bass, Trends Endocrinol. Metab. 18, 4 (2007). This requires the oscillator to be robust yet flex- ecules because there are circadian rhythms in the
Microliter Accessories expected to be crucial to understanding the role of easily removed disposable reactor from the
The nanoVette microliter accessory for DU 730 genetic variation in health and disease. Activo-P11 peptide synthesizer. In this way, the
and DU 800 UV/Vis Spectrophotometers is suit- Applied Biosystems For information peptide synthesizer can be maintained in the
able for DNA and protein applications. The +44 (0) 1494 816062 www.appliedbiosystems.com open lab while cleavage and deprotection proce-
cuvette-sized nanoVette accepts sample sizes as dures can be performed simply, speedily, and
small as 0.7 µl and is offered with interchange- Phosphatase Substrate Systems safely on the P12 in the fume hood.
able 0.2 mm and 1 mm pathlength lids. The RedPhos Microwell Phosphatase Substrate Activotec For information +44 1223 260008
Designed for precise fit in the Beckman Coulter System is a sensitive new colorimetric phos- www.activotec.com
spectrophotometers, the nanoVette can be phatase for microwell assays that can detect less
loaded and cleaned without being removed from than 0.5 pg of phosphatase. The color produced Dispensing Pump
the instrument, saving time and maximizing is stable, linear over a wide dynamic range, and The Furon Precision Dispense Pump (DPD) makes
throughput. The sample can also be recovered generates a strong red color that is easily read by use of cutting-edge technology to deliver
for future analysis. The DU 730 includes eye. The RedPhos Membrane Phosphatase Sub- extremely accurate doses of media with unprece-
advanced tools for protein and nucleic acid strate is suitable for immunoblotting and dot dented repeatability. Patented PTFE rolling
analysis, including determination of dye incor- blot procedures. It produces a strong red reaction diaphragm technology coupled with precision
poration percentage for microarrays and a set of product with sensitivity in the low nanogram stepper motor control enables precise dispens-
DNA/protein calculation and conversion tools. range, sharp band resolution, and a clear image. ing of aggressive or ultra-pure media. Innovative
The DU 800 adds an advanced interface and The color is linear over a wide dynamic range zero-displacement-valve technology enables
additional tools for molecular biology, pro- and resists fading when exposed to light. pulsation-free dispensing. In addition, a pro-
teomics, and enzyme kinetic studies. The KPL For information 301-948-7755 grammable suckback capability provides com-
nanoVette expands the application of both sys- www.kpl.com plete control over residual drops of liquid, ensur-
tems to include very low-volume samples. ing recipe accuracy and maximizing chemical
Beckman Coulter For information 714-993-8955 Peptide Cleavage Device efficiency. The Furon PDP is driven by its own on-
www.beckmancoulter.com The P12 is a new accessory for the Activo-P11 board microprocessor. It can be operated via its
peptide synthesizer that allows the system to be own graphical user interface or controlled
DNA Sequencing Platform used on the lab bench while peptide-resin cleav- remotely via a built-in RS-485 interface. All wet-
The SOLiD System is a next-generation DNA age and side chain deprotection are undertaken ted surfaces are constructed from high-purity
sequencing platform designed to enable new ways in a nearby fume hood. The success of solid-phase fluoropolymers to suit dispensing of ultra-pure
of performing genetic analysis applications. The peptide synthesis using 9-fluorenylmethoxycar- chemicals used in the semiconductor, pharma-
system achieves a raw base accuracy of greater bonyl (Fmoc) amino acids is often limited by dele- ceutical, and medical industries.
than 99.94% due to two-based encoding, a terious side reactions that occur during trifluo- Saint-Gobain Performance Plastics
mechanism that distinguishes random or system- roacetic acid (TFA) peptide-resin cleavage and For information 800-833-5661.
atic errors from true single nucleotide polymor- side-chain deprotection. Most of these side reac- www.microelectronics.saint-gobain.com
phisms. The system combines scalable bead tech- tions modify susceptible residues with TFA-liber-
nology with mate-paired library preparation, ated side-chain protecting groups and linkers.
Newly offered instrumentation, apparatus, and laboratory
which helps researchers cost-effectively identify The use of scavengers to suppress these side reac- materials of interest to researchers in all disciplines in aca-
specific genomic regions where structural varia- tions is well-established; however, common scav- demic, industrial, and government organizations are featured
tions are located. A study has shown that structural engers such as thioanisole are best not used in an in this space. Emphasis is given to purpose, chief characteris-
variation accounts for almost 74% of the variant open laboratory due to their noxious odor. To tics, and availability of products and materials. Endorsement by
Science or AAAS of any products or materials mentioned is not
DNA sequence in the human genome. Identifying overcome this problem, the new P12 cleavage implied. Additional information may be obtained from the
the location of structural variation in genomes is device has been designed to directly accept the manufacturer or supplier.