LYNNMARGULIS:ARevolutionaryScientist

Liketheeventualacceptanceofcontinentaldrift,acceptanceofasymbiotictheoryofcellevolution
hasoftenbeenhailedasascientificrevolutionThewomanmostresponsibleforbringingtheideato
scientificrespectabilityisLynnMargulis.Aprolificwriteranddynamicspeaker,Margulis
captivatesaudiencesandoftenirritatesmoretraditionalbiologistswithherunorthodoxideas.A
profileinSciencedescribedherasanunrulyprovocateur,butasoneoftheworld'sleading
authoritiesoncellularevolution,shesupportsherclaimswithabundantevidence.Althoughmany
biologistscontinuetodisagreewithsomeofherideas,everyonetakesendosymbiosisseriously.
Margulisenteredbiologyduringaparticularlyexcitingperiod.JamesWatsonandFrancisCrick
werejustdiscoveringthestructureofDNAwhenMarguliswasincollege.Afewyearslater,when
shewasagraduatestudent,twoofherprofessorsdiscoveredDNAinchloroplasts.Otherscientists
reportedfindingDNAinmitochondria.Becausetheseearlyreportswerehotlydisputed,searching
forDNAoutsidethenucleuswasnotthesortofresearchprojectthatmostgraduatestudentswould
havechosen.Despitewarnings,MargulisplungedintothecontroversialproblemforherPh.D.
dissertation.Usingradioactivelylabelednucleotides,sheconvincinglydemonstratedthepresence
ofDNAinthechloroplastsofEuglenagracilis,oneofthecuriousunicellularorganismsthatshares
bothplantandanimalcharacteristics.
Marguliswroteherfirstarticleontheendosymbiotictheoryin1967,twoyearsaftershe
completedherPh.D.Atthetime,shewasasinglemotherwithoutapermanentteachingposition.
Shewasalsowritingherfirstbookonendosymbiosis,whichsparkedalivelycontroversywhenit
waspublishedin1970.AlthoughitinitiallybroughtMargulisnotoriety,thecontroversyover
cellularevolutionwasrathershortlived.Bythetimeshepublishedasecondbookon
endosymbiosisin1981,mostbiologistsacceptedimportantpartsofhertheory.Asaresult,
Margulisbecameascientificcelebritywhosesuccesswaspublicizedinbothpopularand
professionalmagazines.
BACKGROUNDTOACONTROVERSY
In1970,whenMargulis'sfirstbookwaspublished,mostbiologistshadneverheardof
endosymbiosis.Thosewhoknewaboutitusuallydismissedit.Inordertosucceed,Margulishadto
carefullydistinguishherideasfromthediscreditedtheoryproposedbyIvanWallinhalfacentury
earlier.Shealsohadtoovercomeabasicassumptionaboutevolutionheldbynearlyallbiologistsat
thetime.Accordingtothetraditionalview,evolutionusuallyoccursgradually;endosymbiosis,
however,isbasedontheideaofrathersuddenevolutionarychanges.Finally,Margulishadto
convincebiologiststotakeDNAinthecytoplasmseriously.AlthoughevidenceforDNAin
chloroplastsandmitochondriawasgrowingstronger,theideathatsomegenesresideoutsidethe
nucleusremainedunorthodox.
Despitethesebiasesagainstendosymbiosis,Margulis'sbookwaswidelyread.Eventhosewho
stronglydisagreedwithherdidnotridiculehertheorythewaybiologistshadbelittledIvanWallin's
theoryabouttheevolutionofmitochondria.Indeed,thebookconvincedmanybiologiststhat

cellularevolutionwasanexciting,ifcontroversial,field.Howhadcellbiologychangedduringthe
50yearsafterWallinproposedhisunsuccessfultheory?
Muchmorewasknownabouttheinternalstructureofcellsin1970thanin1920.UnlikeWallin,
whoknewlittleabouttheinternalstructureorfunctionofmitochondria,Margulishadaccesstoa
greatdealofinformationabouttheintemalstructureofcellswhenshewroteherbook.Powerful
electronmicroscopes,perfectedafterWorldWarII,allowedscientiststostudythepreviously
hiddenpartsoforganelles.Usingnewbiochemicaltechniques,scientistswereabletodiscover
manydetailsofcellularactivities.Mitochondria,longanenigma,werenowknowntobeimportant
sitesofadenosinetriphosphate(ATP)production,andforthefirsttimescientistswerebeginningto
understandhowthiscriticalprocessoccurredonmitochondrialmembranes.By1970biologists
alsobecameawareofmajordifferencesbetweenprokaryoticbacteria,whichlacknucleiandmost
otherorganelles,andeukaryoticcells,whichhaveboth.Thesharpdiscontinuitybetween
prokaryotesandeukaryotes,whichpreviouslyhadnotbeenfullyrecognized,washighlightedby
RobertWhittaker'snewsystemofclassification,whichusedthetwocelltypestodistinguish
kingdomMonerafromfoureukaryotickingdoms(Animalia,Plantae,Fungi,andProtista).The
prokaryotic/eukaryoticdistinctionwasnowattheforefrontofbiologicalattention.Whatother
similaritiesanddifferencesmightbefoundbetweenthetwotypesofcells?Howhadeukaryotic
cellsevolved?WhatwastheevolutionarysignificanceoftheDNAfoundinsomeorganelles?
ThesewerethequestionsthatMargulissetouttoanswerin1970.

THESERIALENDOSYMBlOTlCTHEORY(SET)
AccordingtoMargulis,eukaryoticcellsevolvedthroughaseriesofsymbioticpartnerships
involvingseveraldifferentkindsofprokaryoticcells.Thesmallerpartnersinvadedlargerhostcells
andeventuallyevolvedintothreedifferentkindsoforganelles:mitochondria,chloroplasts,and
flagella.Becausetheseevolutionarystepssupposedlyoccurredasaseriesofdiscreteevents,
Margulis'stheoryisoftenreferredtoastheSET:serialendosymbiotictheory.
Likeotherevolutionarybiologists,Margulisbelievesthatlifefirstappearedontheearthabout
fourbillionyearsago.Thefirstorganismswereextremelysimplemicroscopicdropletsofwater
containingafewgenesandenzymessurroundedbyamembrane.Theyfedonabundantorganic
moleculesthathadbeenproducedearlierintheearth'shistorybyvariousnonlivingchemical
processes.Likesomemodernbacteria,earlyprokaryoticcellsextractedenergyfromthese
moleculesbyfermentation,usingvariousformsofmetabolismthatdonotrequireoxygen.
Luckilyforthefermenters,therewasalmostnooxygenintheatmosphere.Iftherehadbeen,the
primitivecellswouldhavebeenpoisonedbythishighlyreactivegas.Later,asthesupplyof
energyrichmoleculesinthewateryenvironmentbegantobedepleted,othertypesofbacteria
evolvedwhichusedsolarenergytosynthesizetheirownsuppliesoflarge,organicmolecules.
Theseearlyphotosyntheticbacteriawerealsoanaerobic.Inotherwords,theydidnotuseoxygen
andtheirprimitivephotosyntheticreactionsdidnotproduceoxygenasabyproduct.Forovera

billionyears,primitiveecosystemsincludedonlytwotypesofprokaryoticorganisms:simple
photosyntheticbacteriaandfermentingbacteria.
Perhaps2.5billionyearsago,anewgroupofphotosyntheticbacteriaevolved,theancestorsof
today'scyanobacteria.Theseadvancedphotosynthesizerssplitwatertoproducethehydrogenions
(H+)neededtobuildsugarmolecules.Abyproductofthiswatersplittingreactionwasoxygengas.
Thiswasacatastrophiceventinthehistoryoflife.Oxygenissuchareactiveelementthatiteasily
destroysdelicatebiologicalstructures.Astheamountofoxygenintheatmosphereincreased,most
speciesofanaerobicbacteriaweredriventoextinction,victimsoftheearth'sfirstcaseofair
pollution.Somesurvivorsretreatedtoareasofbrackishwaterorotheroxygendepletedhabitats,
wheretheiranaerobicdescendantsstillflourishtoday.Afewprokaryotesbecameaerobicby
evolvingvariousmechanismstodetoxifyoxygen.Themostsuccessfuloftheseprocesseswas
respiration,whichnotonlyconvertedtoxicoxygenbackintoharmlesswatermolecules,butalso
generatedlargequantitiesofATP.
AccordingtotheSET,thephotosyntheticproductionofoxygengasandthesubsequentevolution
ofrespirationsetthestagefortheevolutionofalleukaryoticcells.Thisevolutionaryprocess
occurredinseveralseparatesymbioticevents.Thefirsteukaryoticorganellestoevolvewere
mitochondriastructuresfoundinalmostalleukaryoticcells.InMargulis'stheory,smallrespiring
bacteriaparasitizedlarger,anaerobicprokaryotes.Likesomebacteriatoday(Bdellovibrio),these
earlyparasitesburrowedthroughthecellwallsoftheirpreyandinvadedtheircytoplasm.Eitherthe
hostortheparasitewasoftenkilledintheprocess,butinafewcasesthetwocellsestablishedan
uneasycoexistence.Themutualbenefitstothepartnersareobvious.Therespiringparasite,which
actuallyrequiredoxygen,wouldallowitshosttosurviveinpreviouslyuninhabitable,oxygenrich
environments.PerhapstheparasitealsosharedwithitshostsomeoftheATPthatitproducedusing
oxygen.Inexchange,thehostprovidedsugarorotherorganicmoleculestoserveasfuelforaerobic
respiration.Eventually,asoftenoccurswithparasites,theprotomitochondrialostmanymetabolic
functionsprovidedbythehostcell.Similarly,asoxygenintheatmospherecontinuedtoincrease,
thehostbecamemoreandmoredependentuponitsprotomitochondriatodetoxifythegas.What
beganasacaseofopportunisticparasitismevolvedintoanobligatorypartnership.Thesmall
respiratorybacteriaeventuallyevolvedintothemitochondriaofeukaryoticcells.
Althoughvirtuallyalleukaryoticcellscontainmitochondria,onlythoseofplantsandcertain
protistscontainchloroplasts.Therefore,itseemslikelythatchloroplastsevolvedinonlyafewlines
ofeukaryoticcells,andthiseventoccurredaftermitochondriawerealreadywellestablished.How
didthisnewevolutionarypartnershipevolve?Withhighermetabolicrates,cellscontaining
mitochondriaweremoreefficientthananaerobiccells.Someofthesenewer,unicellularorganisms
grewlargerandevolvedintopredatorscapableofeatingsmallercells.Theirpreyundoubtedly
includedcyanobacteria.Inrarecases,thesesmallphotosyntheticcellsmayhaveresisteddigestion
afterbeingengulfed.Insidethepredator,theysetupasemiindependentexistenceandeventually
evolvedintochloroplasts.
Althoughsuchascenariomayseemfarfetched,weknowthatsimilarpartnershipsexisttoday.
Forexample,theunusualciliateParameciumbursariaishosttomanyunicellulargreenalgaeinthe

genusChlorella.These"pseudochloroplasts"producesugarmoleculesthataresharedwiththehost.
IftheChlorellaareexperimentallyremoved,bothpartnerscontinuetoexistindependently.Without
itsphotosyntheticpartners,however,theParameciumbecomestotallydependent,uponexternal
sourcesoffood.Providedtheopportunity,theParameciumwilleatChlorellabutwillnotdigest
them,thusreestablishingthesymbioticpartnership.Parameciumbursam'aisnotauniquecaseof
modernendosymbiosis.Manyotherorganisms,includingseveralmulticellularanimals,alsoplay
hosttophotosyntheticalgaeorcyanobacteria.
ThemostcontroversialclaimmadebyMargulisisthateukaryoticflagellaevolvedfromsmall,
corkscrewshapedbacteriacalledspirochetes.Manyspirochetesareparasites(thebestknown,
Treponemapallidurn,causessyphilis).Othersarefreeliving,foundinsuchexoticenvironmentsas
theintestinesoftermites.Regardlessofhowtheylive,theseunusualbacteriaswimwithan
undulatingmotionreminiscentofthewhiplikemovementofeukaryoticflagella.Isthissimilariti
evidenceforMargulis'sevolutionaryclaim,orisitsimplyacoincidence?Whynotacceptthemore
orthodoxexplanationthateukaryoticflagellagraduallyevolvedfromthesimplerflagellafoundon
manybacteria?
Margulispointsoutthatalthoughbothtypesofflagellaareusedforlocomotion,prokaryoticand
eukaryoticstructuresareverydifferent.Prokaryoticflagellaconsistofasingle,hollowfilamentof
proteinthatspinsonitsaxislikeatinypropeller.Eukaryoticflagellaaremuchlarger;theycontain
acomplexarrangementof11microtubules,andtheentirestructureissurroundedbyanextension
ofthecellmembrane.Incontrasttothespinningprokaryoticflagellum,theeukaryoticstructure
propelsthecellbylashingbackandforthinawhiplikefashion.Becausetheyaresodifferentin
structure,function,andperhapsevolutionaryorigin,Margulisproposesthattheeukaryotic
flagellumshouldbereferredtobyadifferentterm:undullpodium.