Biogeochemical Cycles

Henry L Ehrlich, Rensselaer Polytechnic Institute, Troy, New York, USA Ronald S Oremland, United States Geological Survey, Menlo Park, California, USA Jonathan P Zehr, University of California, Santa Cruz, California, USA
The biosphere harbours large quantities of the elements essential to life, but the largest portion is tied up as minerals and sediments. Dead biomass and some of the nutrients immobilized in rocks and sediments are made available to living organisms through recyling (biodegradation) by microbes.

Secondary article
Article Contents
. Microbial Metabolism and Global Elemental Cycling . The Carbon Cycle and Global Climate . Nitrogen Cycle and Primary Productivity . Other Elemental Cycles

Microbial Metabolism and Global Elemental Cycling

Of special interest in global elemental cycling are the major elements contained in cellular constituents, namely C, H, O, N, P, S, and in some organisms Si, and the minor elements, including Ca, Mg, Fe, Mn, Cu, Co, Ni, Zn, and in some instances Mo, V, Se and Cr. Because of their limited accessibility in the biosphere, cycling of vital elements is essential for successive generations of organisms. Elemental cycling involves three major compartments in the biosphere: the hydrosphere, parts of the lithosphere and the atmosphere. Among the vital elements, C, H, N, O, S and Se can occupy all three compartments, whereas Ca, Mg, P, Fe, Mn, Cu, Co, Ni, Zn, Si, Mo, V and Cr only occupy the hydrosphere and the lithosphere. Although phosphorus can exist as volatile phosphine (PH3), this compound is too readily autoxidizable to persist in the atmosphere. In elemental cycling, elements can pass through mobile (soluble or volatile) and immobile (insoluble) states. Immobilization may occur as a result of adsorption to a solid, incorporation into cellular constituents, or precipitation and/or crystallization. Remobilization may result from change in pH and/or ion exchange in the case of adsorbed elements, from biodegradation of organic excretions or remains of dead organisms, and from weathering of precipitates and minerals. Living organisms inuence elemental geochemical cycles by controlling rates of chemical transformation, usually through acceleration of slow reactions in a cycle. Microbes exert their inuence by direct enzymatic catalysis, by formation and excretion of metabolic products that are reactants in specic reactions in a cycle, and by release or consumption (cellular uptake) of specic species of elements that are part of a cycle (Ehrlich, 1996). Higher forms of life exert their inuence mainly by the last of these processes. Although, in absolute terms, the biosphere of Earth harbours varying but large quantities of all elements essential to life, only a fraction of any of them are

nutritionally available. The reason is that a portion of each element is tied up at any time in living and dead biomass and in excretions from living biomass, some is adsorbed to solid phases in the biosphere, but the largest portion is tied up in minerals of rocks and sediments. Nature ensures that the vital elements in dead biomass and excretions that have not become inaccessible by burial below the biosphere are made available to new generations of living organisms through recycling (biodegradation) by microbes (Figure 1). Some of the vital elements that occur immobilized in rocks and sediment in the biosphere are remobilized and made nutritionally available by weathering, a process in which microbial activity often plays an important role (Ullman et al., 1996). Microbes promote weathering by catalysing redox reactions, and by producing acids, bases and/or ligands that attack minerals and cause dissolution of mineral constituents (Ehrlick, 1996). Adsorbed elements may be recycled as a result of desorption caused by microbially formed reagents, especially acids and ligands. Although higher forms of life contribute to partial biodegradation of some organic matter, microbes especially fungi and bacteria are involved in complete biodegradation by converting organic to inorganic matter (Figure 1a). In complete microbial degradation, carbon in organic matter is converted to CO2 or methane; hydrogen 2 to H2O or H2; nitrogen to NO3 , NH3 and N2; phosphorus 32 2 2 to PO4 ; and sulfur to HS or SO2 4 . The oxidative conversion of organic to inorganic matter is termed mineralization. In aerobic mineralization, O2 is the ultimate oxidant. In anaerobic mineralization, the oxidant 2 2 is commonly NO3 , Fe(iii ), Mn(iv ), SO2 or CO2, or, 4 more rarely, some other inorganic substances such as 2 2 32 2 AsO3 or SeO3 4 , AsO2 , SeO4 3 , all of which can exist in more than one oxidation state. Biological oxidations of organic matter involving externally supplied oxidants, regardless of the oxidant involved, are categorized as respiration if energy is conserved in the process. Some microbial biodegradation may include fermentation, in which no externally supplied oxidant is involved but energy is nevertheless conserved. In fermentation, intermediate metabolic products undergo a disproportionation in which
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Biogeochemical Cycles
Ass micro- imilation by and m acrofa un

Living biomass

Excre

tion

Dissolved organic carbon

Excretion

ath De

1b Microbial degradation

Assimilation

1a

Particulate organic matter Mineralization by microbes

Mobile, inorganic pool Biological and chemical precipitation 1c Biological and chemical remobilization

Immobile, inorganic pool (minerals)

Figure 1 Cycling of matter in nature. (1a) Cycling in which products of complete mineralization of organic matter pass through a mobile inorganic pool. (1b) Cycling in which organic matter is only partially degraded. (1c) Cycling of inorganic products of mineralization between a mobile and immobile pool.

one portion oxidizes the other in a redox reaction, but the substrate is not completely converted to inorganic matter. Formate, acetate, CO2 and H2 are typical fermentation products. The fermentation products may eventually be mineralized, but only by oxidation through subsequent respiration reactions. When CO2 is the only externally available oxidant anaerobically, a signicant portion of organic carbon that is degraded is converted to methane, but this methane is subject to bacterial oxidation to CO2 when reaching aerobic environments, mostly by a specic group of bacteria (methanotrophs). Products of mineralization may enter the surface or groundwater on land and thus become available as nutrients to the microbial and higher terrestrial and aquatic ora and fauna. Alternatively, they may be transported to the sea, where they are added to the nutrient pool derived from biodegradation of dead organic matter and excretions from marine organisms and become available to marine organisms that can assimilate them. Whether on land or in the sea, some products of mineralization, like CO2, sulde, sulfate, phosphate, iron (ii and/or iii ) and manganese (ii and/or iv ), may become transiently or more permanently immobilized in corresponding inorganic compounds (minerals). In complete global elemental cycles, mobilized inorganic products from microbial mineralization of organic matter are assimilated by new generations of living organisms (Figure 1a). Microbes and plants are the main actors in this. Microfauna and macrofauna tend to short-circuit the carbon and nitrogen cycles by assimilating partially 2 degraded organic matter rather than CO2, SO2 4 , or 2 NO3 (Figure 1b). Some inorganic elements dissolved as
2

cations or anions may be immobilized by enzymatic or nonenzymatic oxidation or reduction to form insoluble compounds, or by reacting with counterions under conditions of supersaturation to form insoluble noncrystalline or crystalline precipitates (Figure 1c). Some immobilized inorganic matter may be remobilized (dissolved) by enzymatic or nonenzymatic oxidation or reduction, or by interaction with metabolically produced acids, bases or ligands (bioweathering) (Figure 1c). The overall workings of the carbon, nitrogen and sulfur cycles are illustrated in Figure 2. In the iron cycle, iron exists in dierent oxidation states and in soluble and insoluble phases, depending in part on environmental pH and the presence or absence of oxygen. Ferrous iron is unstable in oxygen-saturated water at circumneutral pH, autoxidizing to ferric iron. If the ferric iron is not complexed by suitable organic or inorganic ligands, it will precipitate as amorphous ferric hydroxide or oxyhydroxide and may form iron minerals such as haematite (Fe2O3) or goethite (FeOOH). Since assimilation of iron by cells requires it to be in soluble form, many microbes secrete ligands (siderophores) that have a very high anity for ferric iron but low antity for ferrous iron. They form soluble ferric complexes by withdrawing iron from iron oxides. The iron in the complexed form is then taken into the cell and assimilated into cytochromes and ironsulfur proteins. The uptake involves several steps: attachment of the complexed iron to specic receptors at the cell surface, transport of the complex into the cell, reduction of the iron from Fe3 1 to Fe2 1 , release from the siderophore (which has a very low anity for Fe2 1 ) and incorporation into specic iron-requiring molecules. The

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Biogeochemical Cycles

siderophore from which the iron has been released may then be recycled. In some instances, the siderophore is degraded before the Fe3 1 is reduced to Fe2 1 . In that case, the siderophore is not recycled. In still other instances, the ligand that complexes ferric iron in the environment is exchanged for another at the binding site on the cell surface, and the new iron complex is then transported into the cell, where the Fe3 1 is immediately reduced to Fe2 1 and assimilated. Upon the death of a microorganism, its iron is released and may form ferric oxides or ferric phosphate (strengite, FePO4 . 2H2O). These minerals may be redissolved by organic acids and ligands. Ferric oxides may be reduced by certain bacteria anaerobically at circumneutral pH to form magnetite (Fe3O4), a mixed ferrousferric oxide, ferrous carbonate (siderite, FeCO3), vivianite (Fe2(PO4)3 . 8H2O), or dissolved ferrous iron, some of the latter being assimilated. Ferrous iron under anaerobic conditions can react chemically with sulde of biogenic or abiogenic origin to form compounds like iron sulde (FeS) and iron pyrite (FeS2). Pyrite at circumneutral pH in air is relatively stable, whereas FeS dissolves and autoxidizes gradually. Pyrite at low pH (1.53.5) in air oxidizes rapidly, but only when aided by acidophilic iron-oxidizing bacteria (Ehrlich, 1997). Above pH 2, the oxidized iron from pyrite tends to precipitate as basic iron sulfate (jarosite). At low oxygen tension and circumneutral pH, the bacterium Gallionella ferruginea oxidizes ferrous to ferric iron and deposits it as an oxide in its lateral stalk, and the bacterium Leptothrix discophora accumulates ferric oxide in its sheath (Ghiorse and Ehrlich, 1992). Ferrous ion is the most mobile form of iron but, because it is unstable in solution under aerobic circumneutral conditions, it is not readily transported over long distances by water. Geochemical cycling of manganese in the environment is not unlike that of iron, except that manganous manganese (Mn2 1 ) is much more stable at circumneutral pH than is ferrous iron. Other than by assimilation, Mn2 1 may be immobilized aerobically through autoxidation above a pH of about 8 to hausmannite (Mn3O4) or to manganite (MnOOH), both of which very slowly disproportionate to MnO2 and Mn2 1 . Manganous manganese may also be microbiologically oxidized directly to MnO2 without accumulation of the intermediates Mn3O4 or MnOOH. This can occur in soil and in freshwater and marine environments. A number of dierent, unrelated Grampositive and Gram-negative organisms have been implicated. In some instances the oxidized manganese is deposited at the cell surface, in others externally to the cell, for example in concretions occurring in soil or on deep ocean sediment. Some microbes can reduce MnO2 enzymatically to Mn2 1 under anaerobic conditions, using organic carbon or H2 as reductants, and others under either aerobic or anaerobic conditions, all using organic carbon as reductants. MnO2 may also be chemically reduced under anaerobic conditions to Mn2 1 by envir-

onmentally available ferrous iron or sulde (HS 2 ), which may have had a microbial origin. Whereas Mn2 1 oxidation immobilizes manganese, MnO2 reduction mobilizes it. Geochemical cycling of other transition elements such as Cu and Zn involves reversible passage from an immobilized to a mobile state. The immobile state may merely involve adsorption to a solid phase like clay, or it may involve precipitation by sulde of biogenic or abiogenic origin. Mobilization may involve desorption by microbially produced organic or inorganic acid, or it may involve bacterial oxidation if a metal sulde is involved. Immobilization of molybdenum involves redox and precipitation reactions as well as adsorption reactions, and mobilization the opposite. The alkaline earths Ca and Mg are readily immobilized by precipitation as carbonates, phosphates or silicates. Calcium carbonates and phosphates may be formed in the assimilatory processes of microbes and higher forms of life in the formation of protective and support structures (tests and bone, respectively). The counterions involved in the precipitation may themselves be products of metabolism. Ca2 1 and Mg2 1 ions may also be immobilized by adsorption to the surface of microbial cells. Remobilization may be due to microbially produced acids or ligands. In some cases enzymes may be involved.

The Carbon Cycle and Global Climate

Concerns over global warming trends and the integrity of the stratospheric ozone layer have focused scientic attention upon the composition of the atmosphere with respect to its reactive trace gases. It should be borne in mind that global warming can be caused by factors not directly linked to the composition of the Earths atmosphere, such as periods of increased solar luminosity. However, there is broad general agreement that increased concentrations of heat-absorbing trace gases derived from human activities are responsible for the trend towards higher global temperatures observed during the last century. The greenhouse eect is caused by the radiant energy absorbed from incident solar energy on the Earths surface being dissipated as black-body radiation in the infrared energy region. The ability of certain gases to absorb this infrared radiation emanating from the Earths surface results in the trapping of heat in the atmosphere. By far the most important and abundant greenhouse gas in the Earths atmosphere is water vapour; however, the amount of water in the atmosphere responds directly to average global temperatures and is therefore not subject to biogeochemical controls. Analysis of atmospheric gases contained in polar ice cores has clearly demonstrated that the concentration of heat-trapping biogenic gases such as CO2, CH4 and N2O in the atmosphere has risen
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Biogeochemical Cycles

dramatically over the past two centuries, strongly implying that human-related activities have been the causative factor for their rise. The most important greenhouse gas that is aected by global biogeochemical cycles is CO2. It is instructive to compare the major components of the atmosphere of the Earth, a planet that harbours abundant life, with those of our terrestrial planetary neighbours, which do not harbour life, in order to discern what eect life would have on the CO2 content of their atmospheres Table 1). The most striking facet of Table 1 is that the Earth, owing to the activity of photosynthetic plants and microbes, has a strongly oxidizing atmosphere, while our two abiotic neighbours are essentially anoxic. Carbon dioxide is a major component of the abiotic planetary atmospheres of Mars and Venus, while by comparison it is only a trace component of Earths. These data indicate that a major biogeochemical cycle for carbon on Earth constrains the amount of CO2 in its atmosphere because the carbon is stored in its living and dead biota (this would include petroleum and natural gas deposits, and the kerogen in rocks), dissolved in its surface waters (e.g. oceans) and as geological deposits of carbonates, many of which were formed as a consequence of biological activity (e.g. coral reefs, foraminiferal sediments). In contrast, the abiotic planets have high levels of atmospheric CO2, which reects the absence of carbon storage in biological reservoirs and in large hydrospheres such as global oceans. Cycling of carbon on the abiotic planets occurs primarily between the solid geosphere and the atmosphere, a slow process, which means that the turnover times for carbon in their atmospheres is very long. Both Mars and Venus lack Earths tectonic machinery, which accelerates exchange of carbon between the surface and deeper buried geological reservoirs. Analysis of data from the recent Magellan missions to Venus suggest that planet-wide massive volcanic disruptions occur with a period of $ 500 million years, while at other times the planet is essentially quiescent. Hence, such exchanges on Venus occur by force of rare, planet-wide cataclysms. Signicant volcanic activity on Mars appears to have ended about two billion years ago. Because liquid water does not exist on that planets surface, exchange of carbon between the atmosphere and its geological reservoirs must also be slow. In contrast, on the tectonically active Earth the oxidation of exposed kerogens from formerly buried rocks, when combined with

volcanic CO2 emissions, produces quite signicant annual uxes to the atmosphere ( $ 180 1012 gC/year). The capacity of individual atmospheric trace gases to contribute to global warming (or to destroy stratospheric ozone) can be calculated provided that certain important factors are known. These include the capacity of the molecules in question to absorb infrared radiation of a given wavelength (its infrared cross section), the average global concentration of the molecule in the atmosphere (mixing ratio), and the residence time (T) of the molecule in the atmosphere. The residence time is calculated by dividing the substances atmospheric burden, or the total quantity of its molecules in the atmosphere, by the magnitude of its total annual sources or its total annual sinks (i.e. mechanisms of destruction). These calculations are complicated by several phenomena related to mixing of the global atmosphere, which include seasonal oscillations in the mixing ratios of any given compound caused by imbalances between sources and sinks, the northern-tosouthern hemispheric gradient in mixing ratios caused by source/sink imbalances between the two hemispheres (global mixing between the hemispheres takes about one year), the kinetics of the molecules degradation in the troposphere (the largest component of the atmosphere), and the annual ux of the substance from the troposphere to the stratosphere. This last factor, namely ux to the stratosphere, is governed by the residence time of the compound in the troposphere. Unreactive substances without signicant tropospheric sinks have long tropospheric residence times. The longer a substances residence time, the greater the amounts of it that will be transported through the tropopause boundry and be wafted up to the stratosphere. This is an important point for long-lived substances like chlorouorocarbons (CFCs) that contribute to stratospheric ozone destruction. Some of the important atmospheric parameters for key heat-absorbing carbon gases are given in Table 2 and the rest of this section will be devoted to discussions of these gases. Because this section is concerned only with carbon, there will be no discussion of other important atmospheric trace gases (e.g. the oxides of nitrogen) that contribute to global warming and ozone destruction.

Table 1 Surface pressure, avergae global surface temperatures and major atmospheric components of the terrestrial planets of the solar system Planet Earth Venus Mars Pressure (bar) 1.0 95.0 0.01 Temperature (8C) 15 264 2 53 N2 (%) 78 97 3 O2 (%) 21 0 0 CO2 (%) 0.035 3.0 97.0

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Biogeochemical Cycles

Table 2 Properties of selected carbon gases that contribute to global warming Gas CO2 CH4 CO CFC-11 CFC-12 CH3CCl3 CH3Br
a b

MRa 350 000 1700 0.12 0.27 0.53 0.12 0.005

Tb 5e 8 0.5 60 120 5 <1

GWPc 1.0 3.7 1.4 4000 10 000 220 2400

Burdend 72 1016

Sources Natural and anthropogenic Bacterial Combustion Anthropogenic Anthropogenic Anthropogenic Natural and anthropogenic

0.5 1016 0.2 1012 0.09 1012 0.16 1012 0.06 1012 0.03 1012

Mixing ratio, in part per billion by volume. Atmospheric residence time in years. c Global warming potential relative to CO2. d Atmospheric burden, as grams C. e For the purpose of calculating GWP for CO2, T = 230 years.

Carbon dioxide
Carbon dioxide is a relatively weak absorber of IR energy. By comparison, a molecule of CH4 absorbs about 20 times more IR energy than does a molecule of CO2. However, the high mixing ratio and atmospheric burden of CO2 make it by far the most important greenhouse gas in the atmosphere. In relative terms, CO2 is estimated to account for about half the radiative forcing of the atmosphere (not counting water vapour), with the remainder contributed by the sum of all the other IR-absorbing trace gases (e.g. CH4, N2O, CFCs). The residence time of CO2 in the atmosphere is about 5 years, but for the purpose of calculating its global warming potential (GWP) a T of $ 200 years is used. This is the time that would be required for all the CO2 injected as a discrete pulse into the atmosphere to be completely dissipated by absorption into the various sinks for this compound. The value of GWP for CO2 is set as 1.0 in Table 2, so the GWPs for other gases are given relative to the CO2 value and are meant as proportional increases. For example, if the atmospheric mixing ratio of CO2 increased by 10%, a similar proportional increase of 10% in the mixing ratio of CFC-12 would have 10 000 times the heattrapping eect as CO2, while a 10% increase in CO would have only 1.4 times the eect. An ongoing 50-year study of continuous CO2 measurements made by C.D. Keeling and his associates from the Mauna Loa Observatory in Hawaii has documented a steady increase in its mixing ratio by nearly 1.0 ppm annually over this period. Superimposed on these data are the annual uctuations of $ 8 ppm amplitude that are caused by the local seasonal imbalances between biogenic sources and sinks. In the spring and summer months, CO2 mixing ratios are lowest because of its uptake and storage related to plant growth. In fall and winter, the decay of this

material and the decline of photosynthesis elevates the CO2 mixing ratio. However, the long-term increase of CO2 is caused by an imbalance of global sources of CO2 that outweighs its global sinks. Major sources of atmospheric CO2 include the oxidation of organic matter by animal, plant and microbial metabolism (biochemical respiration and fermentation), the weathering/oxidation reactions of exposed kerogens, the combustion of organic matter by biomass burning and use of fossil fuels, net changes in carbon ux associated with land use (e.g. from forest to agricultural), volcanic emissions, and the outux of CO2 from supersaturated surface waters. Major sinks for CO2 include its xation into organic matter by autotrophs (photosynthetic and chemosynthetic), its dissolution into the oceanic mixed layer, and its chemical or biochemical precipitation as carbonates. The balance between global sources and sinks is such that in the northern hemisphere mixing ratios are $ 3 ppm higher than in the southern hemisphere. This implies that in the northern hemisphere the magnitude of sources (e.g. fossil fuel combustion) is stronger than in the southern hemisphere. However, global climate models predict that the interhemispheric CO2 gradient should be larger than that observed, and the oceans in the northern hemisphere provide an insucient sink to absorb this excess quantity of CO2. Thus, a large, unknown terrestrial sink for CO2 in the northern hemisphere has been indicated by global climate models, and stable carbon isotope investigations have indicated that this sink is located in the regions temperate latitudes. Identication of the nature of this sink is an important focus of current research, a fact that will become more critical as global warming progresses and results in a release of CO2 into the atmosphere from carbon stored in northern boreal forests.

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Biogeochemical Cycles

Methane
Methane is the second most important atmospheric trace gas in terms of global warming. Its content in polar ice cores indicates that the tropospheric mixing ratio of methane has increased nearly 3-fold over the past 1000 years, with values doubling over the past century alone. Globally averaged tropospheric mixing ratio measurements have been made over decadal time periods, and an annual 1% increase was observed from 1978 to 1988. The rate of annual increase declined in the early 1980s owing to the combined eects of the Mount Pinatubo eruption and the El Nin o Southern Ocean Oscillation upon the magnitude of tropospheric sinks for CH4. The primary source of CH4 to the atmosphere comes from the activity of anaerobic methanogenic bacteria that form this gas in wetlands, animal intestinal tracts (including the rumen of cows and the hindgut of termites), and in rice paddy soils. The primary evidence for a bacterial source lies in the fact that atmospheric CH4 has a high radiocarbon (14C) content. Although burning of biomass contributes a substantial amount ( $ 10%) of recent carbon to the atmosphere in the form of CH4, this is oset by release to the atmosphere of bacterially formed methane that is depleted in 14C. An example of such a source is the breakdown of methane hydrates in tundra permafrost. The major sink ( 4 90%) for methane is its oxidation by hydroxyl (OH.) radicals present in the troposphere, which initiate its oxidation to CO and eventually to CO2. Hydroxyl radicals are generated from the photochemical reactions undergone by ozone (O3) with H2O and are a measure of the oxidation state of the troposphere. Thus, OH. levels will decline if the concentration of pollutants rises, a factor that will also allow for an increase in CH4 mixing ratios. A second important sink for CH4 is associated with its oxidation by bacteria in soils. The magnitude of this sink is not precisely known, but it is generally estimated to be a few per cent annually, or of comparable magnitude to the annual increase of the tropospheric mixing ratios of CH4. This point is signicant because any feedback factors that tend to diminish the uptake of atmospheric methane by soil bacteria will tend to increase its tropospheric mixing ratio. Such factors may be inhibition of methane oxidation by dryfall of nitrogen compounds into soils, soil desiccation, and water saturation of soil. The methane monooxygenases (MMO) of methanotrophic bacteria can either be membrane-bound (particulate MMO) or cytoplasmic (soluble MMO). The nal sink for tropospheric CH4 is its ux to the stratosphere, where it also undergoes oxidation. Its initial oxidation product is methyl radicals, which scavenge chlorine atoms that would otherwise be available to degrade ozone. Methane also supplies the hydrogen necessary for the water budget of the stratosphere.

Carbon monoxide
Carbon monoxide is a relatively minor constituent of the atmosphere compared with CH4 and CO2 and it has only a small inuence with regard to global warming Table 2). None the less, substantial annual increases ( $ 6%) in its globally averaged tropospheric mixing ratio were observed in the mid-1980s. Natural sources of CO to the atmosphere stem from the OH. lane as well as hydrocarbons emitted from plants (e.g. terpenoids), wildres, and oceanic sources from animals such as siphonophores. Natural sources account for perhaps 45% of the global CO budget, while the rest is derived from anthropogenic sources (fossil fuel combustion, anthropogenic CH4, burning of forests/ savannah for the purpose of clearing land). Tropospheric sinks include further oxidation of CO by OH. radicals. In addition, a number of bacteria and fungi can metabolize CO, and live soils can consume CO from the atmosphere. However, the global signicance of a microbial soil sink is not known.

Halocarbons
These compounds, which are mostly of anthropogenic origin, are of such particular importance with respect to global warming and stratospheric ozone degradation that an international agreement (the Montreal Protocol) has been made to eliminate or constrain their use. Of the halocarbons, the chlorouorocarbons (CFCs) were rst identied by Molina and Rowland (1974) as being destructive to ozone and their use has been banned. CFCs are unreactive and thus they are useful as refrigerants and for industrial purposes, but when released to the atmosphere they are not oxidized by OH.. Hence, they have long tropospheric residence times and their primary sink is transit to the stratosphere, where they undergo highenergy photolysis reactions. Their photolysis liberates atomic chlorine, which reacts with ozone to form oxygen and chlorine oxide. CFCs are also subject to biodegradation under anaerobic conditions via reductive dehalogenation, and CFC-11 (CCl3F) is more readily degraded than is CFC-12 (CCl2F2). However, the quantitative signicance of these biodegradative reactions is unknown, but it is likely to have only a very minor eect on the tropospheric residence times for CFCs. Trichloroethane (CH3CCl3; TCA) has only an anthropogenic source. Its tropospheric mixing ratio doubled from 1978 to 1988, but with the implementation of the Montreal Protocol its use has been restricted and more recent data indicate a decline. It is assumed that the only sink for TCA is its oxidation by OH., which results in its relatively low residence time. Indeed, because OH. cannot be measured directly and there is a 1:1 ratio of OH to TCA in the destruction reaction, the decline of the mixing ratio for TCA has been taken as an index of OH. concentrations in the troposphere. These data have indicated that OH.

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Biogeochemical Cycles

appears to be more abundant than previously estimated, which results in lower estimates of residence time for many atmospheric trace gases consumed by OH.. However, oxidation by OH. is not the sole sink for TCA and there have been observations that it is also biodegraded. The global signicance of this biochemical sink for TCA has been recently estimated by Happell and Wallace (1998) to account for $ 5% of its tropospheric removal by OH.. Methyl bromide is a halocarbon with mixed natural (66 83%) plus anthropogenic (1633%) sources. Although it has a short residence time, there is concern about transport of brominated halocarbons to the stratosphere because the atomic bromine formed from photolysis is far more destructive to ozone than is atomic chlorine. Anthropogenic sources include its use as a fumigant for agriculture and for preservation of structures and stored grains. Its biogenic sources have not been identied, but it can be evolved by a number of phytoplankton, aquatic plants and fungi. Other natural sources come from burning of biomass. The primary sink for methyl bromide is its oxidation by tropospheric OH., which gives a residence time of $ 1.7 years. The oceans have been determined to be a net sink for methyl bromide, which they destroy by chemical or biochemical means. A number of bacteria, such as methanotrophs, can oxidize methyl bromide and one soil isolate has actually been shown to grow on this compound. Shorter et al. (1995) determined that bacteria in soils can oxidize methyl bromide at ambient mixing levels of this substance. This global soils sink, when combined with the oceanic and tropospheric OH. sinks, yields a residence time of $ 0.8 years.

Nitrogen Cycle and Primary Productivity

Next to carbon, nitrogen is the major component of living matter on Earth. The incorporation of carbon dioxide into organic carbon compounds is termed primary production, and is performed by phototrophic organisms including higher plants, macroalgae, eukaryotic microalgae, cyanobacteria and chemoautotrophic bacteria such as ammonia oxidizers. Nitrogen is a major constituent of biological molecules, including nucleotides and amino acids that are the building blocks of the genetic material and proteins of organisms. The xation of carbon by autotrophs represents the base level of the food chain on which the biological productivity of the planet is dependent. The availability of nitrogen often limits the growth rate and productivity of primary producers in terrestrial and aquatic habitats (Vitousek and Howarth, 1991). Nitrogen exists in several chemical forms, the relative abundance of which is a function of chemical stability and biological activity. The largest reservoir of nitrogen on the planet is in the form of gaseous dinitrogen (N2) in the

Earths atmosphere, which comprises approximately 80% by volume of the atmosphere. Other simple chemical forms 2 2 of nitrogen are nitrate (NO3 ), nitrite (NO2 ), ammonium 1 (NH4 ), urea (H2NCONH2), hydroxylamine (NH2OH), nitric oxide (NO) and nitrous oxide (N2O), which represent dierent oxidation states. Nitrate is the most oxidized form of nitrogen, whereas ammonium is the most reduced. Generally, many organisms can use nitrate or ammonium for growth. The assimilation of nitrate is dependent upon its reduction to ammonium, catalysed by specic enzymes (e.g. nitrate reductase). Ammonium is assimilated into organic compounds through the amino acid intermediates glutamine and glutamate. Nitrous oxide, nitric oxide and hydroxylamine are unimportant as sources of xed nitrogen for organisms, but are intermediates in nitrication and/or denitrication. The existence of nitrogen in multiple redox states provides for complex biogeochemical cycles of nitrogen in the terrestrial and aquatic biomes of the Earth (Figure 2). The oxidation of ammonium to nitrate provides a biological mechanism for capturing energy. The conversion of ammonium to nitrite is catalysed by ammonium oxidizers, and the conversion of nitrite to nitrate by nitrite oxidizers, both are nitriers. This is an obligately aerobic process and occurs in aerobic waters and sediments or at aerobicanaerobic interfaces. Oxidized nitrogen (nitrate, nitrite, and nitric and nitrous oxide) can be used as an alternative electron acceptor during respiratory electron transport, making it possible to produce ATP by respiration even in the absence of oxygen. The end product of nitrate reduction may be dinitrogen gas or ammonia. When it is dinitrogen, the process is termed denitrication. When it is ammonia, it is called nitrate ammonication. Denitrifying organisms are active in low-oxygen environments such as sediments and saturated soils. Some organisms, such as enterobacteria, reduce nitrate to nitrite in nitrate respiration, and the nitrite formed is either excreted or further reduced to ammonium. Many organisms can acquire and transform nitrogen from organic compounds, either transferring the nitrogen from one organic compound to another as necessary, or liberating ammonium from the oxidation of organic nitrogen compounds during metabolism and reassimilating it. Nitrogen xation, which is the conversion of dinitrogen gas to ammonium, occurs to some extent abiotically through electrical discharges in lightning, but mostly biologically as a result of the activity of many diverse prokaryotic organisms. Biological nitrogen xation is energetically expensive, and is sensitive to oxygen. Life on Earth is dependent upon nitrogen xation to replenish biologically available nitrogen that is biologically converted to gaseous dinitrogen through denitrication in anoxic or microaerobic environments. Primary producers, in both terrestrial and aquatic environments, use nitrogen in several chemical states including nitrate, ammonium, urea and dinitrogen gas.
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The relative availability of the dierent forms is largely a function of the relative rates of biogeochemical processes catalysed by the microorganisms that produce them. The relative rates of the transformations are regulated by environmental conditions, including the presence of oxygen, nutrients and other electron donors and acceptors. The nitrogen cycle contains steps that are catalysed under either aerobic or anaerobic conditions. Therefore, dierent chemical forms of nitrogen are typical of dierent environments, depending upon the availability of oxygen or alternative electron acceptors. Growth of primary producers can become limited by the availability of nitrogen in both terrestrial and aquatic ecosystems. Nitrogen fertilizers are often used in agricultural practices worldwide. Fertilizers may be applied as nitrates or ammonium, but nitrates are not adsorbed by soil minerals and are rapidly lost to soil solution and subsequently in surface runo. Ammonium, a cation, is adsorbed to a greater extent to soil minerals, especially clays, and is retained within the soil for a greater length of time. The application of nitrogenous fertilizers can be economically expensive, and alternative means to alleviate nitrogen limitation of primary production are benecial. In contrast to some other nutrient cycles, such as that for phosphorus, the nitrogen cycle includes a major component that is gaseous and is a major constituent of the Earths atmosphere. This gaseous form of nitrogen is relatively inert, and is not biologically available except to a restricted, but diverse, group of microorganisms called diazotrophs. These microorganisms, which have the biological capability to x dinitrogen gas into biologically available ammonium, play critical roles in supplying nitrogen in terrestrial and aquatic environments, and are particularly important for many plants, including agriculturally important crops such as legumes. Nitrogen-xing bacteria of the genus Rhizobium are particularly noteworthy in forming close associations with leguminous plants such as alfalfa, with whose root system they form nodules. The association is a complex mutualistic relationship, and molecular signals are exchanged between the host and symbiont in order to allow the symbiotic bacteria to specically recognize the host, penetrate the root hairs and develop into nitrogen-xing bacteroids in a specialized nodule cavity in the host plant. Other such symbioses are also known (such as the relationship between the rmicute genus Frankia and alders), although the biochemical and molecular basis of the hostsymbiont relationship is not as well understood as in Rhizobium. Nitrogen xation is catalysed by the enzyme nitrogenase, which thus far has only been found in prokaryotes. However, evolutionarily related protein sequences have been detected in higher organisms. Nitrogen-xing organisms include archaeal, eubacterial and cyanobacterial taxa. Many of these are free-living in terrestrial or aquatic environments, but there are many important nitrogen-xing organisms that have developed mutualistic associations with other organisms.
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Two important examples are the Azolla Anabaena mutualistic symbiosis, which increases nitrogen availability in rice paddies, and many dierent fungalcyanobacterial associations that are termed lichens. Much research has been focused on stimulating nitrogen-xing microorganisms, either through cultivation practices or by genetic engineering, in order to increase the productivity of agricultural systems. In the environment, the relative rates of nitrogen cycling processes, particularly nitrogen xation, denitrication and nitrication, determine the availability of nitrogen for primary production. In soils and aquatic ecosystems, large amounts of nitrogen can be stored in complex organic matter (dissolved and particulate) that results from the death and decay of macro- and microorganisms. This nitrogen is available to many heterotrophic organisms, although the rate of decomposition and liberation of ammonium (mineralization or ammonication) can be slow. Plant growth in terrestrial ecosystems, be it natural vegetation (including grasslands and forests) or crops, is often limited by the availability of nitrogen (although other macro- and micronutrients also often limit productivity in both terrestrial and aquatic systems). Agricultural practices usually involve fertilization with some form of nitrogen. Microscopic, waterborne (planktonic) algae and bottom-dwelling macroscopic higher plants (macrophytes) are the major primary producers in aquatic systems, and the growth of both groups is often limited by the availability of nitrogen and phosphorus. Nitrogen xation can be important in many freshwater lakes, particularly if there are high concentrations of dissolved phosphorus that drive the ecosystem into nitrogen limitation. Sometimes the nitrogen-xing organisms that form resulting blooms in such systems are lamentous cyanobacteria (blue-green algae), which can form unattractive mats in water and on beaches, with associated odours and sometimes toxicity. The terrestrial and aquatic ecosystems are linked by nitrogen being transported from soils to surface water through runo. The anity of soil minerals for the dierent forms of nitrogen determines the extent of nitrogen loss in surface runo. The exchange of nitrogen between terrestrial and aquatic systems is thus controlled by the nature of the nitrogen cycle in the terrestrial environment. Human activities have substantially aected the nitrogen and carbon cycles on Earth (Vitousek et al., 1997). Agricultural practices over the centuries have contributed signicantly to inputs of nitrogen in terrestrial environments, which impacts the quality of lakes, rivers and even the marine environment (particularly in coastal areas). Combustion of fossil fuels in automobile engines and power plants produces nitrogen oxides (largely nitric oxide, but often termed NOx to account for all of the oxidation end products) that are emitted to the atmosphere. These compounds react with other compounds in the atmosphere, and can be involved in the formation of

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Biogeochemical Cycles

tropospheric ozone that can have a range of deleterious eects (Chameides et al., 1994). The deposition of these oxides of nitrogen in terrestrial and aquatic ecosystems can be an important source of nitrogen as a nutrient (Paerl, 1985; Aber et al., 1989). Many forested ecosystems, particularly in temperate regions, may be limited by the availability of nitrogen. The atmospheric deposition of nitrogen emitted from human activities may ultimately surpass the ability of these systems to retain nitrogen (nitrogen saturation (Aber et al., 1989)) within the watershed, resulting in higher concentrations of nitrogen in surface runo. In addition to the role of nitrogen as a nutrient, the NOx in the atmosphere form nitric and nitrous acids, which are an important component of acidic deposition (acid rain). Therefore, nitrogen saturation of watersheds can result in acidication, as well as nutrientenrichment, of surface waters. Other human activities aect the global nitrogen cycle by contributing nitrogen to terrestrial systems through agricultural practices, industry or wastewater disposal, and land use management practices may have deleterious eects on the global environment owing to perturbations of the nitrogen cycle. Nitrous oxide is a greenhouse gas, and is also involved in destruction of stratospheric ozone. Nitrous oxide concentrations are increasing in the atmosphere, which may be the result of a number of factors, including the burning of biomass and the general nitrogen-enrichment of the environment through fertilization and atmospheric deposition of anthropogenic emissions. The global nitrogen cycle is controlled to a large extent by biological processes, but has been greatly aected by human activities. Anthropogenic eects on the nitrogen cycle include increased contribution of xed nitrogen through the use of fertilizers, but also as a result of nitrogen xation in internal combustion engines and the combustion of fossil fuels (Galloway et al., 1995; Vitousek et al., 1997). Land use practices such as draining wetlands may have major consequences from the removal of habitats that are normally important in removal of nitrogen from the ecosystem through denitrication. These perturbations of the nitrogen cycle have wide-ranging eects throughout the biosphere, hydrosphere and atmosphere of Earth. Eects of this nitrogen enrichment have been suggested to result in decreased plant biodiversity, increased plant stress, and decrease in water quality of lakes and even of the oceans.

production of reactive metabolic products (Ehrlich, 2 2 1997). Bacteria are known that oxidize AsO2 to AsO3 4 , 32 31 and, in the presence of Fe , AsO4 can form the mineral scorodite (FeAsO4 . 2H2O). Some other bacteria and fungi 2 2 are known that reduce AsO3 to AsO2 , AsH3, 4 HAs(CH3)2 or As(CH3)3. The last three reduction products are volatile. Some acidophilic iron-oxidizing bacteria can release antimony contained in various sulde minerals. At circumneutral pH, Stibiobacter senarmontii can oxidize Sb2O3 to Sb2O5. Microbial reduction of Sb(v) has not so far been reported. Various mercury-resistant bacteria have been shown to be able to reduce Hg2 1 and some organic mercury compounds, such as phenyl and methyl mercury, to volatile Hg0. Other bacteria and fungi have been shown to be able to transform Hg2 1 to (CH3)Hg 1 and (CH3)2Hg. Various organic compounds, including products of microbial metabolism, can oxidize Hg0 to Hg2 1 . Thiobacillus ferroxidans has been shown to be able to 1 under aerobic oxidize U4 1 enzymatically to UO2 2 conditions, and others like Desulfovibrio desulfuricans 1 to UO2 under anaerobic have been shown to reduce UO2 2 conditions, the product being water-insoluble. UO2 can 1 under acid conditions by Fe3 1 also be oxidized to UO2 2 21 generated from Fe by acidophilic iron-oxidizing bacter1 can ia like Thiobacillus ferrooxidans. Furthermore, UO2 2 be reduced by H2S produced by sulfate-reducing bacteria in their reduction of sulfate.

References
Aber JD, Nadelhoer KJ, Steudler P and Melillo JM (1989) Nitrogen saturation in northern forest ecosystems: excess nitrogen from fossil fuel consumption may stress the biosphere. BioScience 39: 378386. Chameides WL, Kasibhatla PS, Yienger J and Levy H II (1994) The growth of continental-scale metro-agro-plexes, regional ozone pollution, and world food production. Science 264: 7477. Ehrlich HL (1996) How microbes inuence mineral growth and dissolution. Chemical Geology 132: 59. Ehrlich HL (1997) Microbes and metals. Applied Microbiology and Biotechnology 48: 687692. Galloway JN, Schlesinger WH, Levy H II, Michaels A and Schnoor JL (1995) Nitrogen xation: anthropogenic enhancementenvironmental response. Global Biogeochemical Cycles 9: 235252. Ghiorse WC and Ehrlich HL (1992) Microbial biomineralization of iron and manganese. In: Skinner HCW and Fitzpatrick RW (eds) Biomineralization. Process of Iron and Manganese. Modern and Ancient Environments, Catena Supplement 21, pp. 7599. Cremlingen: Catena Verlag. Happell JD and Wallace DWR (1998) Removal of atmospheric CCl4 under bulk aerobic conditions in groundwater and soils. Environmental Science and Technology 32: 12441252. Molina MJ and Rowland FS (1974) Stratospheric sink for chlorouoromethanes: chlorine atom catalysed destruction of ozone. Nature 249: 810812. Paerl HW (1985) Enhancement of marine primary production by nitrogen-enriched acid rain. Nature 316: 747749.

Other Elemental Cycles

Some elements such as As, Sb, Hg and U, even though not normal constituents of protoplasm, may nevertheless participate in biogeochemical cycles of their own. This is in part due to the ability of specic microbes to aect their chemical state through redox interaction or through

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Biogeochemical Cycles

Shorter JH, Kolb CE, Crill PM, et al. (1995) Rapid degradation of atmospheric methyl bromide in soils. Nature 377: 717719. Ullman WJ, Kirchman DL, Welch SA and Vandevivere P (1996) Laboratory evidence for microbially mediated silicate mineral dissolution in nature. Chemical Geology 132: 1117. Vitousek PM and Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13: 87115. Vitousek PM, Aber JD, Howarth RW et al. (1997) Human alterations of the global nitrogen cycle: sources and consequences. Ecological Applications 7: 737750.

Further Reading
Butler JH and Rodriguez JM (1996) Methyl bromide in the atmosphere. In: Bell CH, Price N and Chakrabarti B (eds) The Methyl Bromide Issue, pp. 2890. New York: Wiley. Capone DG and Carpenter EJ (1982) Nitrogen xation in the marine environment. Science 217: 11401142. Cicerone RJ and Oremland RS (1988) Biogeochemical aspects of atmospheric methane. Global Biogeochemical Cycles 2: 299327. Conrad R (1996) Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Microbiological Reviews 60: 609640. Ehrlich HL (1993) Bacterial mineralization of organic carbon under anaerobic conditions. In: Bollag JM and Stotzky G (eds) Soil Biochemistry, vol. 8, pp. 219247. New York: Marcel Dekker. Ehrlich HL (1996) Geomicrobiology, 3rd edn. New York: Marcel Dekker.

Galloway JN and Likens GE (1981) Acid precipitation: the importance of nitric acid. Atmospheric Environment 15: 10811085. Khalil MAK and Rasmussen RA (1984) Carbon monoxide in the Earths atmosphere: increasing trend. Science 224: 5456. Lashof DA and Ahuja DR (1990) Relative contributions of greenhouse gas emissions to global warming. Nature 344: 529531. McCready RGL and Gould WD (1990) Bioleaching of uranium. In: Ehrlich HL and Brierley CL (eds) Microbial Mineral Recovery, pp. 107125. New York: McGraw-Hill. Prinn RG and Fegley B Jr (1987) The atmospheres of Venus, Earth, and Mars: a critical comparison. Annual Review of Earth and Planetary Science 15: 171212. Prinn RG, Weiss RF, Miller BR et al. (1995) Atmospheric trends and lifetime of CH3CCl3 and global OH concentrations. Science 269: 187 192. Stacey G, Evans HJ and Burris RH (1992) Biological Nitrogen Fixation. New York: Chapman and Hall. Sundquist ET and Broecker WS (eds) (1985) The Carbon Cycle and Atmospheric CO2: Natural Variations Archaean to Present, Geophysical Monograph 32. Washington DC: American Geophysical Union. Tans P, Fung IY and Takahashi T (1990) Observational constraints on the global atmospheric CO2 budget. Science 247: 14311438. Walker JCG (1993) Biogeochemical cycles of carbon on a hierarchy of time scales. In: Oremland RS (ed.) Biogeochemistry of Global Change, pp. 328. New York: Chapman and Hall. Wolfe RS (1964) Iron and manganese bacteria. In: Heukelekian H and Dondero N (eds) Principles and Applications in Aquatic Microbiology, pp. 8297. New York: Wiley.

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ENCYCLOPEDIA OF LIFE SCIENCES / & 2001 Nature Publishing Group / www.els.net