14 Biogeochemical Cycles
distinct populations with a wide variety of metabolic
functions, but which are coordinated within a small space.
The association of various bacterial metabolisms present
in microbial mats induces the formation of chemical
microgradients (Des Marais 2003). For example, in the pres-
ence of light, oxygenic photosynthesis produces dioxygen at
the surface (up to 0.5–1 mm), thereby establishing a gradient
of dioxygen from the surface to the bottom of the mat. In
contrast, a gradient of sulfide appears due to the sulfate-
reducing activity in the deeper zones of the mat (1–3 mm).
This sulfide concentration decreases in the upper layers,
primarily because of the activity of aerobic and anaerobic
sulfo-oxidizing bacteria. In addition, a pH gradient is
established from the surface to the bottom of the mat, created
by the high photosynthetic activity of cyanobacteria coupled
with the low buffering capacity of microbial mats. The
absorption of solar radiations by photosynthetic organisms
and by sediments may also establish a light gradient in
microbial mats. The formation of these gradients relies on
the metabolic richness of the system and the proximity of
different micro-environments created by the superposition
of gradients. The unstable equilibrium of this system can be
observed when changing the gradient of light that affects the
activity of photosynthetic microorganisms. In fact, physico-
chemical gradients within microbial mats fluctuate strongly
with the circadian cycle (Fig. 14.44), typically with the
spatial rearrangements of the associated microbial
communities (van Gemerden 1993). Thus, during a circadian
cycle, vertical shifts in anoxygenic phototrophic bacteria,
denitrifying bacteria, sulfate-reducing microorganisms, and
chemolithotrophic sulfur-oxidizing bacteria, could be
observed within microbial mats.
The establishment of physical and chemical gradients at
the micrometer scale in microbial mats allows the coexis-
tence of various metabolisms (Fig. 14.44). Cyanobacteria
are the pioneer builders of microbial mats due to their ability
to produce exopolymeric matrices. Cyanobacteria are also
considered the main producers of dioxygen on earth. Both
filamentous and unicellular forms group complex
microorganisms, with huge diversity (cf. Sect. 6.6.2).
These primary producers are typically oxygenic photosyn-
thetic organisms, producing organic matter and dioxygen
from solar energy used to fix CO2. In addition, many
cyanobacteria have the ability to fix dinitrogen. These
characteristics explain why they can colonize surface
habitats that are originally poor in organic matter and in
nutrients. This colonization enriched the surrounding
medium in organic matter, in dioxygen, and in nitrogenous
compounds, allowing the development of other
microorganisms. Among these microorganisms, aerobic
599
heterotrophic bacteria will use the organic matter as carbon
and energy source, by performing an aerobic respiration
based on the dioxygen released by cyanobacteria. Faculta-
tive anaerobic heterotrophs are also able to develop in such
ecosystems. This is particularly the case of denitrifying
bacteria and other nitrate respiring bacteria that will benefit
from ammonium oxidizing activities by nitrifying bacteria
or by those microorganisms that are able to oxidize ammo-
nium under anaerobic conditions (cf. Sect. 14.3.5). Fermen-
tative bacteria, i.e. strict or facultative anaerobes, also have
an important role in microbial mats, by participating in the
degradation of organic matter and by providing organic
substrates (organic acids, alcohols) or minerals (dihydrogen)
for other anaerobic microorganisms. Among them, the activ-
ity of sulfate-reducing microorganisms is often very impor-
tant in these ecosystems. From their activity, the generated
sulfide will be oxidized by anoxygenic phototrophic sulfur
bacteria and chemolithotrophic sulfur-oxidizing bacteria. In
these shallow ecosystems, high wavelengths (near-infrared)
penetrate the most deeply, and among anoxygenic photosyn-
thetic bacteria, those containing bacteriochlorophyll a and b
are favored (phototrophic purple bacteria). Other
microorganisms such as methanogenic archaea and iron-
reducing or iron-oxidizing bacteria are also present. Finally,
eukaryotic microorganisms, photosynthetic or not, are also
present in these ecosystems and have a role in the regulation
of prokaryotic populations, primarily as predators. Thus, a
photosynthetic microbial mat groups, on a very narrow spa-
tial scale (a few mm deep), all functions that sustain a proper
functioning of biogeochemical cycles, particularly those of
carbon, nitrogen, sulfur, and iron.
14.4.4.4 Deep Ocean Hydrothermal Vents
These ecosystems, located in hot mid-ocean ridges
(contraction areas with faults), are life oases characterized
by an abundant fauna thriving in inhospitable, cold, and dark
deep seafloors. In these environments, seawater enters faults
of the Earth’s crust and, subjected to high temperatures and
pressures, becomes a hot, acidic, and reduced fluid that is
enriched in metal elements, in sulfide and in dihydrogen,
before being injected back to the oceanic waters as hydro-
thermal vents.
Hydrothermal vents (cf. Sect. 10.3.1) are resurgences
of fluid whose characteristics may vary depending on
environmental conditions. Some of these hydrothermal
vents, called black or white smokers, consist of hot
(200–400  C) and anoxic fluid which is ejected into cold
(4  C) and oxygenated deep oceanic waters. These hydro-
thermal vents are enriched in H2S whose concentration
varies depending on the content of metallic elements
600
(formation of iron metal sulfides, manganese, zinc, copper),
differentiating black from white smokers. These sources
are also enriched in oxidized (CO, CO2) and reduced
(CH4) carbon, and in calcium which precipitates in the
form of CaSO4 in contact with oceanic waters. This
CaSO4 is at the origin of the chimney wall formation of
smokers, which then are enriched in metal sulfides and in
iron and manganese oxides.
Ecosystems that develop in deep hydrothermal vent
receive no solar radiation and biomass production is due
to chemosynthetic processes (Jannasch and Mottl 1985).
Autotrophic microorganisms that grow in these ecosystems
used reduced sulfur compounds (sulfur-oxidizing
chemolithoautotrophs) and other reduced mineral
compounds (such as NH3, H2, Fe2+, or Mn2+) as energy
sources. Methylotrophic microorganisms also colonize
these environments. Many hyperthermophilic and thermo-
philic microorganisms grow directly on the walls of smokers
in the form of microbial mats, or in the water around the
plume of the hydrothermal source. Chemosynthetic
microorganisms are at the origin of a food chain involving
planktonic or benthic animals, filter-feeding organisms and
grazers, including worms, crustaceans, molluscs, and fishes.
The distribution of animal populations is established
according to the distance to the smoker, the different species
being arranged in concentric rings around the source-
ejection depending on the prevailing extreme conditions
(temperature, pH, concentrations of sulfide, and metal).
In addition, in these ecosystems, symbioses between
chemolithotrophic sulfur-oxidizing microorganisms and
metazoans (worms, bivalves) have been described (cf. Sect.
10.3.1). For example, red giant tubeworms (Riftia
pachyptila), which lack digestive tube, feed through the
symbiotic activity of sulfur-oxidizing microorganisms
(endobionts) housed in a particular organ, the trophosome.
The substrates required for the growth of microorganisms
(H2S, CO2, and O2) are provided by the circulatory system of
the worm, and part of the organic matter synthesized by
bacteria is used by worms for their diet. Other symbioses
involving exobiontes, often located in the gills of aquatic
organisms in bacteriocytes, have also been described.
Such symbioses also exist in coastal marine sediments
between bivalves (clams) and chemosynthetic sulfur-
oxidizing bacteria.
Because of the total absence of solar light, deep hydro-
thermal ecosystems therefore seem to exclusively depend
on biomass production by chemosynthetic processes.
However, it was discovered that these areas also contain
phototrophic green sulfur bacteria (Prosthecochloris sp.)
which use geothermal radiations (near-infrared radia-
tions between 750 and 1,050 nm) as energy source.
The question of their exact role still remains open (Beatty
et al. 2005).
J.-C. Bertrand et al.
14.5 Cycles of Metals and Metalloids
14.5.1 Introduction
Many microorganisms are involved in the biogeochemical
cycles of metals and metalloids, primarily by modifying their
oxidation level and/or their chemical forms. Among these
elements, some are essential to life (iron, manganese, cobalt)
while others are toxic at low doses (mercury, cadmium, arse-
nic). Their biological transformations are typically related
either to energetic metabolisms (donor or electron acceptor)
or to resistance and detoxification mechanisms. They can also
be due to incidental or indirect mechanisms (biomethylation,
indirect reduction). Metals and metalloids are also subject to
non-enzymatic redox reactions and it is often difficult to dis-
tinguish between changes of biotic origin and those generated
by strictly physico-chemical processes. The relative impor-
tance of these biotic versus abiotic transformations depends on
environmental conditions, such as the presence or absence of
oxygen, and the prevailing pH (cf. Chap. 16.9).
This chapter will focus on the biogeochemical cycles of
iron and manganese which are among the most abundant
metals on the planet, and whose cycles are closely related.
The standard potential of the couple Mn(IV)/Mn(II) is at
+770 mV, and that of the couple Fe(III)/Fe(II) at +380 mV.
The oxidized forms of iron Fe(III) and manganese Mn(IV)
are excellent respiratory electron acceptors. Thus, the degra-
dation of many organic compounds is coupled to the dissim-
ilatory reduction of Fe(III) and Mn(IV), which play an
important role in the anaerobic degradation of organic mat-
ter (cf. Sect. 3.3.2). Microorganisms involved in the dissimi-
latory reduction of these two metals are frequently the same.
For example, Shewanella putrefaciens produces the energy
necessary to its growth by coupling the oxidation of formate
into CO2 to the reduction of iron or manganese:
Formate þ 2 FeðIIIÞ þ H2 O ! HCO3  þ 2 FeðIIÞ þ 2Hþ
Formate þ 2 MnðIVÞ þ H2 O ! HCO3  þ 2 MnðIIÞ þ 2Hþ
In the presence of these electron acceptors, lactate and
pyruvate are also oxidized but not completely mineralized
(acetate production). In part against the dissimilatory reduc-
tion, many bacterial species derive their energy from the
oxidation of iron and manganese. These organisms can be
either aerobic (Thiobacillus spp. for example) or denitrifying
anaerobic chemolithotrophs, or anoxygenic phototrophs
(Rhodovulum robiginosum and Rhodovulum iodosum).
Because of their abundance, iron and manganese have
been the most extensively studied metals, but the spectrum
of metals used by microorganisms is much larger.
Microorganisms are involved in the biogeochemical cycles
14 Biogeochemical Cycles
of many metals and metalloids, including reduction processes
and, more rarely, oxidation activities. Some microorganisms
are capable of growth by using reduced forms of arsenic and
selenium as electron donors. The case of arsenic to which
certain microorganisms oxidize arsenite (As(III)) to arsenate
(As(V)) is the best documented (Oremland and Stolz 2003)
and particularly interesting. Indeed, in the case of arsenic, the
reduced form, i.e. arsenite, is more toxic because its availabil-
ity is higher compared with the oxidized form. Some
microorganisms that oxidize As(III) use this ability as a
resistance mechanism to detoxify As(III) to As (V), which is
less toxic and less prone to enter the cell. Other organisms,
chemolithotrophs, are capable of coupling the oxidation of As
(III) (electron donor) to the reduction of oxygen or nitrates
involved as terminal electrons acceptors.
Among the many metals which can be reduced by micro-
organisms, uranium U(VI) can be reduced to uranium U(IV)
or chromium Cr(VI) to chromium Cr(III), but arsenic (As),
selenium (Se), vanadium (V), molybdenum (Mo), copper
(Cu), gold (Au), mercury (Hg; Box 14.14), or silver (Ag)
Box 14.14: Iron in Ocean
Stephane Blain
The Iron Cycle in the Ocean
Concentrations of dissolved iron in the modern
ocean are extremely low (often less than 1 nanomole.
L1). This is partly due to the low solubility of this
element in seawater, which is an oxygenated lightly
alkaline environment (pH ¼ 8). However, over geo-
logical time this has not always been the case. Notably,
iron concentrations were much higher during the
Archean (3.8–2.5 Ma) and Proterozoic (2.5–0.5 Ma),
periods when oxygen was absent or found at very low
levels. The first living organisms appeared in the
oceans during these periods have therefore widely
incorporated iron into their metabolisms. Indeed, iron
has two oxidation states, Fe (II) and Fe (III), which
makes it particularly useful for electron transport within
the cells. Iron has become an essential element in many
biochemical functions, such as respiration, photosyn-
thesis, dinitrogen fixation, and nitrate reduction.
The discovery of low levels of iron in the ocean is
relatively recent. Indeed, measuring iron concentra-
tions in the ocean requires so-called ultra-clean
S. Blain (*)
Laboratoire d’Océanographie Microbienne, LOMIC UMR
CNRS-UPMC, Observatoire Océanologique de Banyuls, 66650
Banyuls-sur-Mer, France
(continued)
601
Box 14.14 (continued)
techniques first used in oceanography in the 80s
(Bruland et al. 1979). They are based on non-metallic
sampling equipments and they follow strict protocols
for storage and analysis of the samples. The low iron
supply to the ocean compared with the physiological
demand of the marine microorganisms results in a
limitation of photosynthesis and growth of phyto-
plankton in very large ocean areas (e.g., Southern
Ocean, Equatorial sub-Arctic Pacific). This has pro-
found climatic implications because the process
called biological pump of CO2, which includes pho-
tosynthesis and transport of organic carbon in the
deep layers of the ocean and ultimately to the
sediments, is the main oceanic mechanism which
removes CO2 from the atmosphere (Sarmiento and
Gruber 2006).
A major breakthrough in the demonstration of iron
limitation of biological production in the ocean has
clearly resulted from the realization of a dozen of
artificial fertilization experiments on a small scale
(approximately 100 km2) between 1993 and 2009.
During these experiments, the addition of iron (several
tons) stimulates organic production in the surface layer
(Boyd et al. 2007). This results in an increase in the
concentration of chlorophyll and a decrease of the
partial pressure of CO2 in water. Fertilization alters
the structure of the phytoplankton community in pro-
moting growth diatoms. In some experiments, the
effect on the second trophic level (zooplankton) was
also observed. These experiments did not, however,
clearly demonstrated that the carbon was then trans-
ferred into the deep ocean. But, this was demonstrated
in the study of a region naturally fertilized by iron: the
Kerguelen Plateau in the Southern Ocean (Blain et al
2007). This region has high chlorophyll concen-
trations, while the surrounding waters are much poor
(Box Fig. 14.23). In this study, it was demonstrated
that the increase in biological activity was caused by
an enhanced iron supply, and that this led to an
increase in the deep export of carbon.
Natural fertilization of surface waters of the
Southern Ocean therefore enhanced the biological
pump of CO2.
In the present ocean, the main external source of
iron is the deposition of dust from natural (deserts) or
anthropogenic (industry, transport) origins. Two
types of depositions are distinguished: the wet depo-
sition (rain) and the dry deposition (Jickells et al.
2005). The impact of these deposits on the biological
(continued)
602 J.-C. Bertrand et al.

Box 14.14 (continued) Box 14.14 (continued)

activity is still uncertain, since these events are spo-
radic and relatively difficult to study with conven-
tional oceanographic campaigns. However, there are
some clues suggesting that dustinputs in oligotrophic
regions of the ocean (e.g., Mediterranean, subtropical
gyres) could benefit diazotrophic organisms. Indeed,
the contribution of atmospheric iron would favor
N2 fixation metabolism that has a high iron require-
ment, and thus provide a competitive advantage
to these organisms in a medium poor in nitrogen
(Mills et al. 2005).

Major Unknowns of Iron Cycle, Speciation,

Box Fig. 14.23 Satellite image showing high concentrations
of chlorophyll due to the natural iron fertilization of the surface
water located above the Kerguelen Plateau in the Southern
Ocean
and Bioavailability
Iron is present in very many physical–chemical forms
in the ocean. It could be present as particles, colloids,
or dissolved species. Dissolved iron is mainly in its
oxidized form (Fe III) complexed by organic
molecules. Microorganisms have therefore developed
appropriate strategies to acquire iron from of these
different forms (Box Fig. 14.24).

FeHem
Fe(lll)L

L Fe(lll)Sid

e-

Fe(lll)L Fe(ll)+L
Sid

Sid e-

Fe(lll)L Fe(lll)+L Fe(lll)L Fe(lll)+L

Prokaryote Eukaryote

Box Fig. 14.24 Schematic drawing of a few examples of iron membrane proteins for the transport of the various forms of iron
acquisition mechanisms by marine microorganisms. Abbreviations: through the membrane. The circles represent reductases that reduce
Sid siderophore, Hem Hemin, L organic ligand. The cylinders are Fe(III) to Fe(II)

(continued) (continued)
14 Biogeochemical Cycles
Box 14.14 (continued)
All of these mechanisms are not yet known but
some pathways have been described (Morel et al.
2008). When iron is limiting, a number of bacteria
excrete molecules, siderophores (cf. Sect. 14.5.2) that
forms strong complex with iron. That allows them to
extract iron from other chemical species present in the
environment. The iron-siderophore complex is then
taken up by bacteria (Butler 1998). Eukaryotes seem
to have adopted a different strategy, which consists in
reducing Fe (III) at the surface of the cell to form iron
(II). This facilitates the dissociation of the organic
complexes and allows the transport iron into the cell.
Other mechanisms are likely to be discovered in the
future, such as direct transport of other iron complex
like heme-type. Detailed analysis of the growing num-
ber of genomes available for marine microorganisms
should allow rapid progress in this direction.
The Iron Cycle and Climate Geoengineering
The major role of iron in controlling the biological
pump of CO2 have inspired geo engeneering proposals
describing large scale iron fertilization of the ocean to
mitigate the atmospheric CO2 increase. A very large
majority the scientific community does not support this
idea. Indeed, the efficiency of a such manipulation of
the ocean is not firmly proven. The amount of carbon
that would be eventually stored would be very difficult
to assess. In addition, the side effects of such large scale
manipulations of a global ecosystem are not known and
could be dangerous (Strong et al. 2009).
can also be reduced. These reduction processes can be
related to energetic metabolisms (dissimilatory reduction),
or can be the result of an indirect reduction (reduction by
reduced iron or sulfide). The reduction of these elements is
interesting in the case of treatment processes of
contaminated sites, because the reduced forms are often
less toxic and/or less soluble (unlike iron and manganese).
14.5.2 The Cycle of Iron
14.5.2.1 Iron in the Environment
Iron is quantitatively the fourth constitutive element of the
earth’s crust. It is abundant in the continents and rare in the
oceans where iron resources are often a limiting factor for
primary production (Box 14.15).
Iron is present in the environment as oxides, carbonates,
sulfides, and hydroxides. It exists in different oxidation
603
states, ranging from 0 to +VI (ferrate), but only two of
these states are involved in biological pathways: Fe2+(II)
which is the reduced ferrous form, and Fe3+(III) which is
the oxidized ferric form. Iron is an essential element in some
enzymes: cytochromes, catalases, peroxidases, nitrite
reductases, and iron-sulfur metalloprotein complexes. It is
therefore an essential element in respiratory and photosyn-
thetic processes.
The greater part of iron found in the environment is
insoluble, the solubility of ferric ion being very low at
physiological pH. The solubility of Fe(II) form is substan-
tially greater, but in anoxic conditions. However, under
these conditions, iron is usually precipitated as black iron
sulfide (FeS) or even as pyrite (FeS2), the last one forming a
crystalline structure, highly insoluble and very difficult to
oxidize (Fig. 14.45, pathways 1 and 3).
The oxidation of pyrite requires the sum of chemical and
biological reactions involving two electron acceptors:
dioxygen and ferric ions. In the presence of sulfide (S2)
and when anaerobic conditions prevail, ferric iron (Fe3+) is
chemically (i.e. by abiotic processes) reduced to sulfide
(FeS) and ferrous iron (Fe2+) (Fig. 14.45, pathways 1 and
2). During this reaction, a small portion of sulfide (S2) is
oxidized to sulfur (S ) which participates in the formation of
pyrite by association with sulfide iron (Fig. 14.45, pathway
3). Sulfide iron can be chemically oxidized, in the presence
of oxygen, to ferric iron by releasing sulfur and thiosulfate
(S2O32) (Fig. 14.45, pathway 4).
14.5.2.2 Iron Assimilation by Microorganisms
The inventory of biological functions of iron shows that this
element is essential to life. In the cell, the iron must be in the
Fe2+ state. Due to its low solubility, living organisms have
developed systems to capture and incorporate iron
(Fig. 14.45, pathway 5). Indeed, many microorganisms
produce a wide variety of small organic molecules,
siderophores, capable of fixing Fe3+ with a very high effi-
ciency, ensuring its transport within the cell where it is
reduced and incorporated into the organic material.
Some aquatic bacteria, described as magnetotactic
microorganisms, such as Aquaspirillum magnetotacticum,
Magnetotacticum bavaricum, and Magnetospirillum
magnetotacticum, can transform iron extracellularly to crys-
tal of magnetite (Fe3O4) and construct “intracellular mag-
netic compasses” called magnetosomes (Bazylinski and
Frankel 2004), which are included in cytoplasmic vesicles
(Figure 14.46). Some magnetotactic bacteria do not synthe-
size magnetite but greigite (Fe3S4) (Farina et al. 1990). With
this structure, these motile bacteria can move to areas rich in
organic matter (water-sediment interface), by following the
Earth’s magnetic field. High concentrations of magnetotactic
bacteria were detected in anoxic marine sediments at
3,000 m depth (Petermann and Bleil 1993).
604 J.-C. Bertrand et al.

Box 14.15: Biogeochemical Mercury Cycle Box 14.15 (continued)

Rémy Guyoneaud Proteins involved in mercury reduction are encoded by
genes organizsed in the inducible mer operon, present
Mercury, whose chemical symbol Hg comes from the
in many Bacteria. In the absence of mercury (or at low
Latin name Hydrargyrum (liquid silver) has different
concentrations) MerR transcriptional regulatory pro-
chemical forms in the environment. Main species are
tein is linked to the mer promoter (PmerT) and
elemental mercury (Hg0, volatile), bivalent inorganic
represses the genes expression. In the presence of
mercury (Hg2+ or Hg(Il)), mostly combined with
inorganic mercury or methylmercury, the modification
organic matter, chloride, hydroxydes or sulfide (cinabar,
of the complex MerR-operator-promoter allows the
HgS), monomethylmercury (CH3Hg+) and
operon transcription and thus the synthesis of trans-
dimethylmercury (organic volatile species, (CH3)2Hg).
port proteins, catalytic enzymes, and regulation pro-
Mercury toxicity, is due to its capacity to combine with
tein (MerD) involved in the repression when mercury
thiol groups in proteins. In contrast to biogeochemical
concentration decreases. Mercury reduction is not
cycles of carbon, nitrogen, or sulfur, toxic mercury in
linked to an energetic metabolism (energy conserva-
not an essential element for life. Micro-organisms par-
tion). After its transport inside the cell, inorganic
ticipate in the mercury biogeochemical cycle but it is not
mercury (Hg(II)) is reduced to volatile elemental mer-
used through energetic metabolisms (electron donor or
cury (Hg(0)) by a mercury reductase (MerA). The mer
acceptor) nor assimilation/degradation mechanisms.
operon may comprise one particular gene (merB)
Biological transformations of mercury are linked to
encoding for an organomercurial lyase involved in
resistance mechanisms (transformation of the toxic
methylmercury detoxication. The presence of this
forms to the less toxic volatile elemental mercury) and
gene and its related enzyme allows a broad spectrum
to mercury methylation mechanisms that enhance mer-
resistance (inorganic mercury and methylmercury).
cury accumulation in food webs (Box Fig. 14.25).
The methylmercury is first demethylated to CH4 and
The reduction of inorganic mercury to volatile Hg0
inorganic mercury and the later is afterward reduced
is a prokaryotic resistance mechanism whose genetic
to elemental mercury through MerA reductase. This
determinism is well known (Barkay et al. 2003).

Hg2+ Hg0
CH4 CH3Hg+

Porin External membrane

MerP
Cys Cys

Periplasm
Cys Cys Cys

Cys Cys Cys

Internal membrane
MerT
Cys Cys Cys
Hg0
RSH 2RSH
Cytoplasm

MerB Cys MerA

Box Fig. 14.25 Resistance mechanisms to inorganic mercury and Mercury binds to proteins through cysteine residues, cytoplasmic
methylmercury through proteins encoded on Tn501 transposon transport occurs through small peptidic thiols (RSH) (Redrawn from
(merT, merP, merA) as well as organomercurial lyase (MerB). Barkay et al. 2003)

(continued) (continued)
14 Biogeochemical Cycles
Box 14.15 (continued)
demethylation is called reductive demethylation.
An oxidative demethylation, producing CO2 and
inorganic mercury, called oxidative demethylation,
has been demonstrated under anoxic conditions (sul-
fate reducting or methanogenic conditions).
In ecosystems numerous abiotic processes (photo-
chemical or chemical) and biotic processes are
involved in methylmercury or dimethylmercury
production. The methylmercury accumulates much
more easily in food webs, due to its lipophilic
characteristics. Its half life in biota is much longer
than the one of inorganic mercury and it accumulates
in the central nervous system. Thus, activities that
contribute to methylmercury production are of interest
for human health. Indeed, methylmercury production
(due to acethaldehyde production) and its accumula-
tion in food webs was implicated in the Minameta
disease in Japan (1950–1960). Methylmercury, may
also be produced through biological activities. Some
are indirect mechanisms (non-enzymatic) due to bio-
genic molecules such as iodomethane, methylated
metals, and other metabolites. Mercury methylation
through enzymatic processes mainly occur under
anoxic conditions and it has been demonstrated that
sulfate-reducing bacteria are among the main mercury
Chemical
oxydations
O3
(CH3)2Hg
Air
water
Food Web
Natural
sources
(CH3)2Hg CH3Hg+
(6)
(2) (3)
(CH3)2Hg CH3Hg+
(6)
Sediment
(CH3Hg)2S
Box Fig. 14.26 Biogeochemical mercury cycle showing transfor-
mation and transfers between different ecosystem compartments.
Transformations that may be due to direct biological processes
are indicated with plain arrows. 1 inorganic mercury reduction
through mercury reductase (MerA) or small metabolites originated
from primary production, 2 reductive demethylation, 3 oxydative
(continued)
605
Box 14.15 (continued)
methylators (Compeau and Bartha 1985) even if meth-
ylmercury production capacities may vary a lot in
between strains/populations (Ranchou-Peyruse et al.
2009). Some other microorganisms such as some
iron reducers (Geobacter spp.) may also
producemethylmercury (Fleming et al. 2006). Finally,
the genetic determinisms of methylmercury production
has been elucidated (Parks et al. 2013) and these genes
have been found to be distributed in many other
organisms such as methanogens.
Mercury biomethylation increases mercury
bioaccumulation in organisms and mercury bioampli-
fication through food webs to higher trophic levels
(carnivorous fishes, humans) where its concentration
may be 107 times the concentration in the water. Since
mercury anthropic emissions have increased three to
four times since the industrial era (fossil energy burn-
ing, mining activities, other industrial activities), the
global biogeochemical mercury cycle has been
modified in terms of fluxes. In addition, in some
ecosystems such as the Amazonian region, goldmining
activities has implications for mercury contamination
and methylmercury bioamplification in food webs.
Methylmercury contamination and poisoning is of
public health concern (Box Fig. 14.26).
Hg0
O3
Hg2+ Volatilisation
Precipitations
Hg2+
Anthropic
sources
(2) (1)
Hg2+p Hg0
(4)
(5)
Evaporation
(1)
Hg2+p Hg0
(5) (4)
H2 S
(7)
HgS
demethylation, 4 elemental mercury oxidation (catalase), 5
biological methylation in sediment or particulate material (anoxic
conditions), 6 dimethylmercury production, 7 reactions with sulfide
producing cinabar (HgS), dimethylmercury sulfide. Hg2+p, particu-
late inorganic mercury bond to organic or inorganic particles
606 J.-C. Bertrand et al.

8
Acidic pH

6 S0

Neutral pH

4
7 5
Fe 2+ Fe3+ Siderophores

Phototrophic bacteria
3 9
FeS2 FeS Nitrate reducing bacteria Cell
10 incorporation
Pyrite Aromatic compounds MO
CO2
Fermentation Sugar
1 2 products: Amino
11 acetate, H2 ... acids
2-
+S Long chain fatty acids
Oxidation Assimilation
Reduction Abiotic transformations

Fig. 14.45 Iron biogeochemical cycle showing the different biological pathways (Drawing: M.-J. Bodiou)

a function of pH. At neutral pH, ferrous iron is spontaneously

Fig. 14.46 Magnetotactic bacteria (Vibrio sp.) The magnetosomes
form chains inside the cell (1.5  0.4 μm) (Courtesy from Long-Fei
Wu)
oxidized (by abiotic pathway) to ferric iron (Fig. 14.45, path-
way 6). However, at oxic–anoxic interfaces, it can also be
oxidized by bacteria such as Gallionella ferruginea,
Leptothrix ochracea, or Sphaerotilus natans (Fig. 14.45, path-
way 7). The biological oxidation of iron is the most important
at acidic pH (less than 3) where the Fe2+ form is stable
(Fig. 14.45, pathway 8). This oxidation is carried out by
autotrophic acidophilic micro-organisms such as Acidithio-
bacillus ferrooxidans or Leptospirillum ferrooxidans, which
fix CO2 via the Calvin cycle and use iron as electrons donor
and oxygen as terminal electrons acceptor. The respiratory
chain involved in this mechanism is described in Chap. 3
(Fig. 3.18d). These bacteria are commonly encountered in
polluted acidic environments and their metabolism is used
in the bioleaching process (cf. Sect. 16.9.2). They must
oxidize a large amount of iron to grow. Indeed, the energy
released during the oxidation of ferrous iron (Fe2+) to
ferric iron (Fe3+) is low, because only one electron is
transferred in this reaction:
þ
2 Fe2þ þ 2H
 þ0 ½ O2 ! 2 Fe

3þ

14.5.2.3 Iron Oxidation þ H2 O ΔG0 ¼ 65:8 kJ

The oxidation of Fe(II) to Fe(III) iron by chemical or
microbial processes depends on pH and oxygen concentra- The oxidation of iron in such environments causes signif-
tion. In oxic conditions, the oxidation pathways of iron will be icant deposits of iron oxides which may be visualized
14 Biogeochemical Cycles
Fig. 14.47 Ferric iron accumulation in an acidic stream (Carnoules,
France) (Photograph Rémy Guyoneaud)
as rusty-colored deposits at the surface of sediments
(Fig. 14.47).
The oxidation processes of iron are at the origin of
specific geological formations, visible as brown oxidized
iron strata in ancient sedimentary rocks (i.e. BIFs for
“Banded Iron Formation”). These accumulations of oxidized
iron consist of hematite (Fe2O3) and magnetite (Fe3O4). The
majority of these structures, dated between 2.5 and 1.8
billion years, likely result from iron oxidation by oxygen
produced by cyanobacteria and contain 20 times the amount
of oxygen in the atmosphere of the present planet. Other
hypotheses suggest that the formation of these geological
layers is due to the anaerobic oxidation of iron either by
chemosynthesis or by anoxygenic photosynthesis.
The oxidation of Fe(II) does not happen only in oxic
environments, it also occurs in anoxic conditions at neutral
pH. Indeed, in addition to aerobic acidophilic and neutro-
philic chemolithotrophs, anaerobic oxidation of iron is also
performed by bacteria which use nitrate as electrons accep-
tor (Straub et al. 1996, 2004) (Fig. 14.45, pathway 10). The
description of this process in many natural ecosystems
suggests that it plays a significant role in the coupling of
nitrogen and iron cycles in anoxic sediments. Moreover,
some anoxygenic photosynthetic microorganisms oxidize
iron to fix CO2 by using solar energy (Ehrenreich and
Widdel 1994; Hegler et al. 2008) (Fig. 14.45, pathway 9).
Phylogenetically diverse, they are represented by purple
sulfur (Thiodictyon sp. strain F4), purple non-sulfur
(Rhodovulum iodosum and R. robiginosum) and green sulfur
(Chlorobium ferrooxidans) bacteria.
607
14.5.2.4 Iron Reduction
Iron reduction is carried out via both chemical and biological
processes. The latter case refers to the so-called anaerobic
respiration where iron is the terminal electrons acceptor.
This type of respiration is common in anoxic sediments,
soils, marshes, bogs, and has also been highlighted in deep
aquifers or fossil waters, oil reservoirs, continental hot
springs, and marine hydrothermal vents.
Because the oxidized forms of iron (and manganese)
are highly insoluble, they behave differently compared with
other potential soluble electron acceptors (oxygen, nitrate,
sulfate, or carbon dioxide), which diffuse within the cell. To
reduce these compounds, organisms will develop two
strategies (Lovley et al. 2004): either establishing a direct
contact with the electron acceptor (e.g. Geobacter
metallireducens) or produce “shuttle carriers ” that transfer
electrons from the surface membrane to iron (and manganese)
oxides (Shewanella spp, Geothrix fermentans).
The phylogenetic diversity of microorganisms capable
of dissimilatory reduction of iron is high, with
representatives in both Bacteria and Archaea domains.
The most studied micro-organisms belong to the genera
Shewanella, Geobacter, and Geospirillum. Hyperther-
mophiles reduce iron, such as Thermotoga maritima and
Thermodesulfobacterium commune (in the domain Bacte-
ria), and Pyrobacterium islandicum and Ferroglobus
placidus (in the domain Archaea) (Lovley et al. 2004).
Other electron acceptors can be used by microorganisms
which carried out the dissimilatory reduction of iron: oxy-
gen, other metals (manganese as already mentioned,
uranium, cobalt, chromium, gold), extracellular quinones
(humic substances are the most abundant source of extra-
cellular quinones), some sulfur compounds (S0), nitrate,
fumarate (Lovley et al. 2004).
Concerning the electron donors, the most frequently used
are organic acids (Fig. 14.45, pathway 11). If hydrogen is an
electron donor for several species of Geobacter and
Shewanella, acetate, which is the most important organic
electron donor in many environments, is the most frequently
used. The total oxidation of this molecule by Geobacter
metallireducens is as follows:
Acetate þ 8 Fe3þ þ 4 H2 O ! 2 HCO3  þ 8 Fe2þ
 0 
þ 9Hþ ΔG0 ¼ 233 kJ
This bacterium is also able to develop on a wide spectrum
of compounds, by coupling their oxidation to iron reduction:
benzaldehyde, benzoate, benzyl alcohol, butanol, butyrate,
ethanol, p-hydroxybenzaldehyde, p-hydroxybenzoate,
p-hydrybenzyl alcool, p-cresol, isobutyrate, isovalerate,
608
phenol, propanol, propionate, pyruvate, toluene, valerate
(Lovley 2006). Some examples (Lovley 1991):
benzoate þ 30 FeðIIIÞ þ 19 H2 O
! 7 HCO3  þ 30 FeðIIÞ þ 36 Hþ
toluene þ 36 FeðIIIÞ þ 21 H2 O
! 7 HCO3  þ 36 FeðIIÞ þ 43 Hþ
phenol þ 28 FeðIIIÞ þ 17 H2 O
! 6 HCO3  þ 28 FeðIIÞ þ 34 Hþ
p‐cresol þ 34 FeðIIIÞ þ 20 H2 O
! 7 HCO3  þ 34 FeðIIÞ þ 41 Hþ
Metabolism of sugars has also been demonstrated. It
produces enough energy to allow growth; oxidation may be
total (Küsel et al. 1999) or incomplete (Coates et al. 1998):
C6 H12 O6 þ 2 H2 O þ 8 FeðIIIÞ
! 2 CH3 COOH þ 2 CO2 þ 8 FeðIIÞ þ 8 Hþ
C6 H12 O6 þ 24 FeðIIIÞ þ 24 OH
! 6 CO2 þ 24 FeðIIÞ þ 18 H2 O
The metabolic capacities of microbial iron-reducers have
many environmental applications. The Geobacteraceae can
play an important role in the rehabilitation of deep anoxic
environments contaminated with aromatic hydrocarbons
(benzene, toluene, ethylbenzene, o-xylene, p-cresol, phe-
nol). Their action in the cleanup of groundwaters or
sediments contaminated by hydrocarbons was observed
and provides opportunities for the development of remedia-
tion techniques against contaminated sites (Jahn et al. 2005)
(cf. Sect. 16.8.3).
14.5.3 The Cycle of Manganese
14.5.3.1 Manganese in the Environment
The abundance of manganese in the earth’s crust was
estimated to be 0.1 %. Manganese can exist in different
oxidation states ranging from 0 to +VII (permanganate). In
the nature, only the states +II, +III, and +IV are commonly
found. The oxidation state of manganese is influenced by
chemical and physical characteristics of their environment.
In reduced sediments and at low pH, the form Mn(II), equiv-
alent to the soluble manganese ion Mn2+, is the most abun-
dant. The appearance of the insoluble (in water) oxidized
form, Mn(IV) that corresponds to the manganese dioxide
(MnO2), is favored at high pH and in oxidized environments.
J.-C. Bertrand et al.
However, even if environmental conditions favor changes in
the oxidation state, these chemical conversions are slow. The
oxidation and reduction of manganese in many biotopes are
mainly related to bacterial metabolism.
In some marine and freshwater habitats, precipitation of
manganese forms the so-called polymetallic nodules which
also contain other elements. Chemical analysis of these
nodules shows that they mainly consist of manganese
(20–30 %) and iron (6–15 %). Other metallic elements
such as nickel (1.34 %), copper (1.25 %), cobalt (0.25 %),
titanium (0.60 %), and aluminum (2.90 %) are also present
in these nodules. They also contain sodium, magnesium,
silica, oxygen, and hydrogen. The problem of the genesis
of these nodules is far from being resolved. Four origins are
possible:
1. “Hydrogenated”, slow precipitation of metallic elements
from seawater which leads to concretions with equivalent
concentrations of Fe and Mn and relatively high Ni, Cu,
and Co contents;
2. “Hydrothermal”, giving concretions which are generally
rich in iron and poor in Mn, Ni, Cu, and Co;
3. “Diagenetic,” known from the remobilization of manga-
nese in the sediments and its precipitation at the water-
sediment interface, giving nodules which are rich in Mn
and poor in Fe, Ni, Cu, and Co;
4. “Halmyrolitic,” where the source of metallic compounds
is the attack of basaltic debris by seawater
These theories, termed “mineral theories,” contrast with
the so-called “biologic theories” (Graham and Cooper 1959)
where detritus from organisms are responsible for the
enrichments in Cu and Ni.
14.5.3.2 Biological Functions
Manganese is an essential trace element in several biological
systems. It is essential in the diet of micro-organisms, plants,
and animals. It is necessary in the oxygenic photosynthesis
where it is involved in the functioning of photosystem II. It is
also a cofactor of various enzymes such as pyruvate kinase
which is involved in glycolysis. For some bacteria, the Mn
(II) can be used as an energy source and the forms Mn(III)
and Mn(IV) as terminal electron acceptors. The importance
of microorganisms that are capable to oxidize and reduce
the manganese is demonstrated by their ubiquity in terres-
trial, freshwater, and marine environments. After oxygen,
manganese oxides are among the most effective oxidizing
agents encountered in the environment.
14.5.3.3 Oxidation by Microorganisms
In the nature, Mn oxidation takes place in two ways: either
by spontaneous reaction which is enhanced in alkaline
conditions or by enzymatic reactions (Fig. 14.48). The
14 Biogeochemical Cycles
Fig. 14.48 Manganese O2
biological transformations H2O2
through reduction and oxidation
processes. Some implicated
microorganisms are listed
Oxidation
of Mn(II)
Leptothrix
Arthrobacter
oxidation of manganese involves the transfer of two
electrons (Mn(II) ! Mn(IV)), and comprises an intermedi-
ate step involving a single electron Mn(III). As in the case of
iron(II), Mn(II) is soluble but its oxidation product Mn(IV) is
very insoluble. The resulting oxides can sometimes form
concretions around sediment grains, pebbles, dead, or
biological structures (mollusc shell, fragment of coral, or
other debris) or dark layers in sedimentary rocks.
However, unlike iron(II), Mn(II) is stable in oxic
conditions at neutral pH. Chemical oxidation indeed becomes
significant only when pH is equal or higher than 8. Because
Mn is less prone to chemical oxidation, Mn(II) will be present
at a concentration greater than that of iron in aerobic zones
(marine and fresh waters) as well as in anoxic soils.
Microorganisms capable of oxidizing manganese have
been isolated in many biotopes (marine and fresh waters,
soils, sediments, manganese nodules, hydrothermal vents).
They are particularly prevalent in oxic–anoxic interface
areas and in hydrothermal systems which are a major source
of dissolved Mn(II) in the oceans. Mn(II) is reoxidized by
many bacteria, present in several phylogenetic lineages
(Firmicutes, Proteobacteria) (Tebo et al. 2005). Most stud-
ied species are:
Pseudomonas putida strain GB-1 and MnB1;
Leptothrix discophora strain SS-1 (characterized by a double
precipitation of iron and manganese oxides in the sheet
which surrounds the cells, yielding dark brown or black
colors);
Gallionella spp.;
Bacillus sp. strain SG-1; it is important to note that some
marine Bacillus produce spores that oxidize Mn(II) and
thereby are recovered with a precipitate of manganese
dioxide.
Some Fungi can also oxidize manganese (Thompson
et al. 2005). The main related enzymatic mechanisms
involve a copper oxidase. Its existence is demonstrated by
the inhibition of its oxidizing activity by azide (inhibitor of
copper-protein), and by a stimulation in the presence of
copper (Francis et al. 2001).
609
MnO2 Mn(IV)
Manganese dioxide Dissimilative reduction
of Mn(IV)
Shewanella
Geobacter
Mn(II)
Manganous ions
Based on physiological criteria, it is possible to classify
microorganisms that oxidize manganese into three major
groups (Ehrlich 2002).
Some (group I) oxidize soluble species of Mn(II) using
oxygen as terminal acceptor of electrons; this oxidation can be
coupled or not to the synthesis of ATP. The overall reaction is:
Mn2þ þ 0:5 O2 þ H2 O ! MnO2 þ 2Hþ
Organisms belonging to group II oxidize Mn(II) providing
that it is bound to a solid extracellular substrate Mn(IV)
oxide, ferromanganese, montmorillonite, kaolinite). These
organisms also use oxygen as terminal electrons acceptor.
For example, the reaction catalyzed by these bacteria when
manganese is bound to a hydrated oxidized form such as
MnO2.H2O (H2MnO3) can be summarized as follows:
Mn2þ þ H2 MnO3 ! MnMnO3 þ 2 Hþ
MnMnO3 þ 0:5 O2 þ 2 H2 O ! 2 H2 MnO3
Microorganisms of group III oxidize dissolved Mn(II)
with H2O2 using a catalase as enzyme. The reaction can be
summarized as follows:
Mn2þ þ H2 O2 ! MnO2 þ 2 Hþ
14.5.3.4 Reduction by Microorganisms
As in the case of oxidation, the reduction of manganese can
be performed enzymatically or not. The reduction of Mn(III)
and Mn(IV) forms, which is particularly important in anoxic
environments, generally leads to the solubilization of
manganese.
The most common biological pathway is the bacterial
reduction (Fig. 14.48) which corresponds to a respiration
where the oxidized manganese, which serves as a terminal
electron acceptor, is reduced to Mn(II). This is a dissimila-
tory reduction as well as that of iron, nitrate, or sulfur. Some
Fungi can also reduce manganese.
610
Oxidation
Reduction
2 Fe2+ 1 MnO2
Reduced
3 substrates
Iron-reductase Mn - reductase
Oxidized
substrates
2 Fe3+
Mn2++
Fig. 14.49 Manganese reduction through indirect (reactions 1 and 2)
or direct (reaction 3) biological pathways. Indirect reduction of manga-
nese oxide (MnO2) is due to Fe2+ originated from iron reduction
(reaction 1) or to sulfide (reaction 2). Sulfide may be produced through
Some bacteria can reduce manganese aerobically or
anaerobically. Others perform reduction only in anoxic
conditions where electron donors vary depending of species.
These species include Geobacter metallireducens which can
use butyrate, propionate, lactate, succinate, acetate, and
other compounds which are fully oxidized to CO2.
Shewanella putrefaciens uses pyruvate and lactate as elec-
tron donors but oxidizes them up to only acetate; formate
and H2 are also electron donors. During their development
on solid nutrient medium, colored in black by the addition of
manganese oxide (MnO2), bacteria that reduce manganese
can be identified by the formation of a clear halo around the
colonies, which is due to the dissolution of MnO2.
In the environment, after oxygen and nitrate depletion,
the oxidation of organic matter coupled to the reduction of
Mn(IV) oxides to return back to the reduced and soluble
form Mn(II) is carried out according to the following pri-
mary reaction:
246 MnO2 þ MO þ 364 CO2 þ 104 H2 O ! 470 HCO3 
þ 8 N2 þ 236 Mn2þ þHPO4 2
ðMO ¼ Organic Matter of theoretical composition
C106 H263 O110 N16 PÞ
Manganese oxides can also undergo spontaneously abi-
otic reduction in the presence of Fe(II) and sulfides
J.-C. Bertrand et al.
Reduced
SO42- substrates
Sulfate
reducer
Oxidized
H2S substrates
2 H2S H2S + SO32-
Thiosulfate
reductase
?
S0 S2O32-
thiosulfate reduction or dissimilative sulfate and sulfur reduction.
Direct manganese reduction is due to microorganisms harvesting
a manganese reductase (Redrawn from Nealson and Myers 1992)
(Drawing: M.-J. Bodiou)
(Fig. 14.49). This reduction is indirectly facilitated by the
activity of certain iron(II) and sulfide (S2) producing
microorganisms. For example, in Shewanella putrefaciens,
Fe(III) and thiosulfate are used as electron acceptors to
indirectly reduce Mn(III) from the action of a Fe-reductase
and a thiosulfate reductase which, respectively, transform Fe
(III) to Fe(II) and thiosulfate (S2O32) to hydrogen sulfide
(H2S) and sulfite (SO32) (Nealson and Myers 1992). By
producing sulfides, sulfate-reducing bacteria also contribute
to this indirect reduction (Fig. 14.49). Another example of
indirect chemical reduction is that achieved by organic acids
produced by fermentative bacteria or by certain
cyanobacteria. Escherichia coli produces formic acid from
glucose which reduces MnO2:
MnO2 þ HCOO þ 3Hþ ! Mn2þ þ CO2 þ 2 H2 O
14.6 Conclusion
Each element has a specific biogeochemical cycle, but
cycles of all elements are tightly coupled and interdepen-
dent. The growth of living beings is only possible when all
required biogenic elements are simultaneously available in
14 Biogeochemical Cycles
well-defined concentrations. The synthesis of cellular
materials associates carbon, as cell carbon and/or energy
source, to the incorporation of a wide variety of mineral
elements (oxygen, hydrogen, nitrogen, phosphorus, sulfur,
iron, etc.). Some of them also act as electron acceptors or
donors during redox reactions that are at the root of the
various biogeochemical cycles. Organic matter mineraliza-
tion returns mineral elements back to the natural environ-
ment under many chemical forms, enabling their recycling.
In this chapter, the cycles of iron, manganese, nitrogen,
and sulfur were described as if they operated independently.
But all these cycles are intimately linked by oxido-reduction
reactions, even if all the involved actors are not yet known.
For example, in some cases, there is an anaerobic oxidation
of sulfur or ammonium in the presence of manganese (IV) or
iron oxide as electrons acceptor. In some ecosystems, CH4
can be oxidized in the anoxic zone by one or several
syntrophic mechanisms that associate methanogenic archaea
with other bacterial functional groups such as sulfate-
reducing bacteria or denitrifying bacteria.
14.6.1 The Critical Role of Microorganisms
All living beings participate into the functioning of biogeo-
chemical cycles as known these days. However, higher
organisms are not essential to these cycle functioning. Pro-
karyotic microorganisms express all the functions that
are necessary to biogeochemical cycles, enabling them to
ensure all biotransformations of chemical elements. They
have acquired and achieve these functions over geological
times. For 3 billion years, life was strictly prokaryotic and the
functioning of biogeochemical cycles was totally ensured by
prokaryotic microorganisms (cf. Chap. 4). From their biogeo-
chemical functions, prokaryotes have created environmental
conditions in terrestrial habitats in which eukaryotic life forms
could appear, grow, and diversify.
14.6.2 Microorganism Plasticity
An important property of prokaryotes is their metabolic
plasticity that enables them to use different sources of car-
bon, energy, and electron acceptors, thereby contributing
directly to the functioning of several biogeochemical cycles.
For example:
1. autotrophic and chemolithotrophic Thiobacillus
denitrificans uses sulfide as electron donor and nitrate as
electron acceptor to produce its energy, and CO2 as
611
carbon source. These bacteria are thus directly involved
in the biogeochemical cycles of sulfur, nitrogen and
carbon;
2. several bacteria within the genus Shewanella can live
under chemolithotrophic conditions using hydrogen, or
under chemo-organotrophic conditions with simple
organic compounds. Under both conditions, they grow
either aerobically with oxygen as electron acceptor, or
anaerobically with various electron acceptors such as
iron, manganese, vanadium, arsenic, fumarate, the
TMAO (trimethylamine oxide) and DMSO (dimethyl-
sulfoxide). These very bacteria are also involved in the
biogeochemical cycles of many pollutants (aromatic
compounds, metals) and contribute to contaminated eco-
system bioremediation;
3. some photosynthetic bacteria are able to grow under
very different environmental conditions. For example,
the sulfur-oxidizing Thiocapsa roseopersicina uses
light as energy source under anaerobic conditions and
oxide sulfur compounds (sulfides, thiosulfate). In the
dark and in the presence of dioxygen, this bacterium
is able to achieve aerobic respiration using the same
sulfur compounds or simple organic compounds
(pyruvate, lactate, acetate, etc.) as energy sources. In
addition, this species can use CO2 (autotrophy) or the
same simple organic compounds (heterotrophy) as carbon
sources.
The prokaryote plasticity is confirmed by findings related
to the strain “Candidatus Desulforudis audaxviator.” This
bacterium alone makes 99.9 % of the microbial community
observed in a fault of the earth’crust located at 2.8 km depth
(Chivan et al. 2008). The metagenomic investigation
established that this organism has all the metabolic
capacities necessary for an autonomous life and was per-
fectly adapted to its environment. Thus, this anaerobic, ther-
mophilic, sporulated, and mobile bacterium uses sulfate as
the main electron acceptor, contains dehydrogenases, and
makes all its cell syntheses with organic or mineral carbon
as carbon source and ammoniacal nitrogen or dinitrogen as
nitrogen source. The absence of a complete protection sys-
tem with respect to dioxygen suggests an ancient isolation
from the Earth surface.
All functions performed by microorganisms (functional
diversity) are variously distributed among the different
known microorganisms (taxonomic diversity). Hence, if
some steps in biogeochemical cycles are carried out by
very diverse microorganisms present in almost all phyla
(denitrifying, organic carbon users), others are conducted
by more specialized groups (CO2 users, nitrogen fixers)
612
even limited to some phyla (nitrifiers, methanogens,
methanotrophs, sulfate-reducers, iron-, and manganese bac-
teria). It must be underlined that prokaryotes are the greatest
source of biodiversity still unknown on Earth. Regularly new
microorganisms are discovered. This knowledge leads to
complete the array of microbial actors involved in some
functions, for example, the 2005 discovery of archaea able
to oxidize ammonium.
The metabolic plasticity of prokaryotes is probably far
from being completely understood, since new functions and
physiological characteristics are part of the most recent
discoveries in the functioning of biogeochemical cycles
and, more generally, in microbial ecology. By the intrinsic
characteristics of microorganisms (metabolic plasticity,
short generation time, exchange of genetic materials), new
metabolic functions appear under the influence of human
activities on relatively short time scales (few decades),
such as the metabolism of xenobiotics. This metabolic plas-
ticity confers to prokaryotes this large ecological valence.
The discovery of new metabolic pathways broadens the
concepts related to biogeochemical cycle functioning, and
many microbial functions were recently discovered. For
example, the anaerobic methane or ammonium oxidation,
the thiosulfate disproportionation, the hydrocarbon anaero-
bic mineralization, or the iron oxidation by phototrophic
anoxygenic bacteria, are known prokaryotic activities that
remain to be explored. Similarly, some well-characterized
functional groups have shown new metabolic capabilities;
for example, some sulfate-reducing bacteria, identified as
anaerobic microorganisms, are able to process sulfate-
reduction and grow under oxic conditions. Similarly, some
nitrifying bacteria are able to achieve denitrification. These
findings tend to demonstrate that our knowledge of the role
and capabilities of microorganisms in biogeochemical
cycles, even if already large, is not exhaustive and new
discoveries are still expected in that domain.
14.6.3 Evolutive Cycles
For millions of years, the global cycles of elements were
stable and only environmental changes, often global
changes, affected them. In contrast, since two centuries and
especially during the past 50 years, demographic pressure
and human activity development have trigerred important
imbalances in biogeochemical cycles. Hence, disturbances
in carbon and nitrogen cycles led to the acceleration of
greenhouse effects from emissions of CO2, CH4, and nitro-
gen oxides resulting from excessive use of fossil fuels, waste
disposal, and intense fertilisation of agricultural soils. Simi-
larly, disturbances in the sulfur cycle appear in some
environments to be subject to anthropogenic sulfur-oxide
emissions that generate acid rains.
J.-C. Bertrand et al.
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