Calcium Cycle

Microbiology, Vol. 71, No. 1, 2002, pp. 1–17. Translated from Mikrobiologiya, Vol. 71, No. 1, 2002, pp.
5–22.
Original Russian Text Copyright © 2002 by Zavarzin.
REVIEW
PAPER
Microbial Geochemical Calcium Cycle

G. A. Zavarzin1
Institute of Microbiology, Russian Academy of Sciences, pr. 60-letiya Oktyabrya 7, k. 2, Moscow, 117312 Russia
Received September 13, 2000
Abstract—The participation of microorganisms in the geochemical calcium cycle is the most important factor
maintaining neutral conditions on the Earth. This cycle has profound influence on the fate of inorganic carbon,
and, thereby, on the removal of CO2 from the primitive atmosphere. Most calcium deposits were formed in the
Precambrian, when the prokaryotic biosphere predominated. After that, calcium recycling based on biogenic
deposition by skeletal organisms became the main process. Among prokaryotes, only a few representatives, e.g.
cyanobacteria, exhibit a special calcium function. The geochemical calcium cycle is made possible by the uni-
versal features of bacteria involved in biologically mediated reactions and is determined by the activities of
microbial communities. In the prokaryotic system, the calcium cycle begins with the leaching of igneous rocks,
predominantly through the action of the community of organotrophic organisms. The release of carbon dioxide
to the soil air by organotrophic aerobes leads to leaching with carbonic acid and soda salinization. Under anoxic
conditions, of major importance is the organic acid production by primary anaerobes (fermentative microorgan-
isms). Calcium carbonate is precipitated by secondary anaerobes (sulfate reducers) and to a smaller degree by meth-
anogens. The role of the cyanobacterial community in carbonate deposition is recorded by stromatolites, which are
the most common organo–sedimentary Precambrian structures. Deposition of carbonates in cyanobacterial mats as
a consequence of photoassimilation of CO2 does not appear to be a significant process. It is argued that carbonates
were deposited at the boundary between the “soda continent”, which emerged as a result of subaerial leaching with
carbonic acid, and the ocean containing Ca2+. Such ecotones provided favorable conditions for the development of
the benthic cyanobacterial communities, which were the precursors of stromatolites.
Key words: calcium, carbonate, inorganic carbon cycle, cyanobacterial mats, Precambrian, stromatolites,
microbial communities.
FORMULATING THE PROBLEM found influence on the Earth’s climate through the
The role of prokaryotes in the calcium cycle is not greenhouse effect. The major part of lithospheric Ca is
considered in most microbiology textbooks. Although accumulated in oceanic carbonate sediments, which
no bacteria with a special calcium function are known, gave rise to calcareous rock (Fig. 1).
this function is quite prominent in various eukaryotes A close connection between the cycle of Ca and
ranging from protists (coccolithophorides and foramin- cycles of other biogenic elements makes possible the
ifers) to metazoans (e.g., molluscs forming their skele- formation of gypsum and phosphorite deposits. Sul-
tons from calcium minerals). Coral communities are an fates of the ocean and gypsum deposits in evaporates
example of contemporary reef-builders. In the Precam- owe their origin to the oxidative activities of microor-
brian time, however, there were no eukaryotic organ- ganisms of the sulfur cycle. The formation of phospho-
isms, and yet vast deposits of calcium carbonate were rites and the conversion of calcium phosphate to a uti-
formed in the Late Archean to Proterozoic. Therefore, lizable form were the most likely factors limiting the
either chemical precipitation under physical and chem- development of biota in the Proterozoic, given that the
ical conditions differing from present or the involve- limitation by bound nitrogen, characteristic of algae
ment of prokaryotes is to be admitted. The latter is well and plant cover, was not critical because of nitrogen-
illustrated by the massive development of stromatolites fixing activities of bacterial communities.
as major Proterozoic reef-builders, the emergence of
which was conditioned by the activities of cyanobacte- Calcium and its carbonates preserve the bicarbonate
rial communities similar to contemporary benthic mats. equilibrium by restraining the decrease of pH by car-
Another reason for paying particular attention to the bonate dissolution and the increase by CaCO3 precipi-
calcium cycle is its intrinsic coupling with the inorganic tation. As a consequence, neutral conditions with pH
carbon cycle (Cinorg). Dissolved oceanic Cinorg and varying from 5.5 to 8.5 are produced in the presence of
atmospheric CO2, which are in equilibrium, represent Ca, under which most organisms thrive. The rest that
small-scale dynamic pools that, nevertheless, have pro- occur beyond these normal conditions are known as aci-
dophiles and alkaliphiles. These organisms can also be
1E-mail: [email protected] designated as “calciophobs”, in contrast to neutrophilic
0026-2617/02/7101-0001$27.00 © 2002 åÄIä “Nauka /Interperiodica”

2 ZAVARZIN
Ca pool
of igneous rock
~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~ Mobilization of Ca
by leaching and its
run-off by rivers
Carbonate to the ocean
Calcareous platforms
Lysocline silts
Ca pool Carbonate exportation in geological

of the ocean recycling brought about by subduction
and other tectonic processes
Fig. 1. Calcium pathway in the lithosphere.
ones, which are “calciophilic” with regard to the typomor- logical formations (tens of kilometers), one needs to
phic element of landscapes of their environment. examine how this alkaline barrier is formed and main-
Cycles of Ca and Cinorg can be viewed as two sides tained.
of one process. At the same time, the cycle of Cinorg, In this regard, the capacities of prokaryotes and
through its labile forms CO2 and
–
HC O 3 ,
is linked with eukaryotes are different. Eukaryotes and, in particular,
tissue-forming multicellular organisms are able to cre-
the biotic Corg cycle. The latter involves autotrophic ate locally in cell compartments or in the intercellular
assimilation of CO2 in the course of primary production space the conditions needed for depositing Ca-contain-
and CO2 release in the course of decomposition. This ing skeleton components. With the singular exception
proceeds concurrently with the accumulation of stable of Achromatium oxaliferum, prokaryotes lack this
Corg in geopolymers, mainly as dispersed kerogen, capability and, therefore, act upon Ca compounds in the
accompanied by the release of equivalent amounts of extracellular space via the so-called biologically medi-
O2 in the atmosphere. Therefore, the biota indirectly ated reactions. This differs them from protists and
determines the acid-base conditions on the Earth’s sur- metazoans, which can accomplish direct biomineral-
face via the Ca cycle and the redox conditions via the ization reactions. There are, therefore, three channels
O2 cycle. The biogeochemical succession through the of calcium circulation to be considered: (1) chemical
Earth’s history altered the thermodynamic conditions precipitation of calcium carbonate caused by distortion
and caused the transformation of originally unoxidized of chemical and physical equilibrium, as in CO2 degas-
igneous rock minerals into minerals of the sedimentary sing of groundwater emerging onto the surface, or
cover. when CO2 solubility falls down as the temperature
The outlined arguments warrant a close examination increases, or in the course of evaporation; (2) biologi-
of the scale and forms of participation of prokaryotes in cally mediated precipitation caused by the alkaline bar-
the biogeochemical Ca cycle. The immense literature rier formed as a result of activities of microorganisms;
devoted to calcium carbonates can hardly be reviewed and (3) direct precipitation in skeleton construction
in this paper, and so references are given only to general involving mechanisms of intracellular mineralization.
works dealing with the issues in hand. A vast list of ref- The dissolution of carbonates is caused by the reverse
erences can be found in [1]. (The physiological signifi- processes: the increase of the CO2 concentration due to
cance of calcium as a trace element [2] is not consid- respiration in the oxygenated zone or anaerobic gener-
ered in this review.) ation of organic acids.
Calcium is an element with a constant valence and The necessary condition for a mineral to precipitate
its chemical reactions cannot serve as an energy source is that the source solution becomes supersaturated with
for lithotrophic microorganisms. The dissolution and respect to the insoluble compound. This state can be
precipitation of Ca compounds are governed by the pH calculated from thermodynamic considerations, also
of the medium, rather than by Eh, despite the fact that for multicomponent systems, as a function of such
carbonates are deposited in the oxygenated zone. The affecting factors as temperature, pressure, and the pres-
major mechanism of microorganisms’ action on Ca ence of competing ions [4]. Most geochemical studies
compounds is, admittedly, the alteration of the pH of stick to such estimates, rightfully assuming that, in
the medium and the formation of the acid-base doing so, they get the likely final state of the system. In
geochemical barrier (the D-barrier, according to the practice, however, gross supersaturation is not at all
classification by Perel’man and Kasimov [3]). To infrequent even in homogeneous systems, for example,
understand the precipitation of calcium at any particu- in solutions in soil due to the formation of colloids and
lar scale, ranging from cells (tens of microns) to geo- complex compounds, not to mention heterogeneous
MICROBIOLOGY Vol. 71 No. 1 2002

MICROBIAL GEOCHEMICAL CALCIUM CYCLE 3
conditions. Under such circumstances, it is often hard

to tell what the actual local conditions are. 12.4dissolved + 2solid runoff Surface waters
production 85
The dissolving of a mineral involves a surface
exchange reaction, e.g., with the H+ ion. The solution
near the surface needs to be replenished. In the case of 71 85
molecular diffusion in the interstitial space, it is a slow
process limiting the rate of dissolution. Therefore,
groundwaters are most often undersaturated with Deep waters
2.6 influx dissolution 66
respect to the host rock [5]. The transition into a stable
crystalline state from a supersaturated solution requires
the participation of seed particles or nuclei. Nonequi- 17
librium conditions arise from kinetic factors.
Sediments
BIOGEOCHEMISTRY accumulation 17
AND THE BIOLOGICAL CALCIUM CYCLE
The geochemical cycle of calcium consists of the Fig. 2. Biogeochemical calcium cycle (in 1012 g-atoms/year)
primary cycle, which refers to the extraction of calcium [9].
from igneous rock followed by carbonate deposition,
and the recycle, consisting of carbonate rock dissolu-
tion and subsequent precipitation. The Phanerozoic Carbonate silts form from precipitating plankton during
period was dominated by the recycle, which, in addi- diagenesis of bottom sediments. The age of silts does
tion, proceeded under an oxygenated atmosphere. not exceed that of the seafloor bed. Carbonate platforms
The primary cycle is represented primarily by cal- and reef structures in offshore areas form with the
cium leaching with carbonic acid from igneous rock via involvement of benthic organisms. In the Precambrian,
the atmospheric hydrological cycle. On the one hand, stromatolitic reefs were formed by cyanobacterial com-
this cycle produces carbonates and, on the other, forms munities. Under subaerial continental conditions,
residual aluminosilicates or clay. The reaction can be leaching with carbonic acid eventually results in the
conventionally represented as silicate hydrolysis with formation of calcified weathering crust and pedogenic
carbonic acid, formed by dissolution of carbon dioxide, carbonates.
and the production of carbonate alkalinity The general model of the geological cycle of cal-
2+ –
cium must take into consideration the regions of cal-
CaSiO 3 + 2CO 2 + H 2 O = SiO 2 + Ca + 2HCO 3 . cium mobilization on the mainland and its deposition in
the ocean (Fig. 2) [9].
The igneous rock is exposed to physical weathering,
yielding disintegrated material—marl, gravel, and Contemporary biogenic leaching of calcium can be
sand—characterized by a large surface/volume ratio estimated from the calcium content of the river runoff
and high permeability. Leaching is active in groundwa- to the ocean, serving as a terminal sink for Ca. To a very
ters in the oxygenated zone unaffected by evaporation gross approximation, the calcium cycle is determined
and gives rise to alkaline waters and calcified weather- by the atmospheric hydrological cycle. The oceanic
ing crust. The seafloor region (subaquatic conditions) water evaporates and the dissolved CO2 comes in equi-
and continental plains (subaerial conditions) covered librium with the atmospheric CO2. Part of the water
with clay, the terminal weathering product, are pro- precipitates over the mainland as rainfall and becomes
tected against the loss of calcium. enriched with CO2 produced by the respiration of orga-
In the Corg cycle, the CO2 carbon is concentrated by notrophs. As the last step the precipitated water leaches
autotrophic assimilation and then released in the course calcium and reenters the ocean, which serves as an
of mortbiomass decomposition by microorganisms. As accumulator for salts delivered by runoff. The balance
a result, the mobilization of calcium is accelerated by of calcium in the ocean is determined by its inflow from
the action of decomposers. the mainland and by deposition. Less significant
sources of calcium are hydrothermal changes of
On the geological time-scale, the subaerial leaching
of silicate and carbonate deposits is the most important basalts, porous water, and Ca2+ desorption from clay.
mechanism determining the concentration of CO2 in The average calcium concentration of river water is
–
the atmosphere, and, therefore, the greenhouse effect. 0.34 mM, the concentration of HC O 3 is 0.85 mM; and,
The accumulation of calcareous sedimentary rock in the ocean, the calcium content is 8.98–10 mM [6].
through the Earth’s history points to the trapping of car- The arid climate, resulting in soda mineralization, lim-
bon dioxide and the openness of its cycle. On the geo- its the mobilization of calcium, and its content in soda
logical scale, the CO2 cycle depends primarily on the lakes at pH > 9 is as low as 0.015–0.07 mM [7]. Loca-
shallow ocean areas, where carbonates form, and their tions of Ca accumulation were studied by Ronov and
exchange both with the deeper ocean and the mainland. Yaroshevskii and are clearly revealed by clarke concen-

4 ZAVARZIN
trations of this element (CaO, %): the overall crust, exchange fluxes in the modern ocean are diagrammed
8.12; continental crust, 6.98; and subcontinental crust, in Fig. 2 (in 1012 moles/year) [9].
7.14. The oceanic crust shell: sedimentary, 22.50; and Berner [10] estimated the continental weathering of
basaltic, 11.69; the continental shell: sedimentary, 9.94; silicates in the Phanerozoic from their concentration in
and granitic, 3.79. Terrigenous rocks typically have low river runoff, determined by paleoclimatic conditions.
concentrations of calcium; thus pelagic clays contain As indicated by experimental data for the Alps, silicate
around 0.93%; meanwhile, the Ca content of calcare- weathering increases sevenfold in the presence of plant
ous abyssal sediments is 25.5% [8]. Under terrigenous cover. As a result, in Berner’s 3Geocarb II model, the
conditions, calcite accumulates in the weathering crust concentration of CO2 in the atmosphere as a function of
and, in the arid zone, regions of calcite formation are different factors showed an abrupt break and decline
readily identifiable. With a total runoff of 37400 km3/year, some 300 million years ago in the Devonian, with the
the annual influx to the ocean includes 32.4 × 1012 mol introduction of plant cover formation into the model.
However, there is no geological evidence of such a
of HC O 3 as well as 12.4 × 1012 g-atom of dissolved and
–
break. Therefore, it is reasonable to hypothesize the
2 × 1012 g-atom of suspended calcium. Under modern presence, in the Proterozoic time, of a land cover formed
conditions, assuming that the calcium content of river by nonvascular plants and algae, which, together with the
water is 0.34 mM, it would take merely 1 million years for accompanying organotrophic decomposers, drived the
the concentration of calcium in the ocean to reach 10 mM. process of igneous rock leaching, playing a role similar to
The ocean serves as an accumulator for calcium, which is that of modern plants and fungi.
buried in carbonate sediments. The removal of Ca2+ from
the modern ocean occurs predominantly through the bio- NONBIOLOGICAL REACTIONS
logical formation of calcite on the continental shelf. The OF CARBONATE EQUILIBRIUM
net yield of this process is estimated at 17 × 1012 g-atom From the geochemical standpoint, the key part in the
Ca. The exchange with ocean bottom sediments amounts circulation of calcium and Cinorg, is played by the car-
to 19–24 × 1012 g-atom Ca. The resulting carbonate bonate–bicarbonate equilibrium:
CO2(gas)
+ – 2– 2+
CO 2 ( dissolved ) H 2 CO 3 H + HCO 3 CO 3 + Ca CaCO 3
ëorg
The actual state of the system depends on which of pCO2 is constant and maintained, for example, by res-
its constituent compounds is removed; and, in the piration, the process of calcite dissolution never stops.
above scheme, it is Corg. A distinction should be drawn Given that the term entering the equation is the partial
here between the pH, depending on the concentration pressure of CO2 assimilated in photosynthesis and
of the H+-ion, and the alkalinity A, determined, mainly, released in respiration, the dissolution of calcium car-
by the total of dissolved labile forms of Cinorg. The inor- bonates turns out to depend upon aerobic biological
ganic carbon is determined by the total moles of CO2 + processes. The release of carbon dioxide in respiration
– 2– increases the dissolution of calcite and this explains
H2CO3 + HC O 3 + C O 3 ; while the alkalinity A is equal why sites of carbonate redeposition are confined to the
– 2–
to HC O 3 + 2C O 3 in mg-equiv. The physicochemical oxygenated zone, where the exchange with the atmo-
sphere is possible. The leaching of calcium is markedly
conditions for carbonate equilibrium in aquatic media stepped in the presence of mineral acids: nitric acid
are determined by the equilibrium constants. The car- formed by nitrifiers and sulfuric acid formed by thionic
bonate system determines the pH and, thus, the chemi- bacteria. In the latter case, the calcium concentration of
cal behavior of minerals, and above all that of carbon- the solution is determined by the solubility of gypsum.
ates, in most natural waters. The highest buffering
capacity is shown at pH 6.4. In soda lakes, the carbon- In anaerobic processes, such as sulfate reduction,
– 2–
the reaction is
ate system is buffered with the HC O 3 /C O 3 system at 2– –
pH near 10.3. Waters in equilibrium with calcite have SO 4 + 2Corg + H2O = H2S + + 2HC O 3
their pH values in the range 7.3 to 8.4. and gives rise to increased alkalinity. In the presence of
In closed systems, like soil and silts, the dissolving organic acids, the carbonate equilibrium is determined
of calcite is directly related to the concentration of car- by the stronger acids. In groundwater, pCO2 is main-
bon dioxide in the gas phase. In open systems, where tained primarily by respiration in the feeding zone. For

water percolating through dolomite, the ratio +10‰ at 25°ë. The concentration of carbon by plants
Mg2+/Ca2+ = 0.6 but the equilibrium takes a long time gives rise to increased abundance of the lighter isotope:
to reach. in C-3 plants, it averages –27‰ and in C-4 plants,
With the partial pressure of carbon dioxide in the −13‰ [17]. Therefore, the origin of carbonates can be
ocean water column increasing with pressure and inferred from their isotopic composition. Ryskov et al.
decreasing temperature, the dissolution of carbonates [16] concluded that pedogenic carbonates of Russian
occurs at a depth of 3.5 km in the Pacific and 5 km in soils do not preserve the isotopic composition of the
the Atlantic Ocean. This zone is called lysocline, and dissolved lithogenic material and originated from
here the dissolution is faster than burial in bottom sed- organic matter of plants. It follows that the prevailing
iments. The undersaturation with respect to calcium process of carbonate generation in the pedosphere is
carbonate begins from a 0.5-km depth. Magnesia cal- microbial decomposition of the dead biomass of pri-
cite penetrates to greater depths. mary producers, resulting in the enrichment of soil
solution with light CO2 and in Ca leaching. Regarding
The carbonate–calcium equilibrium in soils is deter- the carbon isotopy of carbonates, it should be noted that
mined by the state of the soil solution, which, in con- the isotopic composition of some of the most ancient
trast to water systems, is liable to rapid change with carbonates from Isua, aged 3.4 billion years, is enriched
weather conditions. Carbonate systems in soil consist in 12C and corresponds to that of Corg of photoautotro-
of calcite, Ca2+ ions of the exchange complex, Ca2+, phs [18]. A markedly lighter isotopic composition was
+ 0 – 2+
CaHC O 3 , CaC O 3 , HC O 3 , C O 3 , H+, OH–, H2CO3, found in marine carbonates formed in methane oxida-
tion [19−21]. By contrast, a global increase in 13C/12C
CO2(dissolved), and CO2 (gas). A thermodynamic calcula- of carbonates up to +9‰ about 2 billion years ago in the
tion of calcite solubility for multicomponent soil solu- Jatulian is interpreted as a change of the isotopic com-
tion systems is fairly complicated, but for a long time position caused by the assimilating activities of cyano-
there were computer programs to do that [11]. Experi- bacteria, which became widespread at that time [22].
mental data show significant variation because of so
many factors contributing to the equilibrium. The sedi-
mentation of carbonates in soil is to a large degree deter- BIOLOGICAL MECHANISMS
mined by the three physical processes that increase the OF CARBONATE EQUILIBRIUM
concentration of the soil solution: (1) evaporation from The reactions of reversible carbonate equilibrium in
the soil surface; (2) transpiration of plants and withering; living organisms are catalyzed by carbonic anhydrase,
and (3) seasonal freezing. Each of these processes affects an enzyme of key importance for the problem in hand.
the carbon isotopic ratio of carbonates. Carbonic anhydrase is a Zn-containing enzyme wide-
The chemical reactions of the calcium cycle are spread both in organotrophs and in autotrophs. In the
accelerated manifold by the biota. The most common former organisms, it is responsible for removing CO2
communities causing primary subaerial leaching are from the cell; and, in the latter, for its supply to the cell.
lithophilic lichens and fungi. The rock surface moist- In autotrophs, carbonic anhydrase is coupled with the
ened by dew condensation is coated by a thin film of mechanism concentrating the utilizable form of inor-
different organisms starting a characteristic rock colo- ganic carbon, which is the CO2 that reacts with ribulose
nization succession, readily recognized on intrusive bisphosphate carboxylase (Rubisco) in the pentose
rock in the arid areas of Tuva [12] and on granite in phosphate cycle.
Fennoscandia. Tombstones are a suitable model to The general reaction of carbonic anhydrase can be
study leaching because they had a smooth surface when expressed as
erected, can be readily dated, and are relatively free
+ –
from excessive man-made pollution. According to dif- H 2 O + CO 2 + E = E – CO 2 = E + H + HCO 3 .
ferent estimates and under various conditions, the bio-
–
genic acceleration of limestone leaching can be as high H2O

as 10 to 10000 times [13, 14]. The activity of carbonic anhydrase can be determined
The role of the biogenic component of the calcium from the rate of pH increases in the presence of dis-
cycle can be estimated from the isotopic composition of solved CO2. Similarly to Rubisco, which is the key
soil carbonates, which was recently analyzed in a study enzyme operating at the entry point of the organic car-
of the CO2 dynamics for Russia [15, 16]. Soil carbon- bon cycle, carbonic anhydrase accomplishes the same
ates are represented by : (1) the lithogenic constituent key function for the Cinorg cycle.
derived from soil-forming rock; and (2) pedogenic car- Acting in conjunction with Rubisco, carbonic anhy-
bonates formed as a result of CaCO3 sedimentation drase concentrates CO2. The role of Rubisco in plants is
from soil solution. The isotopic ratio 13C/12C for marine well known [23]. A high activity of carbonic anhydrase
lithogenic carbonates, e.g., ancient shell rock, varies was shown in calcareous algae Halimeda inhabiting
between +2 and –2‰. Owing to CO2 diffusion, coral reefs. Carbonic anhydrase in unicellular algae
pedogenic carbonates become enriched with the 13C Chlorella and Scenedesmus was studied in detail [24].
isotope by +14.4‰ at 0°ë; +11.8‰ at 15°ë; and In eukaryotic algae, various forms of inorganic carbon

6 ZAVARZIN
cell
Ca2+ [Ca2+]
–
2HCO– carbonic [HCO3 ]
OH– anhydrase [CO 2– ]

3
+ +
CO2 CO2 CO32– Ca2+
photoautotrophic
assimilation sulfated
[galactose] polysaccharide
Golgi
apparatus
SO42– [SO42– ]
CaCO3 of the coccolith
Fig. 3. Deposition of calcium carbonate in cells of coccolithophorides.
are transferred through numerous membrane barriers of in prokaryotic organisms and pyrenoids in eukaryotes
the cell by means of their conversion to carbon dioxide, and the existence of membrane mechanisms of Cinorg
able to diffuse through membranes. By causing rapid transport, which are believed to be of key importance for
attainment of equilibrium between the two forms of the CO2-concentrating mechanism in autotrophs [25].
carbon dioxide, carbonic anhydrase enables gas to pass –
through the membrane to sites of its assimilation in Three possible membrane mechanisms of HC O 3
autotrophic organisms where CO2 reacts with Rubisco. transport into the cell are hypothesized: (1) symport
The reverse process of carbon dioxide removal occurs with Na+ followed by antiport with Na+/H+; (2) ATP-
in respiration. Therefore, this enzyme is needed by both dependent direct transport; and (3) transport by means
autotrophs and organotrophs. In cyanobacteria, the of an unknown transporter operating at high concentra-
coupling of carbonic anhydrase with Rubisco is made –
tions of HC O 3 . The latter mechanism might occur in
possible by their occurrence within a common struc-
ture—the carboxysome. In eukaryotic microalgae, a species inhabiting soda lakes. The interconversion of
–
similar conjunction occurs in the pyrenoid. CO2 and HC O 3 inside the cell is sustained by a car-
–
It is believed that autotrophic assimilation in some bonic anhydrase-like enzyme, but it is HC O 3 that gets
cyanobacteria might incorporate the active transport of into the carboxysome and, under the action of carbonic-
–
the HC O 3 ion, and this, presumably, enhances their anhydrase, is converted into CO2 that combines with
calcite precipitation capacity. The supporting evidence ribulose bisphosphate and produces phosphoglycerate.
comes from the assimilation of Cinorg in alkaline media. All further reactions of the Calvin cycle proceed out-
Of special interest is the organization of carboxysomes side the carboxysome.
The mechanism discussed above does not tell much
about the balance in the outer layer surrounding the cell
SO42– CO32– and in the glycocalyx layer. The interaction of such
mechanisms with the Ca2+ transport specific to cyano-
Ca2+ Ca2+ bacteria remains unclear. The role of carbonic anhy-
drase in chemotrophic prokaryotes, and especially in
cell of Synechococcus connection with the reactions of calcium compounds,
HCO3– + H2O = CH2O + O2 + OH–
has not been studied in detail. Therefore, the problem of
HCO3–
how bacteria catalyze the attainment of carbonate equi-
librium in the space close to the cell cannot be regarded
Ca2+ as resolved or reduced to the attainment of the physical
and chemical equilibrium.
H2O + CO32– = HCO3– + OH– Carbonic anhydrase plays a key part in the forma-
tion of skeletal structures in protists. Among contempo-
Fig. 4. Participation of cyanobacteria in precipitation of cal- rary protists, the most important calcification agent is
cium minerals. believed to be coccolithophorides, which are unicellu-

lar marine plankton algae. Carbonates are deposited in and acids; (2) crystal development and its suppression
this organism as coccoliths, being structural elements by inhibitors depositing on the crystal surface, e.g.,
of the skeleton formed within the Golgi apparatus on anticalcifying proteins; and (3) epytaxy, i.e., matrix
the organic basal elliptic plate consisting of sulfated growth of the crystal upon a structured surface. The
polysaccharide. Upon formation, coccoliths migrate onset of mineralization, therefore, hinges on the presence
out of their cisterns and settle as part of protist’s outer of nucleation centers on extracellular heteropolysaccha-
carbonate skeleton. The process of calcification is fully rides—capsules, slime, and sheaths of trichomes. Their
controlled by the cell. Calcification and photosynthesis emergence depends on the medium conditions and con-
proceed in a one-to-one ratio. A necessary condition for stitutes an adaptive response of the organism quite
the calcification to proceed is that CO2 be eliminated often observed in the environment and community but
from the reaction space. The general course of the pro- rarely found in laboratory cultures. This fact is a source
cess in Emiliana huxlei is sketched in Fig. 3. of considerable ambiguity in the interpretation and
This diagram reveals the key role of carbonic anhy- reproduction of the results.
drase in carbonate transport. The transfer across mem- Calcification in the intercellular space is determined
branes occurs supposedly in the form of nondissociated by the rate of diffusion, which, at 20°ë, for CO2 is
carbon dioxide. The crystal develops in the open part of equal to (in cm–2s–1) 1.5 × 10–5; for HC O 3 10.2 × 10–6;
–
the cell separated by a membrane from the cytoplasm.
This calcification mechanism is, obviously, impossible and for Ca2+ 8.3 × 10–6. As a result, the calcification
for noncompartmentalized cells of prokaryotes. In coc- threshold is determined by the rate of Corg production
colithophorides, coccoliths form on elliptical plates and estimated to be 100–200 nmol/(g min). This mech-
consisting of sulfated polysaccharides and made visible anism was proposed for a calcareous alga Halimedia
by treatment with hypocloride. Similar plates were inhabiting coral reefs. A calcification mechanism
found in cyanobacteria [26]. Sulfogroups are believed involving ejection of the OH– ion by a cell upon utiliz-
to serve as binding centers for calcium. –
ing HC O 3 was put forward for Charales [30]. Similar
The involvement of cyanobacteria in precipitating processes are possible in dense cyanobacterial commu-
calcium minerals from lake water with pH 7.9 and Ca2+ nities, especially benthic ones, forming pseudotissue.
concentration of 11 mM in the course of photosynthesis Photosynthesis is unable to significantly shift equilib-
was demonstrated in model experiments with Synecho- rium from that observed in seawater with 10 mM Ca2+,
coccus [27]. Calcite, gypsum, and magnesite were and the effect of calcification on alkalinity is weak.
observed to deposit on the cell surface serving as the
nucleation center. The sedimentation was caused by a In contrast to skeleton-forming eukaryotes, with
small shift in the pH value induced by photosynthesis. prokaryotes, the supply of calcium to their cells is not
The early stage of gypsum crystal deposition onto the very important, except when it is required as a trace ele-
cell surface can be readily seen in electron micro- ment in several significant physiological processes,
graphs. The diagram of the process proposed by the such as nitrogen fixation, photosynthesis, sporogenesis,
authors of [27] is based on the idea of active transport and other functions that are not considered here and for
of bicarbonate during photoassimilation by way of anti- which special transport mechanisms were evolved by
–
organisms [2].
port of HC O 3 /OH– (Fig. 4).
A presumably chemical sedimentation of calcite CALCIUM CARBONATE FORMATION
was studied using, as an example, calcareous sediments
within the water column, the so-called “whitings”, IN CYANOBACTERIAL MATS
which are calcareous cloudings above carbonate shoals The production of calcium minerals by contempo-
in warm climate regions, occurring, for example, within rary cyanobacterial communities in both natural sam-
the Bahama carbonate platform and in the Persian Gulf. ples and laboratory cultures is well documented. In
It was found that 25% of carbonate suspension was detail, this process was studied for calcium phosphate,
constituted by organic matter, with the solid phase which is an important constituent of the biogenic for-
attached to picoplankton or decomposed remnants of mation of phosphorite deposits [31]. The major issue
planktonic algae. The supposed mechanism includes here is the natural mechanism of phosphate concentra-
the removal of CO2 during photosynthesis. Upon dying, tion, based on phosphorus accumulation by cyanobac-
the organisms turn into negatively charged surfaces teria. Calcium can be derived from seawater, in which
binding cations. The ammonifiers can play a certain the concentration of Ca2+ is close to 10 mM.
part in this process by creating local conditions for pre- The calcification by cyanobacterial communities is
cipitation [28]. of particular interest because of the scale of the process
The kinetics of biological mineralization is regu- they carry out and its primary role in the history of the
lated not only by attaining the mineral’s solubility prod- Earth. Contemporary lagoons with the salinity suffi-
uct but also by crystallization processes with the corre- ciently high to cause the precipitation of CaCO3 pro-
sponding biological mechanisms of their initiation and vide habitat to cyanobacterial mats with a characteristic
inhibition. These mechanisms include [29]: (1) nucle- community structure. In such mats, however, as we
ation and nucleation suppression by organic polyanions showed by the example of Sivash mats, gypsum and

8 ZAVARZIN
calcite undergo sedimentation at a depth of 1–2 mm ical processes so far failed. An interesting example of
under the layer of oxygenic photosynthesis in the devel- such a lamellar organo-sedimentary structure was
opment zone of purple bacteria [32]. The course of cal- found in the Zavarzin Pond in the Uzon caldera [35].
cification in a cyanobacterial culture of Microcoleus Fine suspension of sulfur washed out by hot spring
was followed in a scanning electron microscope. First, water was carried into the pond, where thermophilic
small lumps of calcite appear on sheaths of some Phormidium laminosum developed. Under daily
cyanobacteria, characterized, apparently, by decreased growth dynamics, a sandwich column was formed in
physiological activity. Then, these lumps start to grow which layers of fine-grade sulfur were interlaced with
in number and they cover the sheaths by an uneven min- layers of phormidium.
eral cover. Quite often, live trichomes creep out of the As indicated by laboratory experiments, the condi-
sheaths, leaving behind empty tubes. Next, the intercel- tions for stromatolite formation and lithification of the
lular space starts to be filled with calcite lumps that, cyanobacterial mat are likely to be related with the
eventually, come to form continuous sediment mass. buoyancy given to the mat by O2 bubbles, produced in
We see, therefore, that sheaths of cyanobacteria and photosynthesis, which tear up and float the mat to the
dead cells act as centers of postmortem nucleation. It is liquid phase. Torn mat pieces are carried away. If the
worth noting that carbonaceous stromatolites are con- medium is still, the mat can be loose. Formation of cal-
stituted by grainy carbonate sediment and contain no careous sediments in mats decreases their buoyancy.
lithified bacteria. Microfossils occur in stromatolites in For this reason, it is only portions of mat made heavy
dark silicious inclusions. A notable feature of modern by calcification that rest in places of stromatolite for-
cyanobacterial mats with carbonate deposits is that mation and accrete into solid crusts. The mobility of the
cyanobacteria reside outside the layer of carbonaceous medium turns out to have several important implica-
globules. One inconsistency in such a portrayal of this tions: (1) gas is removed as the liquid flows over the
process is that minerals settle predominantly on dead surface and this prevents bubble formation; (2) light-
cells, which, naturally, lack any photosynthetic activity, weight pieces of mat are carried away; and (3) the
whereas the sedimentation of CaCO3 might be expected heavy fraction is selected as a result of sedimentation of
to correlate with such an activity. Therefore, it should mineral matter and its cementation.
be concluded that live cells must possess some mecha- It follows that facies analysis is needed when con-
nism that prevents the deposition of calcite. A likely sidering stromatolite formation. A detailed analysis not
mechanism would be a positive surface charge of a only of sections of the stromatolite mass but also and in
metabolizing cell, e.g. due to H+, preventing the sorp- the first place of the paleosurface can yield additional
tion of Ca2+ on the membrane but not on sulfur groups information on the physical conditions of the sedimen-
of polysaccharides in sheaths or glycocalix. tation environment.
The idea that photosynthesis plays a major part in
carbonate depositing by markedly increasing the pH in PRECIPITATION OF CALCITE BY
the intercellular space has an inconsistency related to ORGANOTROPHIC BACTERIA
diffusion: for the pH to increase, the exchange with the
outer space must be hindered and, at the same time the As previously mentioned, no chemotrophic organ-
deposition of calcium requires its inflow from the out- ism with a definite calcite-producing function was dis-
side. Therefore, sedimentation may be confined to the covered, although characteristic species of cyanobacte-
pseudotissue of the cyanobacterial community. In spite ria and other bacteria are often found in travertines. A
of the advantages of coupling calcification with photo- general description of calcite formation based on a
synthesis, there are few species among cyanobacteria model experiment and outlining the key stages of the
inclined to calcification. Under contemporary condi- process was given in 1948 by Issatchenko [36]. In his
tions, liming proceeds in Scytonema, Calothrix, Rivu- study he used ammonifiers on a solid peptone-rich
laria, Phormidium, Lyngbya, and Plectonema at sites medium containing water from sources depositing trav-
of travertine deposition. Such habitats are incommen- ertines. Among the emerged colonies, only those of cer-
surable with a wide spatial distribution of stromatolites tain species showed calcite sedimentation. Issatchenko
and calcareous algae in the past. concluded that “the carbonate sedimentation, appar-
ently, follows the same pathway in every live species: first,
The next stage consists in formation by cyanobacte- amorphous carbonate is formed, colloid calcite appears
rial communities of mineral macrostructures similar to next, and then it undergoes crystallization.” Issatchenko
stromatolites. As suggested by Krylov, this process was
simulated in our laboratory by Orleanskii [33, 34]. The concludes with a thesis: omne calx e vivo [36].
idea consists in depositing on the surface of a cyano- Hence, the following steps of bacteriogenic precipi-
bacterial film of CaCO3 either chemically precipitated tation of calcite could be identified: (1) formation of an
from the solution covering the film or simply as pow- alkaline geochemical barrier; (2) formation of a solu-
der. Some part of mobile cyanobacteria creep out to the tion supersaturated with respect to CaCO3; (3) forma-
light on top of the sediment, while the rest remain in tion of calcite colloids; (4) nucleation of CaCO3 on bac-
place as a dark layer. Repetition of this process pro- terial slime hosting immobilized Ca2+; (5) diagenetic
duces a lamellar column. Our attempts to simulate the transformations as such, leading to crystallization of cal-
formation of stromatolites at the expense of physiolog- cium minerals; and (6) transformation of sediments into

rock by cementation and consolidation. Essentially the than considering individual species, we focus on the
same pathway is considered in present-day studies [37]. function of their physiological groups and communi-
Issatchenko’s idea concerning the existence of defi- ties. In this case, the role of chemotrophic organisms in
nite species able to precipitate CaCO3 was put in doubt, the calcium cycles comes out manifestly. The alkaline
although, in fact, the important issue here is the occur- barrier generated by communities of microorganisms is
rence of extracellular structures that could act as pre- due mostly to anion decomposition than to alkali pro-
ferred nucleation centers. Given that the slime-forming duction. Therefore, it is the activities of communities of
capacity is species and even strain specific and, in addi- organisms that need to be considered rather than those
tion, depends on the physiological state of the cell, the of individual species. The first step consists in the
existence of certain species, indeed, can be questioned. mobilization of calcium by organisms producing acids,
One factor that determines the role of bacteria as sedi- while the second step is precipitation of carbonates by
mentation surface is the chemical structure of the cap- organisms decomposing acids. The contraposition of
sule with an, apparently, dominant role of sulfur groups primary and secondary anaerobes and of microaero-
in heteropolysaccharides. As a result, after the precipi- philes oxidizing salts of organic acids is very distinct in
tation conditions for calcium carbonate are attained in the calcium cycle. Groups of organisms increasing the
the community the order of precipitation is determined medium pH by eliminating anions set the scene ready
by the selective features of different organisms as for Ca precipitation. At the same time, the process of
nucleation centers. crystallization depends upon specific conditions deter-
The role of bacteria in calcium precipitation was mined by the chemical (and stereochemical) properties
bluntly denied by Strakhov, who claimed that “the sig- of surface structures.
nificance of bacterial calcite forming is negligent” and
“of major importance is the chemical settling of cal- Calcium leaching from rock proceeds under the
cium carbonate and its introduction in the suspended action of dissolved carbonic acid. Initially, carbon is
form” [38]. His viewpoint found wide recognition but concentrated by primary autotrophs, utilizing atmo-
currently is not accepted in such a general form. Mean- spheric CO2 and producing Corg. The utilization of CO2
while, the notion that the role of aerobic organotrophic upsets the carbonate balance and creates conditions for
bacteria consists merely in generating the needed car- CaCO3 sedimentation. The production of CO2 takes
bonate alkalinity conditions, which can also be created place in aerobic and anaerobic decomposition of car-
by the addition of NaHCO3 in amounts equivalent to the bon-rich dead biomass. The fact that CaCO3 sediments
decomposed organic matter, was experimentally sub- occur in the oxygenated zone is explained by biologi-
stantiated by one research team [39]. The specific role cally mediated Corg oxidation. Organic matter decom-
of bacteria was defended by another team [37]. At the position by microaerophilic aerobes under limited
same time, direct examinations of natural samples exchange with the atmosphere gives rise to elevated
reveal that bacterial aggregates quite often occur inside concentrations of CO2 in soil air and groundwater of the
carbonate particles and are encased by bacteria-free oxygenated zone. Free exchange with the air makes
crystalline shells [40]. We see, therefore, that direct ini- degassing possible, and this links carbonate formation
tiating function of bacterial microcolonies and aggre- with oxidative conditions.
gates in carbonate precipitation is superposed by a A tentative generalization can be made that auto-
chemical process of sediment crystallization made pos- trophs contribute to CaCO3 precipitation and organ-
sibly by biologically induced changes in the medium otrophs to its dissolving. This is not quite true, and the
parameters. Sediment crystallization may well be pre- connection, so popular among geologists, between the
ceded by the formation of amorphous colloids studied formation of carbonates and photosynthesis is not uni-
by Chukhrov [41], which transform into crystalline versal, although the main underlying factor is still the
minerals only in the course of diagenesis. alkalization of the medium giving rise to the alkaline
The role of chemotrophic organisms in the calcium barrier. In more detail, the acting groups of microorgan-
cycle will be seen from a different perspective if, rather isms are listed below.
Conditions for CaCO3 precipitation Conditions for CaCO3 dissolution

Oxygenic photoautotrophs Primary anaerobes producing volatile fatty acids; aerobic o
rganotrophs
producing acids (e.g., fungi); lithotrophs producing acids:
nitrifiers,
thionic bacteria, sulfur bacteria
Secondary anaerobes: Homoacetic bacteria
denitrifying sulfate reducers,
methanogens
Aerobes utilizing volatile fatty acids Aerobic organotrophs, especially microaerophiles,
Ammonifying decomposers causing elevated concentration of CO2

10 ZAVARZIN
It is clear from the above list that groups of microor- The role of secondary anaerobes in calcium precip-
ganisms play very definite roles in the calcium and itation and, especially, in the cementation of porous
inorganic carbon cycles and, therefore, the batch effect rock space, is well know. Above all, this function was
can be studied without trying to assign any particular shown in sulfate-reducing bacteria, converting dis-
species a role beyond that of edifier. It should be recog- solved sulfates or gypsum into hydrogen sulfide with
nized with reference to the calcium cycle that it is not concurrent precipitation of calcium carbonate. The for-
particular organisms but rather the environmental con- mation of carbonate is very spectacular in cultures of
ditions for the community that are specific. This point aceticlastic methane-producing bacteria. Owing to cal-
can be readily illustrated by laboratory experiments cite formation, the specific weight of methanosarcinas
relating, for example, to chalk dissolution during carbo- aggregates increases and they start to settle to the bot-
hydrates fermentation and to carbonates production in tom as if their density were 2 g/cm3 [42]. Granules of
acetate decomposition by methanogens and sulfate methanogenic consortia from wastewater treatment
reducers. plants are often covered with carbonate minerals, dom-
inated by CaCO3 [43]. A vivid example of the role of
All cycles of major biogenic elements turn out to be anaerobes in calcite sedimentation is the formation of
coupled with the calcium cycle. In the nitrogen cycle, calcareous crusts with isotopically light carbonate in
ammonifiers produce high pH contributing to carbonate methane seepage areas on the seafloor, e.g., at hydrogen
precipitation. By forming nitrate, nitrifiers dissolve sulfide zone of the Black Sea [18].
limestone, and this, by the way, is an important factor
in the erosion of building surfaces, particularly, in pol- Decomposition in a closed space by microorgan-
luted urban air. Denitrifiers, by decomposing nitrates, isms of Corg concentrated by biota produces CO2 and is
contribute to carbonate precipitation. The oxidation of the major route of accelerated Ca extraction from igne-
reduced sulfur compounds by thionic bacteria leads to ous rock. The second most significant route is the for-
carbonate decomposition and gypsum formation. On mation of organic acids, shown for some aerobic fungi
the mass scale, this process is effective under evaporitic but more typical of the group of primary anaerobes
conditions in formations of reefs. The dissolution of (fermentative microorganisms). The third most signifi-
carbonates present in the stone facing of buildings by cant route is the formation of mineral acids by aerobic
sulfuric acid is intensified by the formation of gypsum, chemolithotrophs, e.g., by nitrifying or thionic bacteria.
which causes exfoliation, as a result of its large specific The latter give rise to gypsum formation and this links
volume. Sulfate reducers, as previously mentioned, the carbonate cycle with the sulfur cycle. Calcium salts
precipitate calcium carbonate. In the phosphorus cycle, of organic acids are decomposed by secondary anaer-
the dissolution of calcium phosphates is caused by obes, above all by sulfate reducers and aceticlastic
numerous acid-producing organisms. The precipitation methanogens, leading to calcium sedimentation and
of phosphates in cyanobacterial mats leads to the for- porous space cementation. Cementation in the oxygen-
mation of phosphorite deposits. The association ated zone might be associated with decomposition of
between the cycles of biogenic calcium and iron is neg- calcium salts of organic acids by aerobes. Anaerobic
ative because iron becomes mobile under the condi- chemotrophic organisms that precipitate CaCO2 and
tions at which the calcium content is low but ferruge- above all primarily sulfate reducers developing in the
neous limestones are formed. porous space precipitate calcite and cause cementation,
which decreases rock permeability. The formation pro-
Most significant for the calcium cycle is the cycle of cess of the carbonate horizon in soils, where organic
organic carbon (Fig. 5). Given that the main suppliers matter undergoes decomposition, was analyzed in
of CO2 to soil (pedospheric) waters are microorganisms detail by soil scientists. A minimal autonomous com-
decomposing concentrated organic matter of the dead munity sufficing for rock degradation is constituted by
biomass, it is easy to see that, under the oxygen atmo- lithophilic lichens, which comprise both producers
sphere, this function is accomplished by aerobic organ- concentrating CO2 into Corg and decomposers [13].
otrophs, sustaining the calcium cycle by dissolving and A comparison of the capacity of different extremely
eventual precipitation of calcium in the course of CO2 anaerobic organisms to dissolve carbonate breccias
degassing into the atmosphere. Under anaerobic condi- showed the strongest process to occur in a culture of a
tions, the relations are basically different. Physiological psychrophilic anaerobic fermenting organism Rumino-
groups of microorganisms are coupled by trophic rela- coccus (=Lactosphaera) palustris, isolated from an
tions in communities. The distribution of groups of outlet of a spring in a forest near Moscow [44]. It is usu-
organisms within the trophic network of the community ally thought that the formation of calcite eliminates
suggests the likely sequence of precipitation and disso- gaseous CO2. In fact, this is not quite true. In accor-
lution of CaCO3. Calcium precipitated by photoautotro- –
phs—the primary producers—is dissolved by primary dance with the equation 2HC O 3 + Ca2+ CaCO3 +
organic-acid-forming anaerobes, to be once again pre- H2O + CO2, the dissolution of calcite leads to the take
cipitated by secondary acid-decomposing anaerobes, up of carbon dioxide, while its sedimentation to evolve-
e.g., methanogens and sulfate reducers, as shown in the ment of CO2, concealed by a relatively high pH. Micro-
diagram of community trophic interactions. flora of decomposers developing in the cold climate can

create an additional sink for CO2 at the expense of car- either dolomite or protodolomite by biological mineral-
bonate dissolution. ization is not known, and they are assumed to form in
This leads to a paradoxical conclusion that regions diagenesis, although high-magnesium calcite can be
of cold humid climate, where carbonates are continu- deposited by bacterial communities. The available evi-
ally dissolved and carried out into the ocean, constitute dence of dolomite depositing in a sulfidogenic commu-
a sink for atmospheric CO2, and warm ocean regions, nity does not necessarily point to the leading role of
where carbonates are deposited, serve as a source of bacteria. The problem of ancient dolomite formation is
CO2. Actually, in the final analysis, carbon dioxide is not yet solved [48].
eliminated by this cycle.
REEFOGENIC FORMATIONS
CALCIFIED MICROBIAL COMMUNITIES AND LANDSCAPE FORMATION
OF THE PAST BY MICROBIAL COMMUNITIES
The leaching by carbon dioxide could be very active The connection between the carbonate cycle and
in the Archean in the period following the degassing of halogenesis, including the sulfate one, becomes mani-
Earth and, therefore, the mobilization of Ca could have fest at the landscape and facies levels. The building of
occurred very early. The ratio between sediments of reefs and large-scale calcium carbonate sedimentation
marine and continental origin can be estimated from the are both caused by activities of communities of organ-
Sr isotopic ratio. The possibility to distinguish between isms that, in addition to skeletal forms, as we currently
basalt and granite as primary sources is based on the know, include carbonate-depositing primary produc-
87Sr/86Sr isotopic ratio, given that basalts are rich in 86Sr ers—algae and cyanobacteria. The net result of their
and continental granites in 87Sr. As a result, the isotopic activities is the accumulation of carbonates, and this
ratio of weathered carbonates is reflected by the seawa- creates specific physical conditions for the community.
ter 87Sr/86Sr ratio. The later figure fails to identify the A model of such ecosystems are coral reefs—the most
continent as the predominant source of Ca. widespread reef builders in modern warm seas. The
Stromatolites, as the most important fossil of the zonal character of calcium carbonate distribution is
Precambrian, were the subject of detailed investiga- closely related with the climatic conditions [38], and so
tions for dozens of years [21]. Stromatolites are lithi- calcareous minerals can be viewed as indicators of
fied remnants of microbial communities, which, in paleoclimate [49].
addition to cyanobacterial edificators, included a vari- A different aspect of microbial formation of calcium
ety of microorganisms that in most cases were able to carbonates relates to paleogeographic conditions. It is
completely decompose organic matter, most often believed that, in thalassocratic epoches, platforms were
replacing it by carbonates. Stromatolites are for the covered by epicontinental seas. The depths were insig-
most part strongly dolomitized. Calcareous algae differ nificant and more or less stable across the whole water
from stromatolites in that their thalli are enclosed in space with leveled bottom profile. The sediment layers
homogeneous fine-grained calcium carbonate. “Blue- propagated over large distances. In humid climates, a
green calcareous algae, dating back to the Cambrian washing out regime can be supposed in which atmo-
time, reached their fullest flower in the Lower Paleo- spheric precipitation reaches considerable depths and
zoic and only in small quantities stepped over the pushes up groundwater, rich in mineral components, to
Mesozoic boundary. No data relating to the calcareous the surface. The epicontinental sea, or some of its parts,
algae of the Cenozoic are available. Sparse populations can be regarded in this case as something like a big fil-
of this algoflora are still found in mostly continental tration window enabling interaction between surface
bodies of water” [45]. and underground waters. This model presumes that the
A clear enough distinction can be drawn between an pool of minerals does not reside in ocean waters only
older epoch of predominantly dolomite formation and but is constituted by the underground hydrosphere,
the later one, which was predominantly calcareous leaching the underlying rock. Emerging to the daylight
[46]. A major part of sedimentary carbonate rock was surface, these waters enter the development region of
formed in the Proterozoic, when only physicochemical photoautotrophic communities. This can explain the
reactions and biogenic ones mediated by prokaryotes high concentrations of mineral components in places of
were effective [47]. Most of dolomites emerged in this development of cyanobacterial mats. The location in
epoch, while the Phanerozoic is characterized by the thalassocratic epochs of continental platforms under
accumulation of limestone and decreased formation of epicontinental seas could contribute to the predominant
development of biocenoses associated with the subsur-
dolomite. Dolomitization proceeds by the reaction Ca2+ +
2–
face hydrosphere and to the formation of vast regions
Mg2+ + 2C O 3 = CaMg(CO3)2, which produces dolo- populated by cyanobacterial mats [50].
mite with the solubility product of 10–15. Dolomite has Fossil organogenic geological structures are isolated
an alternating arrangement of Ca and Mg layers. Under calcareous bodies owing their origin to the activities of
normal conditions, magnesian calcite with interlaced organisms able to accumulate and deposit calcareous
layers of Ca and Mg is produced. Direct production of material. Such structures can be divided into two large

12 ZAVARZIN
CO2 + H2O
oxygenic
photoautotrophs O2
aerobes
organic matter organotrophic
of dead biomass microaerophiles
anaerobic
hydrolytics
primary +
anaerobes dissipotrophs
H2 volatile fatty acids CO2

syntrophs +
acetate CaCO3
Ca2+
Ca-salts
of organic acids
sulfidogens methanogens
CaCO3
secondary
anaerobes
SO42– H2S CH4
sulfur bacteria
CaSO4
Fig. 5. Involvement of calcium in the trophic network of a microbial community.
groups: Precambrian stromatolites and “coral reefs”. Reefogenic formations in sedimentation basins
The latter term broadly refers to a variety of multicellu- emerged in certain facies zones: the front slope; reef
lar skeletal organisms that evolved in Late Precambrian zone, back-reef flats, and shelf lagoon with free water
times and became predominant in the Phanerozoic. exchange. These zones occur in marginal zones of con-
“Coral reefs” are given their name by similarity with tinents, intracontinental glacial troughs, microconti-
modern structures but in the past they also were formed nents, and island arcs. On the landscape level, stromat-
olites formed a sedimentation barrier in the boundary
by other groups of eukaryotic multicellular colonial zone between the shallow shelf and the deeper parts of
organisms, able to form skeletons. These organisms the ocean. This barrier emerged in the process of sedi-
include calcareous algae and multicellular animals with ment movement along the shore and was similar to reef
three-dimensional skeletons. Modern coral reefs are barriers or island chains. Stromatolite belts sometimes
highly complex ecosystems characterized by extraordi- extend several hundred kilometers in length and mea-
nary biodiversity of species, in which the form-giving sure several hundred meters in thickness. On the facies
role is played by corals. Stromatolites and reef builders level, they are similar to tidal flats and sandbars, which
coexisted over a relatively short period. They occurred also serve as sedimentation traps [51].
in different circumstances: stromatolites developed a Geomorphologically, the formation of carbonate
carpet covering of a surfaces—a “mat”,—whereas reefs reefs requires that a limited space be formed, e.g., a
covered rocks. Both types are referred to as biostromata chain of islands or banks produced by the alongshore
when represented by bedded structures and as bioherms movement of sediments. These sediments undergo
when they are dome-shaped. cementing by calcifying communities, e.g., stromato-

lites, and enclose lagoons, where halophilic communi- The key condition for carbonate depositing is the
ties of microorganisms thrive, which are very similar setting of a chemical alkaline barrier. This could be
for different regions. A few examples of such lagoons formed between the continent with soda waters in arid
are those of Sivash [32], California Bay, and Solar Lake parts and the ocean with water composition close to its
in Sinai [52]. Reefogenic formations encircle shallow modern state. The interface zone between continental
waters and restrict water exchange, giving rise under and oceanic waters, in this case, would be the area of
arid conditions to evaporitic circumstances, in which carbonate deposition and a biological ecotone. The
evaporative concentrating of dissolved salts proceeds mixing of waters need not necessarily occur on the con-
until precipitation. As a result, evolvement of the halog- tinental shelf. It could also take place in epicontinental
enous formation occurs. The term halogenous applies seas connected with the ocean but having underneath
here to all readily soluble compounds from calcium sul- the continental rather than oceanic crust.
fate to K, Mg, and Na chlorides and sulfates. In addition
to chloride compounds, sulfates also are regarded as Species of microorganisms are regarded as univer-
belonging to this group, which, by its origin, is con- sally occurring, but the development of their communi-
nected with the evaporitic group. The lagoons provide ties must be closely correlated with the geographic con-
a habitat for halophilic microbial communities, charac- ditions. It is significant that, being confined to certain
terized by the predominance of cyanobacteria in bio- geographic circumstances, cyanobacterial stromato-
geochemical reaction of organic matter production and lites-forming communities themselves were involved in
organisms of the sulfur cycle in decomposition reac- landscape formation on a very large scale. In our view,
tions [32]. reefogenic formations not only give rise to certain
At the same time, a suitable morphology of the physical conditions but also indicate the location of the
coastal zone alone is not enough to build reefs. In cold geochemical barrier between the ocean and the conti-
humid climates, reefs do not form, and mats merely fix nental slope. Carbonic acid weathering on the continent
sediments by the organic matrix, as shown by the exam- sets up the conditions for soda salinization and the for-
ple of the North Sea [53], where calcium is carried out mation of alkaline calcium-free waters. The warm
into the ocean and redistributed by currents. The Baha- ocean serves as a terminal sink for calcium originating
mas serve as a model of contemporary carbonate for- from humid climate regions and the source of endoge-
mation in warm humid climates and the Persian Gulf nous CO2. The alkaline geochemical barrier forms in
area in arid climates [54]. the regions where vadose waters of the continent meet
with oceanic waters. Such locations are indicated by the
“SODA CONTINENT” formation of stromatolites containing phosphates
because phosphates are mobile in alkaline media free
Igneous rock leaching by carbonic acid is regarded from calcium and iron.
as the primary mechanism of calcium mobilization.
Waters of the atmospheric hydrological cycle and To put the hypothesis of the geochemical to test, it
groundwaters react with rock and make the pool of remains to simulate the behavior of cyanobacterial
alkaline waters. Leaching of alkaline-earth metals with communities in the interface region. The experiment
their eventual deposition as carbonates, proceeds under was performed with a culture of Microcoleus chthono-
subaerial conditions and is regarded by geochemists as plastes, isolated from soda lake Khylgatyn, Chita
the major mechanism of eliminating CO2 from the oblast, far eastern Russia. The culture was placed in a
atmosphere. The source of CO2 is assumed to be degas- bath with an agar slope that had a hole filled with a
sing that proceeds predominantly outside continental medium for alkaliphilic cyanobacteria with pH 10.2. In
platforms through the seafloor. The conventional con- a different version, the slope was made of potter’s clay
cept that immediately follows is that, originally, the the wet surface of which was covered by a thin layer of
ancient ocean was mildly acidic [55]. hot agar (10 ml/100 cm2) to preclude mudding. The
deeper part of the bath was filled with a 20-mM solu-
Meanwhile, subaerial leaching by carbonic acid in tion of CaCl2 and MgCl2 in 3.5% NaCl. The “continen-
arid climates unavoidably results in soda mineraliza- tal” component in this experiment was represented by
tion and formation of solods in the pedosphere. The soda waters, in which only anions were mobile,
scale of soda water production was estimated within the whereas the “seawater” contained a variety of cations.
framework of the “soda ocean” hypothesis [7, 56]. It Microcoleus chthonoplastes was plated midway
could be very large in internal parts of supercontinents, between the hole and the “ocean.” The trichomes of the
such as Pangaea. The location of contemporary soda cyanobacterium spread by gliding on the wet surface.
deposits is indicative of this possibility. Groundwaters The formation of calcium carbonate beneath the shore-
resulting from leaching are alkaline [5] and could pro- line of the “ocean” was apparent in the form of a char-
vide habitats for a relict alkaliphilic microbial commu- acteristic strip of white globules in the diffusion area of
nity. Alkaliphilic, obviously not oceanic, microflora soda water from the hole. The formation of carbonate
could be functionally quite diverse [57, 58]. was especially abundant in zones of massive growth of

14 ZAVARZIN
atmosphere
ëO2, atm
oxygenic O2
autotrophs
NPP +
biomass
dead biomass ëÓrg
decomposition,
NEP biomass
humus, NBP
ëO2, soil air
kerogen, NGP
pH of groundwater
leaching with
phosphates carbonic acid of Ca- clays
and Mg-bearing weathering crust rock
CaSiO3 + 2H2O + 2CO2 = Ca(HCO3)2 + SiO2

bicarbonates
of the ocean
Ca+Mg bicarbonates brought
with runoff into the ocean
Ca(HCO3)2 = CaCO3 + H2O + CO2
CaMg(CO3)2 carbonates reef-building stromatolites

of sedimentation basins
of the Phanerozoic
geological recycling of sedimentary rock,

e.g., by subduction
CO2 with volcanism
and regassing
spreading
degassing
mantle
Fig. 6. Participation of biota in the calcium cycle: NPP is the net primary production (photoassimilation minus respiration); NEP is
the net ecosystem production (NPP minus annual decomposition by organotrophs) at balance with O2 utilized by organotrophs;
NBP is the net biome production; and NGP is the net geosphere production due to deposition during sedimentation.
the organism. Outside the growth zone of microcoleus, CONCLUSION

the chemical sedimentation of carbonate was scattered
and its density much lower. This model illustrates the The overall diagram of the coupling between cal-
cium and carbon cycles is shown in Fig. 6.
correlation between the development of microcoleus
and the alkaline barrier, where calcium is deposited. Having considered the role of microbial communi-
Naturally, this 20-cm model is no more than a school- ties in the circulation of calcium and inorganic carbon,
level illustration of the basic idea. one can easily see how wrong it is that one of the most

important biologically mediated geochemical pro- REFERENCES

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played by communities of microorganisms. The direc- Calculation of the Solubility of Calcite in the CaCO3–
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Research Program “Global Environmental and Cli- and Demkin, V.A., On the Ratio of Pedogenic and Litho-
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Microbiology, Vol. 71, No. 1, 2002, pp. 1–17. Translated from Mikrobiologiya, Vol. 71, No. 1, 2002, pp.

Microbial Geochemical Calcium Cycle

0026-2617/02/7101-0001$27.00 © 2002 åÄIä “Nauka /Interperiodica”

Ca pool Carbonate exportation in geological

Fig. 1. Calcium pathway in the lithosphere.

MICROBIOLOGY Vol. 71 No. 1 2002

conditions. Under such circumstances, it is often hard

MICROBIOLOGY Vol. 71 No. 1 2002

MICROBIOLOGY Vol. 71 No. 1 2002

genic acceleration of limestone leaching can be as high H2O

MICROBIOLOGY Vol. 71 No. 1 2002

OH– anhydrase [CO 2– ]

CaCO3 of the coccolith

Fig. 3. Deposition of calcium carbonate in cells of coccolithophorides.

MICROBIOLOGY Vol. 71 No. 1 2002

MICROBIOLOGY Vol. 71 No. 1 2002

MICROBIOLOGY Vol. 71 No. 1 2002

Conditions for CaCO3 precipitation Conditions for CaCO3 dissolution

MICROBIOLOGY Vol. 71 No. 1 2002

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MICROBIOLOGY Vol. 71 No. 1 2002

H2 volatile fatty acids CO2

Fig. 5. Involvement of calcium in the trophic network of a microbial community.

MICROBIOLOGY Vol. 71 No. 1 2002

MICROBIOLOGY Vol. 71 No. 1 2002

CaSiO3 + 2H2O + 2CO2 = Ca(HCO3)2 + SiO2

Ca(HCO3)2 = CaCO3 + H2O + CO2

CaMg(CO3)2 carbonates reef-building stromatolites

geological recycling of sedimentary rock,

the organism. Outside the growth zone of microcoleus, CONCLUSION

MICROBIOLOGY Vol. 71 No. 1 2002

important biologically mediated geochemical pro- REFERENCES

MICROBIOLOGY Vol. 71 No. 1 2002

MICROBIOLOGY Vol. 71 No. 1 2002

MICROBIOLOGY Vol. 71 No. 1 2002

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