CHEMICAL

GEOLOGY
INCLUDING
ISOTOPE GEOSCIENCE
ELSEVIER Chemical Geology 132 (1996) 5-9

How microbes influence mineral growth and dissolution

Henry L. Ehrlich
Department of Microbiology, Rensselaer Polytechnic Institute, Troy, NY 12180-3590, USA
Received 3 June 1995; accepted 17 November 1995

Abstract

Mineral formation or dissolution is exploited by microbes if it favors their survival. Some microbes are able to dissolve a
mineral by using it: (1) as a source of energy, (2) as a terminal electron acceptor in respiration, (3) as a trace element
requirement, or (4) to enhance competitiveness in a microbial community. Some others form minerals: (1) in the oxidation or
reduction of a dissolved inorganic species in energy metabolism; (2) in the detoxification of poisonous inorganic species; (3)
in active or passive uptake of one or more dissolved inorganic species followed by conversion into a cellular support or
protective structure; and (4) in enhancing their competitiveness in a microbial community. Microbes that interact with
mineral substances are opportunists. Many have a significant impact on the mineral world by catalyzing, or controlling in
other ways, key steps ia mineral formation or dissolution.

1. Introduction building stone and stone sculptures (e.g., Krumbein

Microbes influence the kinetics and course of
reactions involving ~Lissolution of a number of min-
erals, and they alsc, influence the authigenic and
diagenetic formation of a number of minerals in the
lithosphere and hydrosphere of the Earth. One reason
why some microbes, especially bacteria, form miner-
als or dissolve them is that they gain energy from the
process, or it enables them to carry out respiration
when oxygen is limiting or absent. Another reason is
that they may satisfy some or all of their trace
element requirement,; and that of other organisms in
their community with dissolved mineral constituents
[for a review, see Ehrlich (1990)]. Mineral dissolu-
tion by microbes is commercially exploited in bi-
oleaching of metal walues from ores and in biobene-
ficiation of ores (ore enrichment) (Ehrlich and Brier-
ley, 1990). Undesirable effects of microbial mineral
dissolution are manifested in the deterioration of
et al., 1991; Urz~ et al., 1991, 1994).
2. Examples of microbial control of mineral for-
mation and dissolution
In certain environments, some microbes may cause
formation of specific minerals by precipitating dis-
solved components of the minerals through enzyme-
catalyzed oxidation or reduction. In a microbial oxi-
dation process, some of the energy released may be
conserved by the organism. In a microbial reduction
process, the inorganic species being reduced very
likely serves as tenaainal electron acceptor in a respi-
ratory process in which it partially or totally replaces
0 2 . Microbes may also oxidize or reduce inorganic
species as a means of making them less toxic, the
product of the reaction being less toxic than the
reactant (substrate).
Not all microbially formed minerals are generated

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6 H.L. Ehrlich/Chemical Geology 132 (1996) 5-9
enzymatically. Some may be formed by microbes
through passive or active uptake of one or more
inorganic ion species, followed by conversion into a
salt or oxide for cellular support or protection. In this
process, the microbes may serve as templates by
specifying the structural arrangement of the mineral
aggregate they form.
Each of the foregoing reactions may enhance the
competitiveness of the responsible microbe in a bio-
logical community. For example, when toxic metal
ions are present in an aqueous environment, bacteria
that can immobilize these metals by fixing them in
their cell envelope (e.g., Beveridge et al., 1983;
Ferris et al., 1986), or precipitate them as sulfides,
carbonates or phosphates external to their cells (see
Ehrlich, 1990) have an advantage over bacteria and
other microbes susceptible to poisoning by these
toxicants and lacking an ability to detoxify them.
Microbes like diatoms that form frustules,
foraminifera that form calcareous tests, or coccoliths
that form calcareous cell walls (Lowenstam, 1981),
are protected from physical damage such as that
which may result from shear or hypo-osmotic condi-
tions. They may also be protected from predation by
some microbes. Organism lacking this protection are
clearly at a disadvantage. In anaerobic environments,
bacteria that can use inorganic electron acceptors
like nitrate, ferric ion, sulfate and others in their
energy-generating metabolism have a thermody-
namic advantage over fermenting bacteria that can-
not use externally supplied electron acceptors in their
energy-generating metabolism (Ehrlich, 1990, 1993).
In microbial mineral formation, catalysis usually
accelerates the overall rate of reaction whether in a
single chemical step or multiple steps. In the latter
instance, the overall rate of reaction is determined by
catalysis of the rate-controlling reaction. In Mn(IV)-
oxide (MnO 2) formation from the oxidation of Mn(II)
at neutral pH, for example, the oxide is generated
very slowly in the absence of manganese-oxidizing
bacteria. The reaction sequence in the absence of
bacteria has been reported to involve two steps (Hem,
1981; Hem and Lind, 1983; Hem et al., 1982; Mur-
ray et al., 1985). In the first step, divalent manganese
is rapidly oxidized to trivalent manganese (Mn304
(hausmannite) or MnOOH):
3Mn2+ + 3H20 + 0.502 ~ Mn304 + 6H+ (1)
or
2Mn 2+ + 0.502 --~ 3H20 ~ 2MnOOH + 4H + (2)
The hausmannite or MnOOH then disproportion-
ate very slowly in a second step to tetravalent man-
ganese (MnO 2) and Mn 2+,
Mn304 + 4H + ~ MnO 2 + 2Mn 2+ + 2 H 2 0 (3)
or
2MnOOH + 2H + ~ MnO 2 + Mn 2+ + 2 H 2 0 (4)
Because reactions (3) and (4) are slow, they are
clearly rate controlling in the abiotic formation of
MnO z. Bacteria that oxidize Mn 2+ to MnO 2 form
MnO 2 much more rapidly than reactions (1) and (3)
or (2) and (4) (Ehrlich, 1990). Ehrlich (1990) pro-
posed that the bacteria may first enzymatically oxi-
dize Mn 2+ to Mn(III) that remains bound to the
manganese-oxidizing enzyme. The enzyme then cat-
alyzes an oxidation of the bound Mn(III) to MnO 2
rather than a disproportionation to Mn 2+ and MnO 2.
Reactions (5) and (6) summarize this process,
2Mn 2+ + 0.502 + 2H + ~ 2{Mn 3+ } + H 2 0 (5)
2{Mn 3+ } + 0.502 + 3 H 2 0 --* 2MnO 2 + 6H + (6)
where {Mn 3+ } represents enzymatically bound Mn 3+.
The manganese-oxidizing enzyme is assumed to be a
multifunctional catalyst. Assuming reactions (5) and
(6) describe bacterial Mn 2+ oxidation correctly, bac-
terial enzyme catalysis not only accelerates the con-
version of Mn(III) to Mn(IV), but also insures that
all Mn(III) as it is formed is converted to Mn(IV)
rather than just 33% or 50% of it, as in Mn(III)
disproportionation of Mn304 or MnOOH under abi-
otic conditions. In other words, bacterial catalysis by
the proposed mechanism not only speeds up the rate
of formation of MnO 2, but it also redirects the
course of the reaction by changing it from a dispro-
portionation to a full oxidation of Mn(III) to Mn(IV).
It is theoretically possible that bacterial oxidation
of Mn 2+ proceeds in a single step with some or all
bacterial Mn 2+ oxidizers, i.e., without intermediate
formation of Mn 3+ :
Mn 2+ + 0.502 + H 2 0 --9 MnO 2 + 2H + (7)
This reaction yields the same amount of energy
(AG' o - 16.3 kcal per mol Mn 2+) as reactions (5)
 H.L. Ehrlich/ Chemical Geology 132 (1996) 5-9
plus (6). However, the two electrons removed from
Mn 2÷ are not equivalent energetically, which makes
this one-step oxidation mechanism in reaction (7) not
very likely. If bacterJLa were to oxidize Mn 2÷ accord-
ing to this mechanism, they would modify the course
followed by abiotic Mn 2+ oxidation even more dras-
tically than by the mechanism summarized in reac-
tions (5) and (6).
In mineral dissolution, microbial catalysis also
accelerates the process by exerting control over the
reaction kinetics andt sometimes alters the course of
the overall reaction. An example is the oxidation of
iron pyrite to ferric, sulfate. Its reaction sequence
explains the origin of acid coal mine drainage. At pH
2.5, the oxidation of pyrite is very slow in the
absence of appropriate bacteria. In the presence of
acidophilic Thiobacillus ferrooxidans, pyrite oxida-
tion is accelerated by as much as six orders of
magnitude (Singer and Stumm, 1970). Key reactions
in the oxidation of pyrite are the following:
FeS2 + 3.502 + H 2 0 --* Fe2+ + 2H++ 2SO 2- (8)
2Fe2+ + 0.502 + 2 H + ~ 2Fe3÷ + H 2 0 (9)
FeS z + 14Fe3+ + 8H20 --. 15Fe2÷ + 2SO 2- + 16H +
(10)
Reactions (8) and (9) are bacterially catalyzable.
In the presence of T. ferrooxidans, reaction (8) is
rate-controlling initially, but as pyrite oxidation pro-
gresses, reaction (9)becomes rate controlling, and
reaction (10), which is not bacterially catalyzed,
largely displaces reaction (8). In the absence of T.
ferrooxidans, reaction (9) never acquires importance
because autoxidation of Fe 2+ to Fe 3+ is extremely
slow at acid pH. As a result the dissolved iron is
mostly ferrous. Depe.nding on the pH of the reaction
milieu, a portion of the oxidized iron produced by T.
ferrooxidans may precipitate as basic ferric sulfate
such as jarosite, AFe3(SO4)2(OH) 6, where A may
stand for H +, H 3 0 +, Na +, K +, NH~-, or some other
cation (see discussion in Ehrlich, 1990).
An example of a :reductive, mineral-forming reac-
tion that can be slow in the absence of bacteria,
especially around neatral pH, is bacterially catalyzed
reduction of Cr(VI) to Cr(III). In this instance, the
responsible bacteria form a protein (enzyme) that
enters directly into the reductive reaction as a cata-
7
lyst. The reaction is environmentally very beneficial
in that it leads to detoxification of highly toxic
Cr(VI) by converting it to relatively non-toxic Cr(III)
as in Cr(OH) 3. Cr(VI) is a mutagen and carcinogen.
To a significant extent, the low toxicity of Cr(III) is
due to its low solubility around neutral pH. Some
bacteria reduce Cr(VI) to Cr(III) enzymatically under
aerobic and anaerobic conditions, while others re-
duce it only anaerobically. In either case, the reduc-
tive half-reaction is described by:
CrO42- + 5H++ 3e ~ Cr(OH)3 + H2 O (11)
The oxidative half-reaction to which the reductive
half-reaction is coupled, involves the oxidation of an
organic electron donor such as glucose, acetate or
citrate. Cr(OH) 3 represents a convenient formulation
of a hydrated chromium oxide. Cr(V) may be a
transient intermediate in Cr(VI) reduction (Cervantes,
1991; DeLeo and Ehrlich, 1994; Shi and Dalal,
1990; Suzuki et al., 1992).
Cr(VI) may also be non-enzymatically reduced to
Cr(III) by bacteria. In this case the bacteria generate
the reductant for Cr(VI) reduction enzymatically in
their energy-generating metabolism, but the reduc-
tion of Cr(VI) by the reductant in the subsequent
reaction is purely chemically, i.e., it is not catalyzed
by any enzyme. To give a specific example, Fe3÷-re-
ducing bacteria generate Fe 2÷ enzymatically. In the
presence of Cr(VI), this Fe 2÷ then reduces Cr(VI) to
Cr(III) non-enzymatically. Similarly, sulfate-reduc-
ing bacteria generate HS- from SO42- enzymati-
cally. In the presence of Cr(VI), this HS- then
reduces it to Cr(III) non-enzymatically (e.g., DeFil-
ippi, 1994). The HS- becomes reoxidized to S O
a n d / o r SO2- in the process. In all of these reac-
tions, the bacteria control the rate of Cr(VI) reduc-
tion by the rate at which they generate the reductant.
In their absence, the reduction of Cr(VI) is either
extremely slow or undetectable.
Diatoms, single-celled algae with a siliceous cell
wall, are examples of organisms that form a highly
organized, species-specific (genetically determined)
polysilicate structure from dissolved orthosilicate.
The cell in this case provides a template that directs
silicate-deposition into the intricately designed frus-
tule by which each species is recognized. The uptake
and integration of silicate into the frustule structure
8 H.L. Ehrlich/Chemical Geology 132 (1996) 5 - 9
is an active process that is driven by cellular pro-
cesses of energy conservation (photosynthesis in the
light; glucose oxidation in the dark). Whereas the
rate of silicate uptake by diatoms has been measured
in the laboratory, the mechanisms by which the
mono-silicate taken into the cell is incorporated into
the frustules remains unelucidated. It is clear, never-
theless, that mono-silicate would not organize itself
into the silica arrangement in the frustules in the
absence of diatoms (see discussion by Ehrlich, 1990).
Some bacteria and fungi are able to accelerate
dissolution of silicates and aluminosilicates. To date,
their action on these minerals has all been character-
ized as non-enzymatic. The mechanisms by which
they act may involve production of metabolic prod-
ucts such as organic acids that can act as acidulants
a n d / o r ligands, base in the form of NH3, and spe-
cific capsular slime from bacteria. Among the acids,
2-ketogluconic acid formed by some bacteria, and
citric and oxalic acids formed by some fungi have
been shown very effective in the dissolution of sili-
cates (Duff et al., 1963; Vandevivere et al., 1994;
Welch and Ullman, 1993). They furnish protons that
help in breaking Si-O and A1-O bonds through
protonation and catalysis. At the same time, some of
the acids may also act as ligands that pull cations
from the framework of the crystal lattice, facilitating
subsequent breakage of framework bonds. Some bac-
terial slimes (acid polysaccharide) have been re-
ported to form complexes with silicate that lead to
silicate solubilization (e.g., Malinovskaya et al.,
1990). Since the active microbes may live in biofilms
on a mineral surface, the critical metabolic products
they produce encounter the silicate or aluminosilicate
at relatively high concentration and thereby have a
positive effect on the kinetics of the solubilization of
the mineral.
3. Conclusions
These few examples make it clear how microbes
can control mineral formation and degradation,
namely by affecting reaction kinetics and, in some
cases, direct the course of the reaction. Since mi-
crobes are ubiquitous in nature and can exist at
environmental extremes of temperature, hydrostatic
pressure, pH, and redox potentials, their influence on
minerals is felt everywhere in the biosphere. Mi-
croorganisms that promote mineral formation or
degradation are opportunists that exploit environ-
mental situations in which other microbes are at a
disadvantage. Thus, they have a significant impact
on the mineral world and thereby on the land- and
seascape around us.
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