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OCR for page 3404
Proc. Natl. Acad. Sci. USA
Vol. 96, pp. 3404-3411, March 1999
Colloquium Paper
This paper was presented at the National Academy of Sciences colloquium "Geology, Mineralogy, and Human Welfare, "
held November 8-9, 1998 at the Arnold and Mabel Beckman Center in Irvine, CA.
Biological impact on mineral dissolution: Application of the lichen
model to understanding mineral weathering in the rhizasphere
JILLIAN F. BANFIELD*, WILLIAM W. BARKER, SUSAN A. WELCH, AND ANNE TAUNTON
Department of Geology and Geophysics, University of Wisconsin, Madison, WI
ABSTRACT Microorganisms modify rates and mecha-
nisms of chemical and physical weathering and clay growth,
thus playing fundamental roles in soil and sediment forma-
tion. Because processes in soils are inherently complex and
difficult to study, we employ a model based on the lichen-
mineral system to identify the fundamental interactions. Fixed
carbon released by the photosynthetic symbiont stimulates
growth of fungi and other microorganisms. These microor-
ganisms directly or indirectly induce mineral disaggregation,
hydration, dissolution, and secondary mineral formation.
Model polysaccharides were used to investigate direct medi-
ation of mineral surface reactions by extracellular polymers.
Polysaccharides can suppress or enhance rates of chemical
weathering by up to three orders of magnitude, depending on
the pH, mineral surface structure and composition, and
organic functional groups. Mg, Mu, Fe, Al, and Si are redis-
tributed into clays that strongly adsorb ions. Microbes con-
tribute to dissolution of insoluble secondary phosphates,
possibly via release of organic acids. These reactions signifi-
cantly impact soil fertility. Below fungi-mineral interfaces,
mineral surfaces are exposed to dissolved metabolic byprod-
ucts. Through this indirect process, microorganisms can
accelerate mineral dissolution, leading to enhanced porosity
and permeability and colonization by microbial communities.
Mineral Weathering, Microbes, and Geochemical Cycles
The Importance of Mineral Weathering. Rocks at the
Earth's surface typically formed at high temperature and
pressure. Exposure of the minerals to oxygenated solutions
initiates chemical and physical reactions, resulting in mineral
dissolution and crystallization of new phases, such as clays, that
are more stable at Earth's surface conditions (Fig. 1~. Nano-
crystalline products contribute abundant reactive surface area
and thus can impact bioavailability of beneficial and toxic
elements (Fig. 2~. Weathering affects the compositions of
ground water, river and lake water, and ultimately, of oceans
(1~. Resistant primary and secondary minerals are redistrib-
uted to form sediments and soils. Thus, weathering leads to a
major geochemical fractionation near the Earth's surface.
Such reactions have occurred throughout geological time,
shaping the compositions of the mantle, crust, hydrosphere,
and atmosphere. Mineral weathering also directly impacts
humans, affecting water quality, agriculture, architectural sta-
bility, landscape evolution, integrity of repositories for high
level nuclear waste, and distribution of mineral resources.
Microbial Distributions in Natural Environments. Mi-
crobes inhabit diverse environments at, and near, the Earth's
surface. Their potential to cause geochemical change is im-
mense. Viable cells exist in extreme environments, from
subzero temperatures in Antarctica (2-5) to above boiling
PNAS is available online at www.pnas.org.
temperatures in hot springs and hydrothermal vents (6~.
Microbes are essentially ubiquitous in sediments, and meta-
bolically active cells have been discovered in rocks buried
several kilometers below the Earth's surface (6-14~.
Of the three domains of life, the majority of microorganisms
reported to date from soils and sediments are bacteria (11,
15-21~. Archaea, minor members of many microbial popula-
tions, are especially important under more extreme conditions,
such as those encountered in saline lakes (22) and very hot
aqueous environments (22-24~. Eukaryotes typically occur in
more moderate environments, although some fungi and pro-
tists thrive at very low pH (refs. 25 and 27; K. J. Edwards, T. M.
Gihring, and J.F.B., unpublished data). Recent surveys of
subsurface aquifers show large microbial populations, ~105-
108 cells/cm3 (15, 28-30). Cell concentrations ranging from
103 to 109 cells/cm3 have been reported from soils, sediments,
and natural waters (15, 31-33). Greater than 108 cells/cm2 of
surface area occur on metal sulfide minerals (25-27).
Why Do Microbes Interact with Minerals? Some biologi-
cally essential elements are readily available from natural
waters (e.g., Ca, Si, carbonate needed for structural fabrica-
tion) (34), but a subset must be actively scavenged (e.g., Fe, K,
P). All organisms need Fe, but the solubility of Fe in natural
oxygenated near-surface waters is low (35). Some organisms
synthesize Fe-specific complexing agents to improve Fe bio-
availability (35-41). Other microbes utilize compounds that
act as electron shuttles to improve accessibility to redox sites
within minerals. Enzyme cofactors such as Mo, Cu. Zn, Mg,
Fe, Cr. and Ni can be derived by dissolution of sulfide minerals
and ferromagnesian silicates. Phosphorus, required for con-
struction of DNA, RNA, ADP, ATP, phospholipids, and
polyphosphates, is available by dissolution of minerals such as
apatite tCas(PO4)3(F, Cl, OH)] and other typically less soluble
secondary phosphates (42-44~. A subset of organisms (litho-
trophs) associate closely with minerals because they derive
their metabolic energy from inorganic substrates (e.g., Mn+2,
Fe+2, S. NH4+, and H2) (7, 45-484. Other microbes (hetero-
trophs) utilize organic material originating from photosyn-
thetic or lithotrophic microorganisms, and compounds such as
02, NO3, Fe+3, and SO4 2 serve as electron acceptors (45, 46~.
Some interactions between cells, organic products, and
minerals liberate ions from surfaces. This may be incidental
(indirect consequences of growth) or under cellular control.
Deciphering these interactions constitutes an important chal-
lenge for the future. Regardless of whether microbe-mineral
interactions are directed or otherwise, microbial stimulation of
mineral dissolution directly affects the fertility of agricultural
and other soils.
Microbial Controls on Mineral Weathering Reactions.
Most geochemical research on mineral weathering has focused
*To whom reprint requests should be addressed. e-mail: jill@geology.
wisc.edu.
3404
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Colloquium Paper: Banfield et al.
FIG. 1. A granite weathering profile that passes from almost fresh
rock (below) into soil. Characterization of the mineralogy and micro-
biology of samples from throughout this profile reveals chemical and
physical changes that accompany soil formation.
on inorganic aspects (49~. These studies provide valuable
information on chemical dissolution rates, mechanisms, and
products. Results reveal the order of reactivity of silicate
minerals and show how rates depend on temperature, pH, and
mineral and solution compositions. The absolute values of
rates remain in considerable dispute. Conversely, soil scientists
and agronomists have long recognized the fundamental im-
portance of microorganisms in soil development (504.
Understanding of near-surface systems requires integrated
mineralogical, geochemical, and biological analysis. A variety
of organic metabolic products can dramatically suppress or
greatly accelerate rates of dissolution and secondary mineral
formation (51-56~. Energy generation by catalysis of redox
reactions greatly affects element speciation (45, 46~. The form
of nitrogen is dramatically modified by microbial nitrogen
fixation. Organic detritus greatly modifies the water retention
capability and physical properties (porosity and permeability)
of sediments and soils (57~. Conversely, availability of metal
oxides, sulfides, and hydroxides able to support lithotrophic
growth, redox state, and pH dramatically controls microbial
populations. Clay precipitation reactions may provide proton
sources or sinks, and a variety of silicate minerals may serve as
sources of metal reductive and oxidative power. In this paper,
we discuss physical, chemical, and biochemical aspects of
mineral dissolution and clay formation. Our approach is to
FIG. 2. High-resolution transmission electron microscope
(HRTEM) image of nanocrystalline material produced by chemical
weathering.
Proc. Natl. Acad. Sci. USA 96 (1999) 3405
analyze the lichen-mineral microcosm to identify the key
factors responsible for microbe-mineral interactions and then
to combine mineral and microbial characterization and exper-
imentation to quantify the impact of these factors.
Incipient Weathering and Microbial Colonization. In the
initial stages of alteration, only rock surfaces exposed to air
and water are colonized by biofilms. Because of space restric-
tions, incipient weathering at distance from the biofilm-
mineral interface is predominantly inorganic. Inorganic reac-
tions are restricted to sites of fluid access, typically at grain
boundaries or in proximity to defects, and to reactions involv-
ing readily exchangeable ions (such as interlayer sites in layer
silicates) (58-60~. Transmission electron microscope investi-
gations show that incipient silicate weathering involves surface
hydration, surface recrystallization, and release of ions to
solution (60, 61~. The scales of elemental redistribution are
small, and primary mineral chemical gradients are preserved
(62~. Surface energy minimization leads to secondary minerals
(clays and nanocrystalline oxyhydroxides) in highly specific
orientations with respect to the parent mineral (Fig. 3~. Thus,
mineral surfaces are often coated by clays that largely fill space
created by dissolution (63), leaving little room for microbial
occupancy. Only after rock density is significantly reduced by
dissolution does sufficient (micron-scale) space develop for
microbial colonization to proceed.
Dissolution of reactive phases (e.g., reduced minerals such
as sulfides, olivine, and soluble solids such as glass) may
facilitate microbial colonization. Metal sulfides, minor com-
ponents of most crustal rocks (e.g., granites, basalts, meta-
morphic rocks), may be the first minerals to undergo chemical
weathering, leading to generation of acid by the reaction
FeS2(aqueous) + 15/4°2(gas) + 7/2H2O(liquid) ~ Fe(°H)3(solid)
+ 2H2SO4(aqueous
The rate of bacterial oxidation of ferrous iron released from
pyrite surfaces is up to one million times faster than the
inorganic oxidation rate at low pH (64~. Because Fe3+ is the
predominant pyrite oxidant at low pH, acid generation rates in
natural environments are largely determined by microbial
activity (65, 66~. If sulfide mineral weathering in rocks is
microbially mediated, sulfide dissolution can lead directly to
colonization by lithotrophic species. Sulfuric acid generated by
sulfide dissolution accelerates dissolution of surrounding sili-
cates, increasing porosity available for microbial access and
colonization.
What Can We Learn from the Lichen-Mineral Microcosm?
A wide variety of microorganisms colonize mineral surfaces,
among the most familiar of which are lichens. Although
FIG. 3. High-resolution transmission electron microscope
(HRTEM) image showing clays reaction products formed during early
weathering of pyroxene develop in highly specific orientations with
respect to the parent structure.
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3406 Colloquium Paper: Banfield et al.
FIG. 4. Optical micrograph showing a cross section through the
lichen-feldspar interface. Photosynthetic microorganisms (pm) exist
within the upper levels of a mass of fungal hyphae (h). A fungal fruiting
body (a) is present in this image. Fungal hyphae contribute to physical
weathering by penetrating feldspar cleavages and grain boundaries to
expose the interior of crystals to microbial colonization.
classically described as symbiotic associations between photo-
synthetic microorganisms and fungi (67, 68), lichens are actu-
ally extremely complex microbial communities. A mass of
fungal hyphae, or thallus, composes the majority of any lichen.
Photosynthetic microorganisms lie just beneath the upper
surface. Although these are typically green algae, other pho-
tosynthetic microbes such as diatoms and cyanobacteria occur.
This upper zone is a region of carbon transfer, in the form of
sugars, between the photosynthetic assemblage and the fungal
Proc. Natl. Acad. Sci. USA 96 (1999J
partner. Lower light levels preclude photosynthesis deeper
within the lichen thallus, but other prokaryotes reside among
the fungal hyphae. Little is known regarding the biodiversity of
this nonphotosynthetic assemblage, and the role these organ-
isms play in nutrient transfer from substratum to fungus is a
fertile area for research.
Lichens accelerate the degradation of minerals by physical
and chemical methods and are ideal microcosms in which to
study microbially mediated mineral weathering. Their extent is
easily defined and sampled, and a limited assemblage of
minerals grading from fresh to weathered is usually present.
Ideally, mineral surfaces of known age (e.g., tombstones,
building surfaces, or quarry faces) are studied, permitting
field-based weathering rate determinations. Fungal hyphae,
perhaps acting in concert with physical weathering mecha-
nisms such as freeze-thaw, penetrate mineral cleavages and
grain boundaries, leading to accumulation of substratum-
derived mineral fragments within the lower thallus (Fig. 4~.
The intact organomineral interface from lichen-encrusted
boulders in a 90-year-old rock quarry (52) was characterized by
transmission electron microscopy. Mineral surfaces in micro-
bially colonized regions are coated in complex mixtures of high
molecular weight polymers, clays, and oxyhydroxides. Cells are
attached to mineral surface and mineral weathering proceeds
via polymer-mediated dissolution/transport/recrystallization.
Chemical weathering is accelerated relative to uncolonized
surfaces.
A zone model for microbially mediated mineral weathering
has been developed (Fig. 5) based on correlation of different
styles of silicate mineral weathering with pore size-controlled
microbial distributions (53~. In brief, Zone 1 consists of the
upper lichen thallus and is devoid of weathering of substratum
FIG. 5. Zone model cartoon illustrating mineral weathering occurring in zones that are impacted by microbes to different degrees and in different
ways. Zone 4 includes unweathered rock and rock incipiently weathered by inorganic reactions. Zone 3 is where reactions are accelerated by dissolved
organic molecules (predominantly acids) but cells are in direct contact with reacting mineral surfaces. Zone 2 is the area of direct contact between
microbes, organic products, including polymers, and mineral surfaces. Zone 1 is where photosynthetic members of the symbiosis generate fixed
carbon and where crystalline lichen acids precipitate.
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Colloquium Paper: Banfield et al.
FIG. 6. This energy-filtered transmission electron microscope
(EFTEM) zero loss image reveals that complex mixtures of organic
polymers (p) and clay minerals (c) exist at the lichen-microbe inter-
face.
derived mineral particles. Zone 2 is a region of extreme
mineral weathering, characterized by direct contact between
cells, extracellular polymers, associated compounds, and min-
eral surfaces. Complex, nanometer-scale mixture of clay prod-
ucts, organic polymers, and primary minerals are common
(Fig. 6~. In some cases, mineral formation on cell surfaces
preserves relict cell shapes. Unlike essentially inorganic weath-
ering, the secondary mineral orientations are less controlled by
the primary mineral structure and are more determined by the
distribution of polymers onto which they nucleate. Zone 3
weathering reactions, although accelerated by microbial prod-
ucts, are not mediated by direct microbial contact. Orienta-
tions of secondary minerals are more commonly determined
by orientations of the primary minerals, as for essentially
inorganic reactions. Unweathered minerals and minerals un-
dergoing early, predominantly inorganic reactions comprise
Zone 4 (Fig. 5).
Application of Insights from the Lichen-Mineral Interface
to Soils
Microbial Populations in Soils. Microbial populations in-
crease in abundance and diversity as rock is weathered and
transformed to soil. In parallel, the microstructure and chem-
ical complexity of the system increases, making high-resolution
studies of processes occurring in soils extremely difficult. For
this reason, the lichen-rock interface is a preferable system for
study. Insights from the lichen system then must be tested for
their applicability to soils.
A diverse community, comprised of extremely high numbers
of symbiotic and nonsymbiotic microorganisms, inhabit the
soil zone around the roots of vascular plants. Although mi-
crobial concentrations in soils are very high, ~109 cells/cm3,
only ~1-10% of the total, are alive (29~. Thus, viability may
ultimately prove to be a more important parameter than
diversity or overall cell counts for mineral weathering studies.
The assemblage of plant roots and their associated micro-
flora and fauna in intimate contact with soil particles is termed
the rhizosphere. Because many studies reveal the importance
of microbe-mineral interactions to plant nutrition (69), it is
critical to understand the rates and mechanisms of mineral
transformations occurring in the rhizosphere.
Which Microorganisms Are Involved? Microbial popula-
tions In soils are very diverse. One gram of soil can contain
anywhere from hundreds to many thousands of species of
microorganisms (16-21, 70, 71~. Furthermore, the level of
Proc. Natl. Acad. Sci. USA 96 (1999) 3407
diversity from agricultural soils reported in molecular biolog-
ical studies is astonishing.
Identification of individual microbial cells in natural samples
minerals remained challenging until recently. Traditional mi-
crobial identification techniques relied on culturing and iso-
lation of microbial cells from a natural sample and then
characterization of microbial isolates via a series of biochem-
ical tests. This approach gives very biased population data
because, although a large fraction of the visible cells are viable,
only 0.01-10% of microorganisms are culturable by using
current methods. Although these techniques yield some infor-
mation on microbial populations and diversity, all information
on the spatial distribution of organisms is lost. Recent break-
throughs in molecular biological approaches have provided
powerful approaches to study the distribution and diversity of
microbial cells in situ (71, 72, 73~.
The basis of the molecular approach to microbial population
analysis is to extract, amplify, purify, and sequence DNA,
typically the ribosomal DNA, from a natural microbial popu-
lation and then to identify individual organisms by comparison
between the obtained sequences and sequences from known
organisms. Regardless of whether an organism has been
identified previously, differences between its sequence and
those of known organisms can be used to place the species onto
a phylogenetic tree (71-73~. Once the sequence has been
obtained, a DNA-specific, fluorescently labeled probe can be
used to identify individual cells in environmental samples or in
laboratory cultures (25-27, 71, 73, 74~. These probes are
designed so that they will bind only to ribosomal RNA of
organisms with complementary sequence (71, 73~. Under
appropriate experimental conditions, the degree of probe
specificity (e.g., binds to all bacteria versus binds to Thioba-
cillus caldus) is determined by choice of probe sequence (e.g.,
an oligonucleotide common to all bacteria versus one common
to only the target species). Microscopic visualization using
multiple probes allows direct in situ characterization of the
microbial population at the species (or higher) level.
Combined DNA sequencing and probing has been used
successfully in a number of natural environments (25-27, 73
74~. In some cases, it has been possible to quantify the
proportions of bacteria, archaea, and eukaryotes and to cor-
relate abundances with geochemical conditions. This has pro-
vided new insights into interconnections between physical,
chemical, and biological components of natural systems.
Analysis of DNA from environmental samples and charac-
terization of environmental samples using probes constructed
with DNA sequences of interest are powerful new approaches
for geochemical studies. These tools have not yet been de-
ployed widely but should allow future researchers to evaluate
interrelationships between microbial ecology and geochemical
and physical parameters (25~. Ultimately, these data can be
correlated with metabolic information to infer how and why
microbes interact with mineral surfaces in natural environ-
ments.
DNA has been extracted and sequenced from several hun-
dred soil microorganisms (16-21, 70~. Most of the sequences
were from bacteria, but many did not correspond to any of the
known species. Several could not be classified into any of the
larger known bacteria groups. Recently, archaea have been
consistently reported from the rhizosphere. The distribution
and importance of these organisms remain unclear.
Experimental Quantification of Processes Occurring in
Lichen Zones: Insights for Rhizosphere Processes. Plant roots
excrete a combination of sugars, organic acids, and amino
acids. It is believed that plant roots exude carbohydrates to
encourage and sustain the associated microbial community.
This large-scale carbon transfer from photosynthesizes to a
nonphotosynthetic microbial community is analogous to Zone
1 in Barker and Banfield's (53) microbial weathering model
(Fig. 5~.
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3408 Colloquium Paper: Banfield et al.
FIG. 7. Secondary phosphate minerals formed on the surface of
apatite during the early stages of weathering. These insoluble phases
bind P in a relatively nonbioavailable form.
The plant-microbe symbiosis is not the only similarity
between the rhizosphere and lichen communities. Within soils,
some microorganisms live in solution, but most are attached to
mineral surfaces where they can directly affect mineral reac-
tions (75, 76~. Attached cells, largely fungi and bacteria, may
impact mineral dissolution, precipitation, and clay hydration
reactions in a manner analogous to that seen in Zone 2, at the
lichen-mineral interface (Fig. 5~.
Physical restrictions placed on microbial distribution by pore
size also apply to rhizosphere environments. Consequently,
Zone 3 (Fig. 5) reactions are expected in soils as well. Although
only the outer surface of a given mineral grain may be
colonized, interior surfaces may show enhanced dissolution
because of organic acids of plant and microbial origin. Ele-
vated carbonic acid levels may result from fungal and bacterial
degradation of organic matter (77, 78~. Several to several
hundred micromolar concentrations of oxalate, acetate, lac-
tate, formate, pyruvate, propionate, malate, succinate, citrate,
isocitrate, and aconitate have been detected in rhizosphere soil
(79-81~.
The fertility of numerous soils is limited by the abundance
of bioavailable phosphate. In incipiently weathered rocks,
microbial growth also may be phosphorus-limited because the
abundance of organophosphates is low. Phosphorus limitation
can develop during weathering because of either phosphorus
adsorption onto secondary iron oxyhydroxide surfaces or
binding of phosphorus into insoluble secondary minerals.
During the initial stages of weathering, apatite is replaced by
chemically or microbially precipitated secondary phosphate
minerals containing iron (strengite), aluminum (variscite), and
lanthanides (e.g., rhabdophane and florencite; Fig. 7~. Sec-
ondary lanthanide phosphates persist until at least one-third of
the initial mineral constituents are removed by dissolution
(82~. These phosphates are completely solubilized in the soil
zone (83~. DNA staining, in combination with high-resolution
FIG. 8. Microorganisms colonize surfaces of secondary minerals in
pits formed by apatite dissolution. Microbial processes mobilize phos-
phorus from insoluble secondary phases.
Proc. Natl. Acad. Sci. USA 96 (1999J
12_
n~(Den) ~
~1
3~ ~/1
,.
' lime (Da~) 28
FIG. 9. (Left) Fe released from biotite to solution in three exper-
iments, two of which used bacterial cultures (B0428 and B0665) and
one that was a control experiment. Significant enhancement of biotite
dissolution rate is observed. (Right) Results of a feldspar dissolution
experiment (pH 4.0) using undifferentiated and medium molecular
weight polysaccharides demonstrate enhanced feldspar dissolution by
two to three orders of magnitude under some conditions.
scanning electron microscope observations and unpublished
experimental data, suggest that solubilization of secondary
phosphates results from microbial colonization (Fig. 8~. Mi-
crobes apparently respond to phosphate limitation by locating
themselves at sites of inorganic phosphorus release or by
excretion of organic acids or other complexing compounds to
actively dissolve the otherwise insoluble secondary phosphate
minerals (5, 43, 84~. Further work is needed to determine
which organic compounds are important. The effectiveness of
likely compounds should be tested experimentally. Analysis of
organic constituents in phosphorus-stressed cultures could be
used to verify the microbial response. Identification of the
mechanisms involved and microorganisms responsible for
release of phosphorus from resistant secondary phosphates
may provide new strategies for enhancement of productivity of
low fertility soils (e.g., how to enhance the effectiveness of
phosphate fertilizers and to manage soil fertility through
manipulation of microbial populations).
Dissolution of inorganic phosphates may localize microbial
activity and stimulate weathering of adjacent minerals. For
example, it has been shown (85) that microbially mediated
feldspar dissolution rates increase when feldspars contain
apatite inclusions. Because feldspar dissolution rates are
strongly pH-dependent, it is probable that the results can be
attributed to release of acidic microbial byproducts.
Mineral dissolution studies with cultures of bacteria and
fungi show a dramatic increase in dissolution rates of feldspar,
biotite (Fig. 9a), quartz, apatite, and other minerals (54,
86-93~. In experiments with bacteria, mica, and feldspar, there
is a direct correlation between microbial organic ligand pro-
duction and increased release of Si, A1, and Fe (88-90~.
Although these experiments replicate natural systems to some
extent, they are inherently complex because of the combina-
tion of acidity effects, ion-complexing effects, and growth
media effects. Thus, it is difficult to distinguish the contrib-
uting factors.
Lichen-mineral interface characterization studies suggest
that microbial colonization can dramatically impact both the
rates and the mechanisms of silicate mineral weathering
reactions via direct and indirect processes. To compare the
effectiveness of organic-mineral interactions that depend on
contact between microbes and mineral surfaces with those
interactions that only involve soluble compounds, it is neces-
sary to develop appropriately simplified experimental models.
Acid production is the most basic mechanism by which
microbes affect weathering reactions. We infer that this is
largely responsible for enhanced reactivity in Zone 3 (Fig. 5~.
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Colloquium Paper: Banfield et al.
Solutions of organic acids in concentrations comparable to or
slightly higher than ground water show increase in dissolution
rates of less than one order of magnitude (56, 57~. These
relatively small effects may hide much larger responses in
natural systems in which local microenvironments may be
characterized by very high acid concentrations because of cell
proximity.
It is possible to demonstrate directly that microbes can cause
low pH microenvironments at mineral surfaces. The pH values
can be measured by using microelectrodes (94) or, in even
smaller volumes, by using confocal-based techniques. For
example, pH values of 3-4 were detected in proximity to
bacterial cells within cleavages in biotite when the bulk solu-
tion pH was 7.0 (88~. As acidity increases, below pH = 5, the
rates of silicate mineral dissolution increase by a factor of aH+
(95~. Lowering pH to 3-4 corresponds to a 10- to 1,000-fold
increase in dissolution rate. The mechanism of the reaction
changes as well. Typically, elements such as Fe and Al are
relatively insoluble at neutral pH and form secondary Fe-
hydroxides and vermiculite or smectite-like silicate clays.
However, as acidity increases, Fe and Al solubility and mobility
increase, probably leading to formation of different secondary
minerals, such as the aluminosilicates kaolinite and halloysite.
In addition to inorganic acid production, microbes also can
catalyze mineral weathering rates by production of organic
ligands. Ligands can complex with ions on the mineral surface
and can weaken metal-oxygen bonds. Alternatively, ligands
indirectly affect reactions by forming complexes with ions in
solution, thereby decreasing solution saturation state. Exper-
imental studies using relatively dilute solutions of compounds
such as oxalic acid, citric acid, pyruvate, a-ketoglutarate,
acetate, propionate, lactate, etc. have shown rate enhance-
ments for silicate dissolution of up to one order of magnitude
(96-101~. The effect is somewhat similar to that of acid
production because organic ligands affect silicate mineral
dissolution stoichiometry by complexing with, and increasing
the solubility of, less soluble major ions such as Al and Fe (96,
102, 103~.
The transformation of biotite to vermiculite with the release
of the interlayer K is perhaps one of the most important
biologically mediated geochemical reactions occurring in the
rhizosphere (104-106~. Uptake of K+ by microbial cells and
plant roots lowers solution saturation state, thereby indirectly
promoting the weathering. However, plants and associated
ectomycorrhizal populations have more aggressive methods
for weathering sheet silicates. The extensive transformation of
biotite to vermiculite has been attributed to root-induced pH
decreases in the rhizosphere and acid dissolution of the mica
structure (1044. In a similar experimental study (93), plant
roots and ectomycorrhizal fungi actively produced oxalate and
increased biotite weathering when they were stressed for K and
Mg. Plant roots and associated microbial populations also
physically disrupt sheet silicates, exposing new surface area for
chemical alteration (107).
It has been shown that microorganisms produce intermedi-
ate molecular weight organic compounds that are important in
iron transport to the cell surface (36, 37~. Under conditions of
Fe limitation, microbes produce siderophores that have a very
high affinity for Fe+3. Siderophores form very strong stable
bidentate complexes with octahedrally coordinated Fe+3 as
well as with other major elements in minerals, e.g., Al and Si.
Several hundred siderophores from microbial cultures and
natural environments have been isolated and identified, most
of which have either hydroxamate or catecholate functional
groups. Estimates of siderophore concentrations in soil mi-
croenvironments range from 10 to 2,000 mg/liter (38, 39~.
Mineral weathering experiments with naturally occurring sid-
erophores show that these compounds can accelerate the rate
of Fe-oxide and silicate mineral dissolution by about one order
Proc. Natl. Acad. Sci. USA 96 (1999 J 3409
of magnitude and thereby dramatically impact Fe cycling in
soils (35, 38, 39, 41).
In addition to producing acids and low and intermediate
molecular weight organic ligands, microbes also produce high
molecular weight polymers. Observations of naturally weath-
ered minerals associated with lichens show that, in the direct
zone, these polymers coat surfaces. Polymers can affect min-
eral weathering reactions by several processes (52, 53~. Slime
layers are ~99% water, so they can increase the contact time
between water and the mineral surface. Polymers also increase
the diffusion of ions away from the mineral surface. However,
these extracellular polymers may have more direct chemical
effects on mineral weathering as well.
The effect of high molecular weight organic molecules on
mineral dissolution rates was quantified by using dissolution
experiments involving model extracellular polymers. The
model polysaccharides (alginates) varied in the ratio of con-
stituent mannuronic and guluronic acids. Mannuronic and
guluronic acids differ in their effect because of different
concentrations and orientations of carboxylic acids functional
groups. Like low molecular weight organic acids, polysaccha-
rides can increase the extent of mineral weathering (Fig. 9b),
presumably by complexing with ions in solution, thereby
lowering solution saturation state (51, 108~.
Microbially induced metal binding and mineralization is
important in the rhizosphere as well as at the lichen-mineral
interface. Cell surfaces and associated polymers provide ef-
fective nucleation sites for secondary silicate mineral precip-
itation. Some rocks contain high abundances of minerals
enriched in potentially toxic elements (e.g., As, Cd, Cu, U).
Microorganisms react to high metal concentrations in a variety
of ways. One biochemical response to toxic substances is
production of extracellular polymers that bind and effectively
immobilize the compound and, in some cases, biomineraliza-
tion. For example, microbes immobilize U by intra- and
extracellular precipitation of secondary minerals (109, 110~.
Alternatively, some microbes exposed to arsenic employ mo-
bile genetic structures (plasmids) to manufacture proteins that
(although counterintuitive) reduce the less toxic Ass+ to more
toxic As3+ and secrete it from their cells (111~. In other cases,
microbes can completely volatilize the toxic element (e.g., by
formation of methyl-mercury compounds) (111~. Thus, micro-
bial responses to toxic metals can dramatically change metal
abundances and elemental speciation.
Applications of Microbe-Mineral Interaction Studies for the
21st Century. Among the many challenges for the 21st century
are questions concerning how (i) to maintain agricultural soil
fertility to ensure food production for a still-growing world
population; (zi) to prevent further environmental damage; and
(iii) to invent cost-effective ways to remediate existing con-
tamination of soil, sediments, and water. Improved knowledge
of how microorganisms interact with their environments and
contribute to geochemical transformations will be critical to
these endeavors.
We have established above that microbes are important
agents of physical and chemical change in natural systems. In
fact, global-scale models verify that chemical weathering re-
actions directly impact climate. It is widely accepted that, early
in Earth's history, the atmosphere was dominated by CO2 and
that oxygen concentrations only increased with the evolution
of efficient photosynthetic microbial populations. Early inor-
ganic rock weathering resulted in accumulation of Ca and Mg
in ocean waters, leading to precipitation of Ca, Mg-carbonates
and draw down of CO2. The rates of chemical weathering of
Ca-silicates, Mg-silicates, and Ca, Mg-silicates determine the
rate of supply of Ca and Mg to oceans and thus affect the
magnitude of this critical feedback mechanism (112-116).
Mineral dissolution rates are important inputs into global
climate models (112-115~. However, the impact of microbial
processes on weathering reactions over geological time are
OCR for page 3410
3410 Colloquium Paper: Banfield et al.
unclear, and the relevant rates remain in dispute. If microor-
ganisms significantly affect mineral dissolution rates, then the
evolution of the biosphere (dominated by microorganisms for
the majority of time), atmosphere, hydrosphere, and litho-
sphere have been closely coupled (117~. Much can be learned
about the long term response of the Earth system through
quantifying the microbial-mineralogical feedback mecha-
nisms. Thus, a challenge for the next century will be to develop
more rigorous and comprehensive models for climate change.
Climate change implies altered patterns of rainfall and
temperature and thus, modification of the processes occurring
in surficial materials, including soils. Prediction of the conse-
quence of climate change requires a rather comprehensive
understanding of the interrelationships between mineralogy,
soil chemistry, microbial populations, rainfall, and tempera-
ture. Such understanding will benefit from investigations of
soil-forming mineral reactions occurring under diverse cli-
matic and hydrological conditions. Analyses must include
detailed characterization of primary minerals and their weath-
ering products, a census of microorganisms and determination
of their patterns of distribution, and contextural information
about soil physics and chemistry.
It should be possible to increase the rates of soil develop-
ment and optimize methods used to maintain or increase soil
fertility through knowledge about microbial populations and
how microbes cooperate to affect mineral dissolution, degra-
dation of organic compounds, immobilization of ions, precip-
itation of minerals, and change in solution chemistry. For
example, identification of microbial species capable of solubi-
lizing secondary phosphates may provide new insights for
improved fertilizer efficiency (e.g., simultaneous addition of
microorganisms or microbial compounds with phosphate fer-
tilizers).
Understanding of microbial metal tolerance and of metal
resistance strategies should lead to new approaches to envi-
ronmental cleanup. Understanding how microbes affect the
fate of contaminants in the natural environment will be critical
for waste treatment and site remediation. An example of
current regulatory interest is the long term, near-site contain-
ment of nuclides released from geological repositories. Chal-
lenges such as this demand sophisticated models that include
all factors, inorganic and biological. Interdisciplinary study of
microbe-mineral-solution interactions are required for model
development.
As we learn about the remaining 99-99.9% of organisms we
currently know essentially nothing about, new species with new
capabilities will be discovered. These may be vitally important
sources of new compounds of tremendous technological im-
portance. The discovery of hyperthermophilic microorganisms
by Thomas Brock (University of Wisconsin, Madison, WI) (26)
led to the identification of a thermally stable enzyme, taq
polymerase, which has revolutionized the PCR step of DNA
analysis. It is difficult to predict what the future will hold, but
the discovery of enzymes capable of carrying out redox
reactions at silicate and oxide mineral surfaces as well as in
solutions may be of some importance for enhancement of soil
fertility, economic metal extraction, and materials science.
The global-scale balance between inorganic and microbial
process is unclear, and the quantitative effects of microbes on
geochemical cycles are essentially a mystery. At present, we are
identifying specific processes that may be important and are
quantifying them via laboratory studies. Ecological aspects of
microbially dominated systems, including the symbioses and
competition, largely remain a challenge for the future. New
understanding of Earth's surface processes should come from
detailed and quantitative studies that utilize current molecular
biological and biochemical approaches in concert with high-
resolution mineralogical and geochemical analyses.
Proc. Natl. Acad. Sci. USA 96 (1999)
The authors acknowledge the editorial assistance of Dr. J. V. Smith
(University of Chicago) and thank Dr. R. A. Eggleton (Australian
National University), K. Edwards (University of Wisconsin, Madison,
WI), T. Gihring (University of Wisconsin, Madison, WI), and Dr. P.
Bond (University of Wisconsin, Madison, WI) for their contributions
to this work. This research was supported by Grants EAR-9317082 and
EAR-9706382 from the National Science Foundation and Grant
DE-FG02-93ER14328 from the Department of Energy.
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Representative terms from entire chapter:
mineral surfaces
