Download Mineral formation by bacteria in natural microbial communities

FEMS Microbiology Ecology 26 (1998) 79^88
MiniReview
Mineral formation by bacteria in natural microbial communities
Susanne Douglas *, Terry J. Beveridge
Department of Microbiology, University of Guelph, Guelph, Ont. N1G 2W1, Canada
Received 6 October 1997; revised 18 March 1998; accepted 21 March 1998
Abstract
This review focuses on bacteria and their role in mineral formation. As a consequence of their small size and diverse
metabolic capabilities bacteria, more than any other type of living organism, are able to interact intimately with metal ions
present in their environment. Some metals are required for metabolism and are taken into the cell through various mechanisms,
then incorporated into the necessary physiological pathways and biosynthetic structures. This physiological aspect of metalbacterial interaction will not be discussed but, rather, the ability of bacteria to accumulate metal ions and incorporate them into
mineral phases will be described. This activity has widespread importance for the shaping of our planet and the recycling of
mineral elements. Since bacteria are most frequently found as part of microbial communities it is within this context that their
mineral-forming ability will be discussed. z 1998 Published by Elsevier Science B.V. All rights reserved.
Keywords : Bacteria; Microbial ecology; Mineral formation
1. Mineral formation on bacterial cells
In almost any environmental sample, examination
of the cells by electron microscopy reveals mineral
precipitates closely associated with bacterial cells
(Fig. 1). There are several characteristics which bacteria exhibit that make them ideal nucleating agents
for mineral precipitation. Bacterial cells are very
small, especially in low-nutrient environments. Typically, a single rod-shaped bacterium will have a diameter of approximately 0.5 Wm and a length of 1
Wm [1]. Due to their small size, bacteria as a group
have the highest surface area-to-volume ratio of any
group of living organisms and this, together with the
presence of charged chemical groups on their cell
* Corresponding author. Tel.: +1 (519) 824-4120 ext. 3813;
Fax: +1 (519) 837-1802; E-mail: [email protected]
surface, is responsible for the potent mineral-nucleating ability of these cells. Eubacterial cell walls come
in two main formats, Gram-positive or Gram-negative [1]. Either type may be overlain by a number of
other surface structures. These may be proteinaceous
in nature (e.g., S-layers) or composed primarily of
carbohydrate polymers (e.g., capsules) and may occur singly or in combination; a more detailed description of these structures can be found in [1]
and [2]. Whatever types of cell surface structure the
cell may have, the main charged chemical constituents found in these structures at neutral pH are carboxyl, phosphoryl, and amino groups. In general,
negatively charged groups dominate over positively
charged ones, giving the cell surface an overall
anionic charge [1].
Initiation of mineral formation on bacterial surfaces has been proposed to follow a generalised pattern
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PII: S 0 1 6 8 - 6 4 9 6 ( 9 8 ) 0 0 0 2 7 - 0
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which can be thought of as occurring in two steps
[3]. In the ¢rst step, metal ions present in the aqueous surroundings of the cell interact with charged
groups in the surface structures. The interaction is
stoichiometric such that there is an electrostatic
charge complementation between the charged groups
in cellular polymers and the metal ions. Subsequently, the presence of bound metal ions in the
wall fabric lowers the total free energy of the system,
thereby initiating further metal deposition. In this
case, precipitates form at the nucleation site between
metal ions and excess counter ions from the £uid
phase; the wall binds more metal than would have
been expected based solely upon charge interactions
with wall polymers. Thus, metal aggregates are
formed within the wall matrix, their size constrained
by the physical presence of the polymer meshwork
itself. Depending on microenvironmental geochemistry, negatively charged counterions (e.g., sulfate,
phosphate, carbonate, sul¢de, or silicate ions) determine speci¢c mineral phases [4]. Mineral formation
on the bacteria is generally not controlled by the
organism; it happens because of the physicochemistry of the bacterial surface and the chemistry of the
cell's environment. Actively metabolising bacteria
with highly energised plasma membranes can inhibit
mineral formation since the cell wall is £ooded with
protons which compete with metal cations [5].
The following sections will describe several di¡erent types of environments in which bacterially mediated mineral formation has been suggested to play a
major role in formative geological processes. These
by no means represent an exhaustive survey of the
many descriptions of in situ bacterial mineral formation but are meant to serve as representative examples of the types of minerals that have most often
been found in association with bacterial cells.
2. Microbial ecology of sul¢dic mine tailings
An example of an environment in which the links
between geochemistry, microbial physiology, and
mineralogy can be seen is in sul¢dic mine tailings.
These interactions have recently been documented in
detailed reports of geomicrobiological studies of
abandoned and active mine tailings dumps in northern Ontario [6^9]. The exploitation of base metal
(Cu, Zn, Fe, Ni, etc.) ore deposits has led to extensive environmental contamination in the areas surrounding and including the tailings dumps from such
mines. In general, pyrites (metal sul¢de minerals) are
the most common form mined for metal extraction.
After extraction the ¢nely ground waste rock is
mixed with water and deposited as a slurry (tailings)
in large impoundments, often nearby lakes. The tailings still contain a signi¢cant amount of sul¢dic minerals which, together with Fe (and to a lesser extent
other metals), represent an oxidisable energy source
for a large group of bacteria collectively termed acidophilic lithotrophs [7]. This group is exempli¢ed by
the thiobacilli, a group of Gram-negative rod-shaped
bacteria which are autotrophic and can oxidise both
ferrous Fe and sul¢de to produce ferric iron and
sulfuric acid, often with pHs as low as 1^2 [10].
Abiotic acidi¢cation can also occur but is a much
slower process than the bacterially mediated one
[8]. This `acid mine drainage' can enter groundwater,
nearby rivers, and lakes. Many abandoned mine tailings dumps exist and represent an enormous environmental and economic problem. An understanding
of the microbiology of these environments is the key
to developing long-term, ideally self-sustaining bioremediation tactics.
Detailed studies [7,8] have unravelled some of the
relationships among the major groups of microorganisms present in tailings from sul¢dic base metal
mines. Samples were taken at 5-cm intervals with
depth (down a vertical tailings pro¢le) to learn about
the geomicrobiological inter-relationships that existed in this environment. The samples consisted of
sediment with little free water and were analysed for
bacterial numbers, mineralogy (both bulk and cellassociated), dissolved metals and sulfate, and pH.
Two groups of bacteria, the thiobacilli and the sulfate-reducing bacteria (SRB), were enumerated by
the most probable number method (MPN) and examined for their ability to a¡ect porewater geochemistry and precipitate mineral phases. Even though
most tailings are pyritic, no previous studies had included investigations of SRB activity since these bacteria require anaerobic, neutral to alkaline environments and were not thought to be signi¢cantly
represented in oxic, metal-rich, acidic tailings.
A dynamic relationship exists between the thiobacilli and the SRB [7,8]. In the tailings, a colour
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change from orange to grey with depth roughly corresponded to a change from oxic to anoxic conditions. Even in the orange oxic zone, where thiobacilli
¢x inorganic carbon and oxidise Fe and sul¢de from
the waste rock, signi¢cant numbers of SRB were
found. The peak numbers of thiobacilli correlated
well with maximum sulfate and soluble iron in the
tailings, as well as with the region of lowest pH [8].
As the leachate percolates through the tailings some
bu¡ering occurs through interaction with carbonate
minerals, and free metal concentrations in the pore
water may be reduced by precipitation into minerals.
This process is enhanced by the presence of bacterial
cells, which provide nucleation sites for their deposition. As the tailings become anoxic with depth, generally due to saturation by groundwater, SRB numbers begin to increase [8]. These organisms, in an
energy-yielding anaerobic respiratory process, reduce
sulfate to sul¢de which is released from the cell [11].
Sul¢de reacts strongly with metal ions, resulting in
the formation of sul¢de precipitates both on the SRB
cell surface and throughout the immediate surroundings [9].
Although it is probable that autotrophic SRB exist, these bacteria are generally considered to require
organic molecules (usually simple organic acids) as
carbon sources and electron donors for sulfate reduction [11]. The main source of organic nutrients
in the tailings is that contained in rainfall and derived from the degradation of microbial cells. Thus,
thiobacilli and other bacteria in the oxic zone represent an important source of organic carbon in this
environment [7,8]. SRB can be found in lower numbers in the oxic zone they must survive within anaerobic, circumneutral pH microenvironments, likely
maintained through bicarbonate production.
Several types of secondary minerals have been
found associated with bacterial cells in tailings and
it is believed that these would not have formed without the presence of the bacteria [6]. As in other environments, the cells provide nucleation sites for
mineral development and also a¡ect microenvironmental chemistry such that particular (and otherwise
unexpected) mineral types form. In the oxic zone, the
predominant mineral type associated with thiobacilli
was Fe-oxides [8], while on and near the SRB cells in
the oxygen-depleted zone Fe monosul¢des were
formed [9]. The large amount of Fe and sulfate re-
81
leased by the microbial activity in the oxic zone also
led to the precipitation of melanterite (FeSO4 W7H2 O),
a mineral form observed throughout the tailings pro¢le and not associated with cell surfaces [8]. In other
tailings environments [6] the metal content of re-precipitated minerals re£ected the original heavy metal
content of the tailings. However, the mineral form
was unlike that of unaltered tailings; it included minerals containing phosphorus presumably derived
from the accompanying bacterial cells. These studies
serve to highlight the profound e¡ect bacteria can
have on the geochemical processes occurring in a
tailings environment.
3. Silicate formation by bacterial cells
In many diverse environments, including river
sediments [12,13], mine tailings [8], hot springs
[14,15], and surface sul¢de springs (Douglas, unpublished observation), silicate minerals, often of a claylike composition and structure, are found in intimate
association with bacteria (see Fig. 1). It is quite likely
that the bacteria were instrumental in their formation, rather than simply binding pre-formed detrital
minerals, since the composition of silicates clearly
not associated with bacterial cells often di¡ers markedly from those found on the cell. In addition, these
precipitates are more crystalline and larger in structure than those found on bacterial cell surfaces. Even
in environments with low dissolved silica concentrations, such as freshwater lakes and rivers, clay-like
precipitates are found on bacterial cells. The metal
content of the clays is usually re£ective of the metals
present in the surrounding water [12].
In some cases, exempli¢ed by microbial communities in silica hot springs, `pure' silica (i.e., with no
associated metal ions) is found to form around bacterial cells, eventually encasing them in an amorphous silica matrix; a process that may be analogous
to that which led to the preservation of bacteria as
microfossils in the geological record [16,17]. In a
study of hot spring microbial mats in Iceland, it
was found that, with depth in the mat, bacterial cells
became progressively more mineralised so that eventually all that remained was the bacterial surface
layers encased in amorphous silica [14]. Even though
hot spring waters are supersaturated with respect to
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Fig. 1. Stained ultrathin section of bacterial cells from a microbial mat community in a saline alkaline lake in British Columbia, Canada.
Bacterial cells are surrounded by abundant mineral precipitates which appear as thin, dark deposits on and around the cells. In this case
the mineral was an Fe, Mg silicate, resembling sepiolite. Bar = 250 nm.
silica, silicate minerals will not precipitate unless a
nucleation surface, such as that presented by a bacterial cell, is present [18].
Laboratory simulations of microfossil formation
have indicated that cells exposed to heavy metal
ions such as Fe before being subjected to high silica
concentrations with or without raised temperatures
(60³C) for extended periods of time were better preserved and remained as recognisable cells [16]. It was
concluded that pre-treatment of cells with Fe inhibited the activity of autolytic enzymes, thus preventing degradation of cellular structures prior to their
preservation [16,18]. In the light of these results, it is
remarkable that recognisable sheath structures remained in the Iceland silica matrix. No Fe or other
metal ions were detected in these silicates, indicating
that, if present, the metal concentration was below
the detection limits of the energy-dispersive X-ray
spectrometer used in the analysis of the precipitates
(i.e., 6 1% by weight). At another site in Iceland, Fe
silicates were found as the cell-enclosing matrix and
it was suggested that, due to the presence of Fe, it is
plausible that these cells may eventually be preserved
in the geological record as microfossils [15].
Recently, it has been shown that bacterial surfaces
are also good sorption interfaces for silicate ions
directly. Although the cell surface has a net electronegative charge, some positive amine groups are
present within the wall matrix. At near-neutral pH,
these represent sites for interaction with silicate
anions yet, there are not enough available amine
groups to account for the large amount of silicate
which is eventually bound. Additional silicate binding occurs as a result of crossbridging involving metal ions which link Si anions to carboxyl or phosphoryl groups within the wall matrix [19]. Thus,
negatively charged polymeric groups can also be involved in silicate deposition. Binding of silicate
anions leads to the deposition of poorly ordered silicate mineral phases in association with the bacterial
cell surface. These eventually become crystalline and
speci¢c clay phases can be formed. As these silicate
minerals develop they also act as sorption interfaces
for metal ions, increasing the overall metal binding
ability of the bacteria [20,21]. However, the bacterial
cell wall appears to have a greater a¤nity for metal
ions than the clay phases and, on a per weight basis,
has a higher metal binding capacity [22^24].
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83
Fig. 2. Stained thin section of a Synechococcus GL24 cell. This cell has been prepared using a quick-freeezing technique (freeze substitution) in order to preserve its structural integrity. This micrograph shows one pole of the cell at which the surface layers are clearly visible.
S: S-layer; P: peptidoglycan ; C : cytoplasmic membrane. Note the regular structure of the S-layer and its close association with the outer
membrane. The large hole in the cell is the former location of a polyphosphate inclusion which was lost during processing for elelctron
microscopy. Bar = 100 nm.
4. Mineral formation in microbial mats or bio¢lms
Carbonaceous
organosedimentary
structures
known collectively as microbialites provide the best
studied examples of mineralised microbial communities. Such structures have been preserved in the geological record, providing information of past geomicrobiological activity and environmental conditions.
Extant microbialites are presently still forming in
certain environments, usually warm shallow marine
waters which provide adequate light and shelter from
disruptive physical forces and protection from grazing invertebrates (e.g., molluscs).
The formative processes responsible for the presence of microbialites have been under debate for
some time but a consensus appears to be forming
that microorganisms (particularly bacteria and cyanobacteria) are necessary for their deposition [24,25].
These structures basically consist of a microbial community, made up of a dominant type of oxygenic
phototroph and associated microorganisms which
have ¢ne-grained carbonate precipitates (usually calcite or aragonite) associated with them. The formation of these minerals may be promoted by physio-
logically induced alkalisation of the microenvironment around the cyanobacterial cells or
may be due to abiotic geochemical factors such as
evaporation from the calcite-supersaturated aqueous
environment within which these structures are usually found [24,26]. It is probably a combination of
both, with each type predominating at particular
times, depending on seasonal environmental variations. Whatever the mechanism of CaCO3 formation
may be, it is clear that the presence of bacterial cells
is necessary for mineralisation. Again, the bacteria
provide nucleation sites for mineral deposition. It
has also been suggested that the often extensive gelatinous sheaths of many unicellular and ¢lamentous
cyanobacteria are important for trapping of abiotically formed precipitates [27,28].
Microbialites are generally classi¢ed as one of two
major structural types as described by Kennard and
James [29]. Stromatolites have a laminated structure
in cross section, with light-coloured carbonate-rich
bands alternating with darker organic-dominated
layers on scales of millimetres. Over time, cementation processes result in a hardening of the layers
which are no longer actively forming [30]. In general,
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Fig. 3. Negatively stained whole mount of S-layer from Synechococcus GL24. The S-layer has been shed by the cell in large fragments.The
hexagonal arrangement of the constituent protein molecules making up this paracystalline structure can be clearly seen. Bar = 100 nm.
the structure of stromatolitic microbialites arises
from the presence of ¢lamentous cyanobacteria (as
opposed to unicellular forms) as the main structuredetermining factor of the mat [29]. The second structural type is commonly referred to as a thrombolitic
microbialite and has an open clotted texture which
appears to be made up of many small globular structures cemented together. Thrombolites appear to be
formed due to the presence of unicellular cyanobacteria as the main structural entity [24].
Di¡erent forms of carbonaceous microbialites
have been found in widespread and often fascinating
environments. The largest known calcareous microbialites were formed in the late Precambrian. However, extremely large, presently forming microbialites
were recently discovered in Lake Van, Turkey [31].
This is a large, deep alkaline (pH s 9.7) lake with
microbialitic tower-like structures growing up to 40
m high to depths of 100 m in a dense population of
structures. The columns are covered in a dark green
to black microbial mat comprised of coccoid cyano-
bacteria as the major phototroph with the formation
of aragonite occurring within their sheaths. The columns are porous, with Ca-rich groundwater percolating up through them so that, at the ends of pinnacles where the ground water exits the column
structure, abiotic calcite is deposited. It is not known
why the di¡erence in mineral phases between biogenic and abiotic calcium carbonate exists. However, the
authors speculated [31] that somehow the organic
matrix provided by the cyanobacteria directs the formation of aragonite rather than calcite.
Stromatolite-like structures have also been found
in rather unlikely environments such as caves, where
laminated structures (`speleotherms') are being deposited by a cyanobacterially dominated microbial
community [26]. Stromatolite-like structures have
even been found in deserts where coccoid cyanobacteria belonging to the pleurocapsa group are responsible for formation of `crusts' consisting of calci¢ed
laminated layers over desert soils in California (Borrego Desert) and the Sinai desert in Israel [32].
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85
Fig. 4. Unstained whole mount of S-layer fragments from Synechococcus GL24 cells grown in Fayetteville Green Lake water. Although
the sample was not stained, the S-layer pattern is clearly visible due to the precipitation of gypsum within the holes of the array.
Bar = 100 nm.
5. Possible mechanisms for carbonate formation
A general mechanism for carbonate mineral deposition by bacteria involves the ability of the cells to
produce an alkaline microenvironment as a result of
their physiological activity. Organisms capable of
doing this include SRB, which release bicarbonate
[33], nitrate reducers (releasing ammonium ions),
and urea-degrading bacteria (also release ammonium
ions [34]). By far the most prevalent reaction is that
of oxygenic photosynthetic microorganisms, principally cyanobacteria, which release hydroxyl ions as
a result of using bicarbonate ions as a carbon source
in the aqueous neutral to alkaline environments they
inhabit [35].
5.1. Fayetteville Green Lake
The detailed mechanism of carbonate deposition
on a cyanobacterial cell was outlined for Synechococcus GL24 (Fig. 2), a unicellular cyanobacterium iso-
lated from Fayetteville Green Lake, New York [36].
In the lake, Synechococcus cells represent the dominant phytoplankton due to the highly oligotrophic
nature of this small, but deep (55 m), meromictic
lake [30]. The lake water has high levels of Ca (10
mM), SO23
4 (11 mM) and carbonate (V10 mM) ions
in its hypolimnion [37]. Synechococcus lives as a
planktonic population, the numbers of which follow
a seasonal progression with a maximum of 107 cells
ml31 in summer to 104 cells ml31 under ice cover in
winter [38]. They also exist as a benthic population
where they are the main formative agent of a thrombolitic bioherm on the steep sides of the lake basin
and on almost every solid surface (sticks, rocks, etc.)
within the photic zone. The bioherm is formed by
similar processes as described for mineralisation in
the water column but, since these cells are growing
as bio¢lms on the lake shore, their calci¢cation and
eventual entombment leads to an outbuilding of the
bioherm structure [30].
Each Synechococcus cell is surrounded by a para-
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S. Douglas, T.J. Beveridge / FEMS Microbiology Ecology 26 (1998) 79^88
crystalline surface array as its outermost, de¢ning
layer [36] (Fig. 3). These are structures made of
many identical protein molecules which self-assemble
on the bacterial surface to form a structure that
completely encloses the bacterium and that, when
viewed by electron microscopy, has a regularly symmetrical pattern to it. The S-layer of Synechococcus
GL24 is hexagonally symmetrical with diamondshaped pores 11U22 nm. The S-layer plays an important role in the ability of this cyanobacterium to
precipitate gypsum (CaSO4 WnH2 O) and calcite
(CaCO3 ) from the lake water (Fig. 4).
The S-layer is more hydrophobic than most bacterial surfaces but negatively charged sites which can
bind Ca2‡ are present in the pores [39]. Once Ca is
bound, it complexes SO23
4 ions when microenvironmental pH is not much higher than that of bulk lake
water (pH 7.9), or CO23
3 , when bicarbonate metabolism pushes the microenvironmental pH above 8.3.
For the latter, HCO3
3 is taken into the cell and converted by carbonic anhydrase to CO2 and OH3 [40].
The CO2 is incorporated into cell biomass while
OH3 ions are released into the cell's microenvironment [41] and concentrated around the cell. As a
consequence, the microenvironmental pH around a
Synechococcus cell can become highly alkaline when
the cells are active. When they are grown to high
densities (106 cells ml31 ) in test tubes containing natural lake water (total volume 10 ml) the pH can
increase to 10.5 within 48 h [42]. In Fayetteville
Green Lake, as the lake water warms in midsummer, it takes on a milky appearance due to the
presence of large numbers of suspended Synechococcus cells, all surrounded by calcite minerals and existing as cell-mineral aggregates. These eventually
sink to the lake bottom, forming its extensive marl
sediment.
In the laboratory Synechococcus cells suspended in
Fayetteville Green Lake water can become totally
encrusted in gypsum or calcite within 8 h, yet these
bacteria divide only once within 72 h [42]. To prevent their total encasement in mineral, and death,
they continuously shed o¡ patches of mineralised
S-layer which is rapidly replaced by new material.
Eventually, as cells enter senescence, this shedding
ceases, and the bacteria become surrounded by a
crust of calcite, die, and sink to the bottom as a
¢ne-grained calcitic sediment particle.
6. Precipitation of minerals other than carbonates in
natural microbial communities
Stromatolitic structures involving non-carbonaceous mineral types have also been observed and
postulated to have a microbially catalysed deposition
mechanism. Phosphorites are P-rich sedimentary
rocks, usually composed of carbonate hydroxyl £uorapatite (Ca10 (PO4 CO3 )6 F2ÿ3 ) which occurs as nodules and crusts originally formed in oceanic environments [43]. The nodular and stromatolitic forms of
these mineral deposits could be of microbial origin.
Southgate [43] examined columnar phoscretes in
Australia in an attempt to discern their formation
mechanism. In these laminated structures, a ubiquitous association between the phosphate and organic
matter was found. It was concluded that phosphates
may preferentially nucleate upon the `organic matter', which would provide nucleation sites for its deposition. Soudry and Champtier [44] interpreted Pcoated structures seen by scanning electron microscopy to be cyanobacterial sheaths due to their size
and morphology. A similar study [45] suggested
these structures may represent fungal hyphae coated
with phosphoritic minerals.
In addition to the minerals described above, organosedimentary structures of microbial origin have
also been associated with dolomite [46], gypsum
[47], and deposits of elemental metals such as Cu
[48] and Au [49]. It is interesting that bacteria can
form placer gold during laboratory simulations using
aqueous solutions of gold chloride [50]. In all cases,
bacteria were implicated as the `concentrating factor'
for the metals and it is likely that, as more investigations are undertaken, their role will become clearer
and the phenomenon more widely seen.
7. Conclusion
The preceding discussion reveals that bacteria
have played and are continuing to play a determinative role in the mineralogical characteristics of most
soil and sediment environments. As the number and
variety of geomicrobiological studies continue to
grow it is hoped that the complex geochemical role
of bacteria will become clearer. Many essential elements (C, S, N, P) have a large lithospheric reservoir
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S. Douglas, T.J. Beveridge / FEMS Microbiology Ecology 26 (1998) 79^88
within which they are largely unavailable to many
living organisms. Bacteria can liberate such elements
by processes such as weathering as well as reformulate them into a wide range of minerals.
The ability of bacteria to accumulate metal ions
has led to speculation that these organisms represent
an important cleansing mechanism in natural environments. The immobilisation of metal ions and
their subsequent transport into aquatic sediments
or deep soil layers represents an important means
of lowering the `free' metal concentration in environments threatened by the presence of toxic metals
(e.g., Cd, Ni, Cu). Our understanding of the mechanism and extent of bacterial metal binding activities
can help us to learn how much of a heavy metal load
a natural environment can take without breaking
down. In addition, bacteria may represent a potentially signi¢cant tool in bioremediation strategies.
[7]
[8]
[9]
[10]
[11]
[12]
[13]
Acknowledgments
T.J.B.'s research has been funded by the Natural
Sciences and Engineering Research Council of Canada (NSERC) through operating and infrastructure
grants. The latter provided partial support for the
NSERC Regional STEM Facility where all the authors' electron microscopical work was performed.
[14]
[15]
[16]
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