FEMS Microbiology Reviews 20 (1997) 503^516
Microbial solubilization and immobilization of toxic metals:
key biogeochemical processes for treatment of contamination
C. White, J.A. Sayer, G.M. Gadd *
Department of Biological Sciences, University of Dundee, Dundee DD1 4HN, UK
Abstract
Microorganisms play important roles in the environmental fate of toxic metals with a multiplicity of physico-chemical and
biological mechanisms effecting transformations between soluble and insoluble phases. Such mechanisms are important
components of natural biogeochemical cycles for metals and metalloids with some processes being of potential application to
the treatment of contaminated materials. This paper will concentrate on three selected aspects which illustrate the key
importance of microorganisms in effecting changes in metal(loid) solubility, namely toxic metal sulfide precipitation by sulfatereducing bacteria, heterotrophic leaching by fungi, and microbial transformations of metalloids, which includes reduction and
methylation. The basic microbiology of these processes is described as well as their environmental significance and use in
bioremediation.
Keywords:
Toxic metal; Sul¢de; Heterotrophic leaching; Oxalate; Metalloid; Reduction; Methylation
Contents
1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2. Metal precipitation by sulfate-reducing bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.1. Mechanisms of metal removal by sulfate-reducing bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.2. Processes utilizing sulfate-reducing bacteria for metal removal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3. Heterotrophic leaching by fungi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.1. Fungal metal-chelating agents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4. Microbial metalloid transformations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.1. Microbial reduction of metalloid oxyanions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.2. Methylation of metalloids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.3. Microbial metalloid transformations and bioremediation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
* Corresponding author. Tel.: +44 (1382) 344266; Fax: +44 (1382) 344275; e-mail: [email protected]
0168-6445/97/$32.00 ß 1997 Federation of European Microbiological Societies. Published by Elsevier Science B.V.
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C. White et al. / FEMS Microbiology Reviews 20 (1997) 503^516
1. Introduction
Environmental contamination by toxic metals is of
increasing economic, public health and environmental signi¢cance [1^4]. Although there is variation in
national standards and reporting, an indication of
the extent of land contamination by toxic metals
can be gained from the fact that, in the United
States, 389 out of 703 National Priorities List sites
contained toxic metal contaminants and the existence of at least 100 000 such sites was estimated
for the European Union [5,6]. The impact of biological processes on metal contamination and the potential for bioremediation are dependent on the nature of the site and the chemical environment. In
soils or sediments the potential ecological or public
health hazard posed by toxic metals depends upon
the form in which metals occur. Mineral components, for example, may contain considerable quantities of metal which are unavailable to organisms
but soluble metal species have greater mobility and
bioavailability [4,7]. Biological processes can either
solubilize metals, thereby increasing their bioavailability and potential toxicity, or immobilize them
and reduce their bioavailability. The relative balance
between mobilization and immobilization varies depending on the organisms, their environment and
changing physico-chemical conditions. As well as
being a key component of natural biogeochemical
cycles for metals, these processes may be exploited
for the treatment of contaminated solid and liquid
wastes [1,3,8]. Metal mobilization can be carried out
by a range of microorganisms and processes include
autotrophic and heterotrophic leaching, chelation by
microbial metabolites and siderophores, and methylation which can result in volatilization. Similarly,
many organisms can contribute to immobilization
by sorption to cell components or exopolymers,
transport and intracellular sequestration or precipitation as insoluble organic and inorganic compounds, e.g., oxalates [9], sul¢des or phosphates
[10^12]. Depending on the metal and its detailed
chemistry, biologically mediated reduction of highvalency species may e¡ect mobilization, e.g.,
Mn(IV) to Mn(II), or immobilization, e.g., Cr(VI)
to Cr(III) [7,13]. In the context of bioremediation,
solubilization of metal contaminants provides a
route for removal of the metals from soils, sediments
and industrial wastes by, e.g., acid leaching or chelation. Alternatively, processes such as precipitation
may enable metals to be transformed in situ into
insoluble, chemically inert forms. Immobilization
processes are particularly applicable to removing
metals from mobile phases such as groundwaters
and leachates. This paper will address three biological processes which are of signi¢cance in determining metal mobility in di¡erent environments and
which have actual or potential applications in bioremediation of metal and metalloid pollution. These
are sulfate reduction and precipitation of toxic metals as sul¢des, interactions with microbial organic
acids which can either mobilize or precipitate metals
and, lastly, metalloid biotransformations involving
reduction or methylation.
2. Metal precipitation by sulfate-reducing bacteria
Sulfate-reducing bacteria are heterotrophic bacteria which require strictly anaerobic conditions with
an Eh of less than 3200 mV [14]. The main organic
carbon/energy substrates utilized by the fastest-growing organisms, e.g., Desulfovibrio species, are low
molecular mass organic acids such as lactic or acetic
acid and alcohols such as ethanol [14,15]. The pattern of carbon dissimilation is essentially similar in
all cases in that the organic substrate is oxidized
either completely to CO2 or to some intermediate
compound. ATP is generated via an electron-transport chain with sulfate as the terminal electron acceptor which is reduced to sul¢de [15,16]. The generation of sul¢de has a number of consequences that
are relevant to biotechnological metal removal.
These are the creation of reducing conditions, removal of acidity and precipitation of metals from solution
as sul¢des. Metal sulfates frequently occur in polluted
waters including acid mine drainage [17] and can also
arise from metallurgical processes such as the smelting of sul¢dic ores [18]. This provides a readily available substrate for sulfate reduction which can be exploited for purposes of bioremediation.
2.1. Mechanisms of metal removal by sulfate-reducing
bacteria
The main mechanism whereby sulfate-reducing
C. White et al. / FEMS Microbiology Reviews 20 (1997) 503^516
bacteria remove toxic metals from solution is via the
formation of metal sul¢de precipitates. The solubility
products of most toxic metal sul¢des are very low so
that even a moderate output of sul¢de can e¡ectively
remove metals, reducing concentrations to levels well
below those permitted in the environment [19]. Sulfate-reducing bacterial cultures are necessarily anaerobic and most metal sul¢des are stable under these
conditions. Sulfate-reducing bacteria also create conditions which favor chemical reduction of metals, for
example, uranium(VI) to uranium(IV) [13].
Sulfate-reducing bacteria are almost entirely mesophilic with maximum growth occurring in the range
pH 6^8 [14]. However, some isolates can grow in
moderately acid conditions where the bulk phase
pH is in the range 3^4. In these environments the
sulfate-reducing bacteria are found in sediments
and their apparent acid tolerance is derived from
the existence of more neutral microenvironments
within this habitat which are maintained by the activities of the sulfate-reducing bacteria [20]. Both sulfate reduction and metal reduction utilize protons
and therefore contribute to the generation of alkalinity in the environment of the organism. As well as
a direct e¡ect on the pH of waste-waters, which may
be bene¢cial in the case of acid mine drainage, the
solubility of most toxic metal compounds, including
sul¢des, is also lower at neutral than at acidic pH so
that alkalization enhances metal removal as sul¢des.
In addition to lowering the solubility of metal sul¢des, an elevation in pH can also contribute directly
to precipitation of certain metals, e.g., Al, as hydroxides.
2.2. Processes utilizing sulfate-reducing bacteria for
metal removal
Sulfate reduction and metal precipitation as sul¢des are signi¢cant components of some successful
large-scale processes for biotechnological metal removal. Sulfate reduction is signi¢cant in the operation of arti¢cial and natural wetlands and contributes signi¢cantly to metal removal [20]. Both sulfateand iron-reducing bacteria occur in arti¢cial wetlands which have been used as a low-cost treatment
for acid mine drainage in which the activity of sulfate-reducing bacteria has been signi¢cant in raising
pH [21]. Recent observations have indicated that
505
Fe(III)-reducing bacteria are of equal or greater signi¢cance with sulfate-reducing bacteria in these systems and Fe(III)-reducing bacteria may be the main
route for alkalization if carbon substrates are in
short supply [22]. In an operating system of arti¢cial
meanders the main reported route for removal of
metals from the water column was by biosorption
on detritus and algae [23] but it is also likely that
sulfate-reducing activity in the sediment will have
contributed to mineralization of the sedimented metals. Sul¢de precipitation also occurs during anaerobic digestion in the presence of sulfate where metalremoval is a useful by-product of organic waste
treatment [24].
Reactor-based processes using bacterial sulfate reduction have also been developed for treatment of
metal-contaminated waters. One system using 900 ml
¢xed-bed reactors with spent mushroom compost as
the support was used to remove nickel from a simulated mine water containing approximately 20 mM
sulfate and 0.85^16.9 mM nickel. Approximately
75% of the nickel present was removed when no
additional carbon source was supplied and more
than 95% when sodium lactate was provided [21].
A pilot-scale study used the same support medium
in either 3 200 l ¢xed-bed vessels in series (`Pittsburgh system') and single 4500 l vessels (`Palmerton
system') at residence times of between 9 and 17 days.
The `Pittsburgh system' raised the pH from 3.2 to 6.4
and removed all of the Fe and Al in the system. The
`Palmerton system' also raised the pH to between 6.2
and 7.1 and removed the majority of the Zn, Mn, Ni
and Cd in the in£ow. The amount of Ca in solution
increased in both systems indicating that the limestone component of the compost had contributed
to neutralization [25].
The most extensive use of a process utilizing sulfate-reducing bacteria is in the treatment of contaminated groundwater at the Budelco zinc-smelting
works at Budel-Dorplein in The Netherlands. The
pilot plant comprised a purpose-designed 9 m3 stainless steel sludge blanket reactor using sulfate-reducing bacteria and was developed by Shell Research
Ltd and Budelco B.V. This plant successfully removed toxic metals (primarily Zn) and sulfate from
contaminated groundwater at the long-standing
smelter site by precipitation as metal sul¢des. The
reactor used a selected but unde¢ned consortium of
U
C. White et al. / FEMS Microbiology Reviews 20 (1997) 503^516
506
Fig. 1. Diagram showing the integrated process for bioremediation of metal-contaminated soils. The outline reactions and conditions for
the bioleaching and bioprecipitation stages are shown in addition to the inputs and organisms utilized. M2‡ = target metal ions (considered
as divalent cations). Adapted from [30].
sulfate-reducing bacteria with ethanol as the growth
to commercial scale in 1992 using an 1800 m3 con-
substrate. It was capable of tolerating a wide range
crete reactor built by Parques B.V. (Netherlands)
of
in£ow
pH
and
operating
temperatures,
and
and is capable of treating over 7000 m3 day31 .
yielded out£ow metal concentrations below the ppb
An integrated biological approach utilizing auto-
range. Methanogenic bacteria in the consortium also
trophic leaching by sulfur-oxidizing bacteria fol-
removed acetate produced by the sulfate-reducing
lowed by sulfate reduction and metal sul¢de precip-
bacteria, leaving an e¥uent with an acceptably low
itation
BOD [18,26,27]. Excess gaseous H2 S was stripped
contaminating toxic metals from soils (Fig. 1). In
out of waste gases using a ZnSO4 solution. A de-
the
tailed analysis of this process including mass-balance
which produce sulfuric acid, are employed to leach
was also carried out [28]. The process was expanded
metals from soils, both by the breakdown of sul¢de
has
also
integrated
been
process,
developed
to
sulfur-oxidizing
remove
bacteria,
C. White et al. / FEMS Microbiology Reviews 20 (1997) 503^516
minerals and by liberation of acid-labile forms from,
e.g., hydroxides, carbonates or sorbed metals. The
metals are released as an acidic sulfate solution
which enables both a large proportion of the acidity
and almost the entirety of the metals to be removed
in a subsequent process using bacterial sulfate reduction. In a laboratory study, using arti¢cially metalcontaminated soil, production of sulfate commenced
almost immediately and the e¥uent pH also dropped
rapidly after an initial lag period due to cation exchange in the soil. As the pH decreased, metals were
leached in the order: Mn, Cr, Ni, Co, Cd, Zn, Cu,
Pb, although there were considerable overlaps where
several metals were leached simultaneously. During
the initial phase of operation the leach liquor was
recycled through the soil in order to facilitate acidi¢cation until the leachate pH dropped to 3.0, when
single-pass operation commenced and the liquor was
passed to the second, bioprecipitation stage. The
leachate fed into the bioprecipitation reactor varied
in sulfate concentration over the approximate range
35^50 mM, pH 1.5^3.0. The bioreactor used for this
stage was an internal sedimentation feedback bioreactor [29] capable of retaining a high concentration
of biomass. It contained a mixed, unde¢ned culture
of sulfate-reducing bacteria produced by combining
a number of metal-tolerant enrichment cultures from
di¡erent environmental origins [11,12]. It was supplied with a concentrated nutrient mixture containing ethanol as carbon/energy source with additional
inorganic phosphate and ammonium as well as organic nitrogen, supplied in the form of cornsteep
[11,12]. Metals were mainly precipitated as solid sul¢des, although other compounds such as hydroxides
and carbonates were undoubtedly present. Removal
of the target metals by the bioreactor achieved more
than 98% e¤ciency overall with the exception of Mn
and, to a lesser extent, Ni and Pb (Table 1) [30]. The
metals were concentrated substantially in the sul¢de
precipitate as compared to the concentration in clari¢ed liquor, greatly facilitating safe disposal.
3. Heterotrophic leaching by fungi
Fungi can remove both soluble and insoluble metal species from solution and are also able to leach
metal cations from solid wastes [31,32]. To date,
507
most biological metal leaching has been carried out
with chemoautotrophic bacteria such as Thiobacillus
species. In an industrial context, bioleaching must be
as simple as possible and these organisms do not
need an organic carbon source (although a sulfur
source is necessary), gaining energy from redox reactions, and they have a greater acidi¢cation capacity than most fungi [32,33]. However, these bacteria are acidophilic and may not tolerate the higher
pH values of many industrial metal-loaded wastes
including soils. Heterotrophic fungi can withstand a
much wider pH range, and many can produce organic acids which can solubilize and complex metal cations [32]. There are many fungi capable of producing
organic acids and Burgstaller and Schinner [32] list
several species which produce large amounts, including Yarrowia lipolytica (citric), Mucor spp. (fumaric,
gluconic), Rhizopus spp. (lactic, fumaric, gluconic),
Aspergillus niger (citric, oxalic, gluconic), Aspergillus
spp. (citric, malic, tartaric, K-ketoglutaric, itaconic,
aconitic), Penicillium spp. (citric, tartaric, K-ketoglutaric, malic, gluconic) and Schizophyllum commune
(malic). By altering parameters such as the N and
P balance of the medium and optimum pH, these
species can be used to produce a wide range of organic acids for metal leaching purposes. Furthermore, the presence or absence of metal ions, e.g.,
manganese, can have a strong in£uence on the production of citric acid [34], while a high glycolytic £ux
rate, which provides the precursors for citrate, pyTable 1
Metal concentrations in the bioleaching and bioprecipitation
stages of the integrated process for bioremediation of metal-contaminated soils
Metal
Metal concentration (Wmol l31 )
Leachate Bioprecipitation products
Clari¢ed liquor `Sludge'a
Cadmium
40
0.1
40
Chromium
10
0.1
10
Cobalt
51
0.2
51
Copper
19
0.2
19
Lead
4
0
4
Manganese
637
182.0
455
Nickel
51
1.7
50
Zinc
49
3.1
46
a
This material is the concentrated suspension of biomass and precipitated metal sul¢des which were obtained from the active zone
of the bioreactor. Adapted from [30].
C. White et al. / FEMS Microbiology Reviews 20 (1997) 503^516
508
3.1. Fungal metal-chelating agents
Sayer et al. [37] used a screening method to detect
and isolate fungal strains capable of solubilization
ability using three insoluble toxic metal compounds
(Co3 (PO4 )2 , ZnO and Zn3 (PO4 )2 ). The assay, based
on observing clear zones around colonies growing on
agar amended with the insoluble metal compounds
[37,38], also provided information on relative toxicities and tolerance. Fig. 2 shows the solubilization of
Zn3 (PO4 )2 by
A. niger after 6 days growth at 25³C.
Of a number of soil isolates tested, approximately
one third were able to solubilize at least one of the
test
metal
compounds
(Co3 (PO4 )2 ,
ZnO
and
Zn3 (PO4 )2 ), and approximately 10% were able to
solubilize all three [37] (Table 2).
It has been shown [38^41] that
Fig. 2. The solubilization of Zn3 (PO4 )2 by
Aspergillus niger when
grown on malt extract agar amended with 0.4% (w/v) Zn3 (PO4 )2 .
P. simplicissimum
can leach Zn2‡ from insoluble zinc oxides present in
industrial ¢lter dust (which mainly comprises ZnO)
s 100 mM) being
The photograph was taken after 6 days growth at 25³C and
with large amounts of citric acid (
shows the clear zone of solubilization extending into the agar
produced after 9 days incubation. Adsorption of the
around the colony. Scale bar = 1 cm.
dust onto the mycelium was required to trigger acid
production, possibly due to an alteration in plasma
membrane H‡ -ATPase activity.
A. niger culture ¢l-
ruvate and oxaloacetate, is also necessary [35]. There
trate has been used to leach Cu from copper con-
are several examples of fungi being used for metal
verter slag [42]. The ¢ltrate was able to solubilize
leaching. Strasser et al. [36] optimized oxalic acid
18% Cu, 7% Ni and 4% Co and these amounts
production by
were increased when HCl was added. It was sug-
A. niger
which was able to produce
over 200 mM oxalic acid when grown on sucrose and
gested that the H‡ attacked the raw minerals while
lactose (low cost carbon sources) at pH 6.0 in a fed
the organic acid anions present in the ¢ltrate com-
batch stirred tank reactor. Oxalic acid can act as a
plexed the released metal cations. `Red mud' is the
leaching agent for a variety of metals which form
waste product from the extraction of Al from baux-
soluble metal oxalate complexes, including Al, Fe
ite. Vachon et al. [43] have leached red mud chemi-
and Li.
cally using sulfuric, citric and oxalic acids, and bio-
Table 2
Growth e¡ects and solubilization of 15 mM ZnO, 5 mM Zn3 (PO4 )2 and 5 mM Co3 (PO4 )2 by 56 strains of soil fungi, grouped according
to the combinations of the individual metal compounds used
Stimulation of growth
ZnO
1
Sol.
Inhibition of growth
Sol.
1
47
13
No growth e¡ect
8
Sol.
3
Zn3 (PO4 )2
13
1
22
5
21
2
Co3 (PO4 )2
4
1
47
14
5
2
ZnO, Zn3 (PO4 )2
0
^
22
2
5
^
ZnO, Co3 (PO4 )2
0
^
42
8
1
1
Zn3 (PO4 )2 , Co3 (PO4 )2
3
^
21
3
3
^
ZnO, Zn3 (PO4 )2 , Co3 (PO4 )2
0
^
21
3
1
^
Numbers shown are the strains exhibiting stimulation or inhibition of growth, or no change in growth from the control, and accompanying
solubilization. Sol., solubilization of metal compound(s) ; ^, not detected. Adapted from [57].
C. White et al. / FEMS Microbiology Reviews 20 (1997) 503^516
Fig. 3. Complexation of 100
WM
2‡
Zn
509
(solid line) shown by polarograms obtained by stepwise additions of 10
U
100
Aspergillus niger
Wl
culture ¢ltrate, obtained after 15 days growth at 25³C. The decrease in peak height and shift in the evolution potential is indicative of
complex formation.
logically, using adapted thiobacilli from sewage and
complexation by microbial metabolites. Fig. 3 shows
strains of
the complexation of Zn
tatum
most
A. niger, P. simplicissimum, Penicillium noTrichoderma viride
P. simplicissimum
and
. The thiobacilli were
e¤cient
although
was
the
2‡
by
A. niger
culture super-
natants, which contain at least three organic acids,
citric, oxalic and gluconic. Successive additions of
most e¤cient of the fungal strains, and it was no-
supernatant
ticed that the ability of the fungal-derived solutions
and
(mainly citric acid) to leach Al was far greater than
complex formation. This fungal culture supernatant
pure citric acid.
was found to be at least as e¡ective at complexing
Citric and oxalic acids are often cited as powerful
Zn
a
2‡
shift
as
resulted
in
the
in
a
decrease
evolution
commercially
in
peak
potential,
available
citric
height
indicating
and
oxalic
natural chelating agents, and in the soil, organic acid
acids. Complexation of metal ions with citrate can
production can be important for the release of met-
result in the formation of highly mobile species and
als and nutrients such as phosphate [44,45]. Oxalate
therefore allow transport and activity of toxic metals
and citrate are released into the soil by plant roots
at a distance from their source. On the other hand,
and fungal hyphae, and soil oxalate concentrations
interaction with oxalic acid could ultimately lead to
of up to 1.0 M have been reported [46]. These low
the formation of insoluble oxalates which could im-
molecular mass organic acids are capable of forming
mobilize toxic metal species. Metal oxalates can be
stable complexes with many metals in solution. Ox-
produced by a wide range of fungi including mycor-
alate has a high capacity for the solubilization of
rhizas
phosphate
Most metal oxalates are immobile and resistant to
and
citrate
is
a
powerful
iron
chelator
[47].
further
and
lichenicolous
solubilization,
fungi
with
[9,48^53]
only
a
few
(Fig.
species
4).
of
Polarography and stripping voltammetry are ana-
anaerobic bacteria, aerobic actinomycetes, bacteria
lytical techniques, within a group of methods known
and fungi able to degrade them readily [54]. How-
as voltammetry (current-voltage measurements at a
ever, while the deposition of calcium oxalate is wide-
desired electrode) which can be used to assess metal
spread, the deposition of oxalates containing poten-
C. White et al. / FEMS Microbiology Reviews 20 (1997) 503^516
510
Fig. 4. Insoluble metal oxalate crystals produced under colonies of
Zn3 (PO4 )2 , scale bar = 10
Wm,
(B) Sr(NO3 )2 , scale bar = 10
Wm,
Aspergillus niger
growing on malt extract agar amended with (A)
(C) Cu3 (PO4 )2 , scale bar = 10
Wm,
(D) Mn3 (PO4 )2 , scale bar = 100
Wm.
tially toxic metal ions has rarely been observed in the
growing on wood treated with a copper-containing
natural environment, apart from the precipitation of
fungicide [55^57], and lichenicolous fungi growing
copper as copper oxalate by wood rotting fungi
on copper sul¢de bearing rocks [48,49,58].
511
C. White et al. / FEMS Microbiology Reviews 20 (1997) 503^516
4. Microbial metalloid transformations
Microorganisms can transform metal and metalloid species by oxidation, reduction, methylation
and dealkylation [13,59,60]. Biomethylated metal derivatives are often volatile and may be eliminated
from a system by evaporation [61]. Two major transformation processes have been described for metalloids, (i) reduction of metalloid
oxyanions to elemental forms, e.g., SeO 3 and SeO 3 to Se and (ii)
methylation of metalloids, metalloid oxyanions or
organometalloids
to methyl derivatives, e.g.,
AsO 3 , AsO3 and methylarsonic acid to (CH ) As
(trimethylarsine). Transformation processes have biogeochemical signi¢cance, since they modify the mobility and toxicity of metalloids, and are also of biotechnological potential in bioremediation [13,59,
60,62^66].
2
4
3
4
2
3
o
3 3
2
4.1. Microbial reduction of metalloid oxyanions
Reduction of selenate (Se(VI)) and selenite
(Se(IV)) to elemental selenium can be catalyzed by
numerous bacterial and fungal species [64,67].
Maiers et al. [68] described reduction of SeO 3 to
elemental selenium, resulting in a red precipitate,
by microbial populations isolated from water, sediment and soil from the selenium-rich Kesterson Reservoir in California,
USA. Microbial reduction of
100 mg Se l3 (1.3 mmol Se l3 ) was e¡ected within
one week of incubation
with up to 75 mg Se l3
3
(0.9 mmol Se l ) being reduced to Se . Electron
dense bodies consisting of Se were found to be associated with cells of Pseudomonas maltophila O-2, a
strain isolated from
a toxic waste site, following inmedium [69]. Certain
cubation in SeO 3-containing
organisms can use SeO 3 as an electron acceptor to
support growth. Oremland et al. [70] reported oxida-3
tion of acetate, with concomitant reduction of SeO
to Se , by bacteria isolated from anoxic sediments.
The authors proposed
the following overall mechanism for SeO 3 reduction:
2
4
1
1
1
1
o
o
2
3
2
4
2
4
o
2
4
4CH3 COO3 ‡ 3SeO243 !
3Seo ‡ 8CO2 ‡ 4H2 O ‡ 4H‡
…1†
Macy et al. [71] reported that a Pseudomonas sp.
was able to respire SeO 3 to SeO 3, with oxidation
of C-labelled acetate to CO , by the following
equation:
2
4
14
2
3
14
2
CH3 COO3 ‡ H‡ ‡ 4SeO243 !
…2†
2CO2 ‡ 4SeO233 ‡ 2H2 O
Another bacterial isolate, a strict anaerobe, was
able to reduce SeO3 3 to Se , though it was not
of these organisms
able to reduce SeO . Co-culture
resulted in reduction of SeO 3 to Se . More recently,
a novel species, Thauera selenatis, has
been isolated
to
that 3is capable of anaerobic SeO 3 respiration
SeO with concomitant reduction of NO3 : SeO 3
formed from this reduction was further reduced to
Se [72^74]. The authors suggested that the periplasmic nitrite reductase was responsible for SeO 3 re-3
duction [75]. It is generally believed that while SeO
may act as a terminal electron acceptor
to support
growth of some organisms, SeO 3 reduction does
not support growth and is more likely to3 function
in detoxi¢cation [64]. Reduction of TeO to Te is
also an apparent means of detoxi¢cation
found in
bacteria [76]. Uptake of TeO 3 by resistant cells is
followed by reduction to Te which is deposited in or
around cells, particularly near the cytoplasmic membrane [69,77^82].
In contrast to bacterial systems, fungal reduction
of metalloids has received less biochemical attention
although it is known that numerous ¢lamentous3 and
unicellular fungal species are capable of SeO reduction to Se , resulting in a red coloration of colonies [67,83^85]. Both extracellular and intracellular
deposition of Se³ has been demonstrated
[67].
Less work has been done on TeO 3 reduction by
fungi: Smith [86] showed
that Schizosaccharomyces
pombe reduced TeO 3 to Te giving black or gray
colonies.
2
4
2
3
o
2
4
o
2
4
2
3
2
3
3
o
2
3
2
4
2
3
2
3
o
o
2
3
2
3
o
2
3
2
3
o
4.2. Methylation of metalloids
Microbial methylation of metalloids to yield volatile derivatives such as dimethylselenide or trimethylarsine is a well-known phenomenon catalyzed by a
variety of bacteria, algae and fungi [59,60,63,65^
67,85,87]. While bacteria and fungi are important
in volatilization of selenium from soils and sedi-
512
C. White et al. / FEMS Microbiology Reviews 20 (1997) 503^516
ments, bacteria are thought to play a more dominant
role in selenium-contaminated waters [88]. The
mechanism for selenium methylation appears to involve transfer of methyl groups as carbonium (CH‡3 )
ions via the S-adenosyl methionine system [59]. Less
work has been carried out on tellurium methylation
by fungi [66] although there is evidence of dimethyltelluride and dimethylditelluride production by a
Penicillium sp. [89]. Several bacterial and fungal species have been shown to methylate arsenic compounds such as arsenate (As(V), AsO343 ), arsenite
(As(III), AsO32 ) and methylarsonic acid
(CH3 H2 AsO3 ) to volatile dimethyl- ((CH3 )2 HAs) or
trimethylarsine ((CH3 )3 As) [63]. Methylated derivatives of arsenic are generally less toxic than organic
forms.
4.3. Microbial metalloid transformations and
bioremediation
Selenium has received most attention to date
although it is likely that transformations of other
metalloids, e.g., As, Te, will also be important. Removal of selenium (as SeO243 ) from contaminated
water and soil by bacteria and fungi has been demonstrated. Oremland et al. [90,91] described in situ
removal of SeO243 , by reduction to Seo , by sediment
bacteria in agricultural drainage regions of Nevada.
Flooding of exposed sediments at Kesterson Reservoir with water (in order to create anoxic conditions)
resulted in reduction (and thereby immobilization) of
large quantities of selenium that had been present in
sediments [92]. Microbial methylation of selenium,
resulting in volatilization, has also been used for in
situ bioremediation of selenium-containing land and
water at Kesterson Reservoir, California [93]. Selenium volatilization from soil was enhanced by optimizing soil moisture, particle size and mixing [94]
while in waters it was stimulated by the growth
phase, salinity, pH and selenium concentration [95].
The selenium-contaminated agricultural drainage
water was evaporated to dryness until the sediment
selenium concentration approached 100 mg Se kg31
dry weight. Conditions such as carbon source, moisture, temperature and aeration were then optimized
for selenium volatilization and the process continued
until selenium levels in sediments declined to acceptable levels [93,96]. Some potential for ex situ treat-
ment of selenium-contaminated waters has also been
demonstrated. SeO243 in uranium-mine discharge
waters was microbially reduced to Seo after passage
through a soil column [97]. Removal of SeO243 in the
presence of NO33 by reduction to Seo in an algalbacterial system has also been suggested [98]. NO33 ,
an inhibitor of SeO243 reduction, was removed during
algal growth in the ¢rst stage with the water
then being treated in an anaerobic digester. Macy
et al. [73] described the simultaneous removal of
SeO243 and NO33 under anaerobic conditions from
selenium-contaminated drainage water by Thauera
selenatis in recycled sludge blanket and £uidized
bed reactors (1-l working volume). NO33 and
SeO243 levels were reduced by approximately 98%,
the ¢nal product of the reduction process again
being Seo .
5. Conclusions
The microbial processes described in this paper are
all signi¢cant components of metal and metalloid
biogeochemistry, although details such as the global
scale and environments a¡ected vary. Bioprecipitation by sulfate-reducing bacteria and volatilization
by biomethylation have received the most extensive
practical applications to date of the processes discussed. However, since the chemistry and biology
of individual polluted sites largely dictates the bioremediation method to be applied, it can be expected
that a wider range of processes will be applied in the
future.
Acknowledgments
G.M.G. gratefully acknowledges ¢nancial support for his own work from NERC/AFRC (Special
Topic Programme: Pollutant transport in soils
and rocks), BBSRC (BCE 03292, SPC 2922, SPC
02812, BSW 05375, SPC 05211, TO6495), the
Royal Society (London) (638072:P779 Project
grant), British Nuclear Fuels plc, the Royal Society of Edinburgh (Scottish O¤ce Education Department/RSE Support Research Fellowship 19941995) and NATO (ENVIR.LG.950387 Linkage
grant).
C. White et al. / FEMS Microbiology Reviews 20 (1997) 503^516
References
[15] Hansen, T.A. (1993) Carbon metabolism in sulfate-reducing
bacteria. In :
[1] Gadd, G.M. (1992) Microbial control of heavy metal pollution. In :
513
Microbial Control of Pollution (Fry, J.C., Gadd,
G.M., Herbert, R.A., Jones, C.W. and Watson-Craik, I.A.,
The Sulfate-Reducing Bacteria :
Contemporary
Perspectives (Odom, J.M. and Singleton, R., Eds.), pp. 21^
40. Springer Verlag, New York, NY.
[16] Peck, H.D. (1993) Bioenergetic strategies of the sulfate-reduc-
Eds.), pp. 59^88. Cambridge University Press, Cambridge.
ing bacteria. In : The Sulfate-Reducing Bacteria : Contempo-
[2] Gadd, G.M. (1997) Roles of microorganisms in the environ-
rary Perspectives (Odom, J.M. and Singleton, R., Eds.), pp.
mental
fate
of
radionuclides.
In :
CIBA
Foundation
203 :
Health Impacts of Large Releases of Radionuclides (Bock,
41^75. Springer Verlag, New York, NY.
[17] Uhrie, J.L., Drever, J.I., Colberg, P.J.S. and Nesbitt, C.C.
G.R. and Cardew, G., Eds.). John Wiley and Sons, Chiches-
(1996)
ter.
with
[3] White, C., Wilkinson, S.C. and Gadd, G.M. (1995) The role
of microorganisms in biosorption of toxic metals and radio-
In
[4] Wainwright, M. and Gadd, G.M. (1997) Industrial Pollutants.
immobilisation
leach
mines
by
of
heavy
bacterial
metlas
associated
sulphate
reduction.
Hydrometallurgy 43, 231^239.
[18] Taylor,
M.R.G.
clean-up
nuclides. Int. Biodeterior. Biodegrad. 35, 17^40.
situ
uranium
and
methods
McLean,
for
R.A.N.
contaminated
(1992)
sites.
Overview
JIWEM
6,
of
408^
417.
In : The Mycota, Volume IV : Environmental and Microbial
[19] Crathorne, B. and Dobbs, A.J. (1990) Chemical pollution of
Relationships (Wicklow, D.T. and Soderstrom, B., Eds.), pp.
the aquatic environment by priority pollutants and its control.
85^97. Springer-Verlag, Berlin.
In : Pollution : Causes, E¡ects and Control (Harrison, R.M.,
[5] Wilmoth, R.C., Hubbard, S.J. and Burckle, J.O. (1991) Pro-
Ed.), pp. 1^18. The Royal Society of Chemistry, Cambridge.
duction and processing of metals : their disposal and future
[20] Hedin, R.S. and Nairn, R.W. (1991) Contaminant removal
risks. In : Metals and their Compounds in the Environment :
capabilities of wetlands constructed to treat coal mine drain-
Occurrence, Analysis and Biological Relevance (Merian, E.,
age. In : Proceedings of the International Symposium on Con-
Ed.), pp. 19^65. VCH, Weinheim.
structed Wetlands for Water-Quality Improvement (Moshiri,
[6] Schmitt,
H.W.
and
Stitcher,
H.
(1991)
Heavy
metal
com-
pounds in soil. In : Metals and their Compounds in the Envi-
G.A., Ed.), pp. 187^195. Lewis Publishers, Chelsea, MI.
[21] Hammack, R.W. and Edenborn, H.M. (1992) The removal of
Relevance
nickel from mine waters using bacterial sulphate-reduction.
[7] White, C. and Gadd, G.M. (1997) Reduction of metal cations
[22] Vile, M. and Wieder, R.K. (1993) Alkalinity generation by
ronment :
Occurrence,
Analysis
and
Biological
Appl. Microbiol. Biotechnol. 37, 674^678.
(Merian, E., Ed.), pp. 311^331. VCH, Weinheim.
and oxyanions by anaerobic and metal-resistant organisms :
Fe(III)
chemistry, physiology and potential for the control and bio-
structed
remediation
Pollut. 69, 425^441.
of
toxic
metal
pollution.
In :
Extremophiles :
Physiology and Biotechnology (Grant, W.D. and Horikoshi,
G.M.
and
White,
C.
(1993)
Microbial
for
acid
versus
mine
sulfate
drainage
reduction
in
treatment.
wetlands
Water
con-
Air
Soil
[23] Gale, N.L. (1986) The role of algae and other microorganisms
in metal detoxi¢cation and environmental clean-up. In : Bio-
T., Eds.). John Wiley and Sons, New York, NY.
[8] Gadd,
reduction
treatment
of
metal pollution ^ a working biotechnology ? Trends Biotech-
technology
for
Processing
Industries
the
Mining,
Metal-re¢ning
(Ehrlich,
H.L.
and
and
Fossil
Holmes,
Fuel
D.S.,
Eds.), pp. 171^180. John Wiley and Sons, New York, NY.
nol. 11, 353^359.
[9] Sayer, J.A. and Gadd, G.M. (1997) Solubilization and trans-
[24] Cowling, S.J., Gardner, M.J. and Hunt, D.T.E. (1992) Re-
formation of insoluble metal compounds to insoluble metal
moval of heavy metals from sewage by sulphide precipitation :
oxalates by
thermodynamic calculations and tests on a pilot-scale anaero-
Aspergillus niger
. Mycol. Res. (in press)
[10] Yong, P. and Macaskie, L.E. (1995) Enhancement of uranium
Citrobacter
bic reactor. Environ. Technol. 13, 281^291.
sp. via enzymically-medi-
[25] Dvorak, D.H., Hedin, R.S., Edenborn, H.M. and McIntyre,
ated growth of polycrystalline NH4 UO2 PO4 . J. Chem. Tech-
P.E. (1991) Treatment of metal-contaminated water using bac-
nol. Biotechnol. 63, 101^108.
terial sulfate-reduction : results from pilot-scale reactors. Bio-
bioaccumulation by a
[11] White, C. and Gadd, G.M. (1996) Mixed sulphate-reducing
technol. Bioeng. 40, 609^616.
bacterial cultures for bioprecipitation of toxic metals : factorial
[26] Scheeren, P.J.H., Koch, R.O., Buisman, C.J.N., Barnes, L.J.
and response-surface analysis of the e¡ects of dilution rate,
and Versteegh, J.H. (1991) New biological treatment plant for
sulphate
heavy metal contaminated groundwater. In :
and
substrate
concentration.
Microbiology
142,
2197^2205.
[12] White, C. and Gadd, G.M. (1996) A comparison of carbon/
EMC91.
Non
Ferrous
Metallurgy
Present
Proceedings of
and
Future,
pp.
403^416. Elsevier, Amsterdam.
energy and complex nitrogen sources for bacterial sulphate-
[27] Barnes, L.J., Scheeren, P.J.M. and Buisman, C.J.N. (1994)
reduction : potential applications to bioprecipitation of toxic
Microbial removal of heavy metals and sulphate from con-
metals as sulphides. J. Ind. Microbiol. 17, 116^123.
taminated groundwaters. In : Emerging Technology for Biore-
[13] Lovley, D.R. (1995) Bioremediation of organic and metal contaminants with dissimilatory metal reduction. J. Ind. Microbiol. 14, 85^93.
[14] Postgate, J.R. (1984) The Sulphate-Reducing Bacteria. Cambridge University Press, Cambridge.
mediation of Metals (Means, J.L. and Hinchee, R.E., Eds.),
pp. 38^49. Lewis Publishers, Boca Raton, FL.
[28] Barnes,
L.J.,
Janssen,
F.J.,
Sherren,
J.H.,
Versteegh,
J.H.,
Koch, R.O. and Scheeren, P.J.H. (1991) A new process for
the
microbial
removal
of
sulphate
and
heavy
metals
from
C. White et al. / FEMS Microbiology Reviews 20 (1997) 503^516
514
contaminated waters extracted by a geohydrological control
ic acids on the release of phosphorus from phosphate rocks.
Soil Sci. 158, 442^453.
system. Trans. Inst. Chem. Eng. 69, 184^186.
[29] Pirt, S.J. (1985) Principles of Microbe and Cell Cultivation.
[46] Godtfredsen, K.L. and Stone, A.T. (1994) Solubilization of
manganese dioxide bound copper by naturally occurring or-
Blackwell, Oxford.
[30] Eccles, H.and Holroyd, C.P. (1996) An integrated bioremediation route for contaminated land and liquid e¥uents. In :
ganic compounds. Environ. Sci. Technol. 28, 1450^1458.
[47] Tyler, G. and Strom, L. (1995) Di¡ering organic acid exudation pattern explains calcifuge and acidifuge behaviour of
Minerals, Metals and the Environment II (in press).
[31] Wainwright, M. and Grayston, S. (1989) Accumulation and
plants. Ann. Bot. 75, 75^78.
oxidation of metal sulphides by fungi. In : Metal-Microbe In-
[48] Purvis, O.W. (1984) The occurrence of copper oxalate in li-
teractions (Poole, R.K. and Gadd, G.M., Eds.), pp. 119^130.
chens growing on copper sulphide-bearing rocks in Scandinavia. Lichenologist 16, 197^204.
IRL Press, Oxford.
[32] Burgstaller, W. and Schinner, F. (1993) Leaching of metals
drated copper oxalate, moolooite, in lichens. Mycol. Res.
with fungi. J. Biotechnol. 27, 91^116.
[33] Ballester, A., Gonzalez, F., Blazquez, M.L. and Barril, M.A.
(1989) Microbial leaching of copper from lead mattes. Metal-
51, 715^718.
[50] Lapeyrie, F., Chilvers, G.A. and Bhem, C.A. (1987) Oxalic
acid synthesis by the mycorrhizal fungus
lurg. Trans. B208, 773^779.
[34] Ma, H., Kubicek, C.P. and Rohr, M. (1985) Metabolic e¡ects
of manganese de¢ciency in
[49] Chisholm, J.E., Jones, G.C. and Purvis, O.W. (1987) Hy-
Aspergillus niger :
evidence for
Paxillus involutus.
New Phytol. 106, 139^146.
[51] Asea, P.E.A., Kucey, R.M.N. and Stewart, J.W.B. (1988) In-
Penicillium species in
increased protein degradation. Arch. Microbiol. 141, 266^
organic phosphate solubilization by two
268.
solution culture and soil. Soil Biol. Biochem. 20, 459^464.
[35] Harmsen, H.J.M., Kubicek-Pranz, E.M., Rohr, M., Visser, J.
[52] Lapeyrie, F., Ranger, J. and Vairelles, D. (1991) Phosphate
and Kubicek, C.K. (1992) Regulation of 6-phosphofructo-2-
solubilizing activity of ectomycorrhizal fungi in vitro. Can. J.
kinase from the citric-acid-accumulating fungus
niger. Appl. Microbiol. Biotechnol. 37, 784^788.
Aspergillus
[36] Strasser, H., Burgstaller, W. and Schinner, F. (1994) High
yield production of oxalic acid for metal leaching processes
by
Aspergillus niger. FEMS Microbiol. Lett. 119, 365^370.
[37] Sayer, J.A., Raggett, S.L. and Gadd, G.M. (1995) Solubilization of insoluble metal compounds by soil fungi : development
of a screening method for solubilizing ability and metal toler-
Bot. 69, 342^346.
[53] Cunningham, J.E. and Kuiack, C. (1992) Production of citric
and oxalic acids and solubilization of calcium phosphate by
Penicillium bilaii. Appl. Environ. Microbiol. 58, 1451^1458.
[54] Morris, S.J. and Allen, M.F. (1994) Oxalate metabolising microorganisms in Sagebrush Steppe soil. Biol. Fertil. Soils 18,
255^259.
[55] Murphy, R.J. and Levy, J.F. (1983) Production of copper
oxalate by some copper tolerant fungi. Trans. Br. Mycol.
ance. Mycol. Res. 99, 987^993.
[38] Burgstaller, W., Strasser, H., Wobking, H. and Schinner, F.
Soc. 81, 165^168.
Peni-
[56] Sutter, H.P., Jones, E.B.G. and Walchli, O. (1983) The mech-
[39] Schinner, F. and Burgstaller, W. (1989) Extraction of zinc
[57] Sutter, H.-P., Jones, E.B.G. and Walchi, O. (1984) Occurrence
(1992) Solubilization of zinc oxide from ¢lter dust with
cillium simplicissimum : bioreactor leaching and stoichiometry.
Environ. Sci. Technol. 26, 340^346.
from an industrial waste by a
Penicillium sp. Appl. Environ.
Microbiol. 55, 1152^1156.
[40] Franz, A., Burgstaller, W. and Schinner, F. (1991) Leaching
with
Penicillium simplicissimum : in£uence of metals and bu¡-
ers on proton extrusion and citric acid production. Appl. En-
of crystalline hyphal sheaths in
Poria placenta
and
(Fr.) Cke. J.
Inst. Wood Sci. 10, 19^23.
[58] Fox, T.R. and Comerford, N.B. (1990) Low molecular-weight
organic acids in selected forest soils of the southeastern USA.
Soil Sci. Soc. Am. J. 54, 1139^1144.
[59] Gadd, G.M. (1993) Microbial formation and transformation
viron. Microbiol. 57, 769^774.
[41] Franz, A., Burgstaller, W., Muller, B. and Schinner, F. (1993)
In£uence of medium components and metabolic inhibitors on
citric acid production by
Poria placenta (Fr.) Cke.
Poria vaillantii (Pers.) Fr. Mat. Organ. 18, 241^263.
anism of copper tolerance in
Penicillium simplicissimum.
J. Gen.
Microbiol. Rev. 11, 297^316.
[60] Brady, J.M., Tobin, J.T. and Gadd, G.M. (1996) Volatilization of selenite in a aqueous medium by a
Microbiol. 139, 2101^2107.
[42] Sukla, L.B., Kar, R.N. and Panchanadikar, V. (1992) Leach-
Aspergillus niger
of organometallic and organometalloid compounds. FEMS
Penicillium species.
Mycol. Res. 100, 955^961.
culture
[61] Trevors, J.T. (1986) Mercury methylation by bacteria. J. Basic
[43] Vachon, P., Tyagi, R.D., Auclair, J.C. and Wilkinson, K.J.
[62] Steinberg, N.A. and Oremland, R.S. (1990) Dissimilatory
(1994) Chemical and biological leaching of aluminium from
selenate reduction potentials in a diversity of sediment types.
ing of copper converter slag with
¢ltrate. Biometals 5, 169^172.
red mud. Environ. Sci. Technol. 28, 26^30.
Microbiol. 26, 499^504.
Appl. Environ. Microbiol. 56, 3550^3557.
[44] Bolan, N.S., Naidu, R., Mahimairaja, S. and Baskaran, S.
[63] Tamaki, S. and Frankenberger, W.T. (1992) Environmental
(1994) In£uence of low-molecular-weight organic acids on
biochemistry of arsenic. Rev. Environ. Contam. Toxicol.
the solubilization of phosphates. Biol. Fertil. Soils 18, 311^
319.
[45] Kpomblekou, K. and Tabatabai, M.A. (1994) E¡ect of organ-
124, 79^110.
[64] Lovley, D.R. (1993) Dissimilatory metal reduction. Annu.
Rev. Microbiol. 47, 263^290.
C. White et al. / FEMS Microbiology Reviews 20 (1997) 503^516
[65] Gadd, G.M. (1993) Interactions of fungi with toxic metals.
Escherichia coli
515
cells harboring resistance plasmids. J. Ultra-
struct. Mol. Struct. Res. 99, 18^26.
New Phytol. 124, 25^60.
[66] Karlson, U. and Frankenberger, W.T. (1993) Biological alky-
[81] Lloyd-Jones, G., Ritchie, D.A. and Strike, P. (1991) Biochem-
lation of selenium and tellurium. In : Metal Ions in Biological
ical and biophysical analysis of plasmid pMJ600-encoded tel-
Systems (Sigel, H. and Sigel, A., Eds.), pp. 185^227. Marcel
lurite (
Dekker, New Yorkm NY.
of
selenium
oxyanions
by
unicellular,
polymorphic
and ¢lamentous fungi : cellular location of reduced selenium
and implications for tolerance. J. Ind. Microbiol. 14, 300^311.
[68] Maiers, D.T., Wichlacz, P.L., Thompson, D.L. and Bruhn,
D.F. (1988) Selenate reduction by bacteria from a seleniumrich environment. Appl. Environ. Microbiol. 54, 2591^2593.
[69] Blake, R.C., Choate, D.M., Bardhan, S., Revis, N., Barton,
L.L. and Zocco, T.G. (1993) Chemical transformation of toxic
Pseudomonas
metals by a
) resistance. FEMS Microbiol. Lett. 81, 19^24.
[82] Moore, M.D. and Kaplan, S. (1992) Identi¢cation of intrinsic
[67] Gharieb, M.M., Wilkinson, S.C. and Gadd, G.M. (1995) Reduction
TeO233
strain from a toxic waste site. En-
viron. Toxicol. Chem. 12, 1365^1376.
high-level
resistance
members of the class
to
rare-earth
oxides
Proteobacteria :
and
oxyanions
lurite, selenite and rhodium sesquioxide reduction in
bacter sphaeroides. J. Bacteriol. 174, 1505^1514.
[83] Zieve,
R.,
Ansell,
P.J.,
Young,
T.W.K.
(1985) Selenium volatilization by
in
characterization of tel-
and
Mortierella
Rhodo-
Peterson,
P.J.
species. Trans.
Br. Mycol. Soc. 84, 177^179.
[84] Ramadan,
S.E.,
Razak,
A.A.,
Yousse¡,
Y.A.
and
N.M. (1988) Selenium metabolism in a strain of
Sedky,
Fusarium.
Biol. Trace Elem. Res. 18, 161^170.
[85] Morley, G.F., Sayer, J.A., Wilkinson, S.C., Gharieb, M.M.
[70] Oremland, R.S., Hollibaugh, J.T., Maest, A.S., Presser, T.S.,
and Gadd, G.M. (1996) Fungal sequestration, mobilization
Miller, L.G. and Culbertson, C.W. (1989) Selenate reduction
and transformation of metals and metalloids. In : Fungi and
to elemental selenium by anaerobic bacteria in sediments and
Environmental
culture : biogeochemical signi¢cance of a novel sulfate-inde-
Gadd, G.M., Eds.), pp. 235^256. Cambridge University Press,
pendent respiration. Appl. Environ. Microbiol. 55, 2333^2343.
[71] Macy, J.M., Michel, T.A. and Kirsch, D.G. (1989) Selenate
reduction
by
a
new
Pseudomonas
species :
a
new
mode
of
anaerobic respiration. FEMS. Microbiol. Lett. 61, 195^198.
[72] Macy, J.M., Rech, S., Auling, G., Dorsch, M., Stackebrandt,
E. and Sli, L.I. (1993)
Thaueria selenatis gen. nov., sp.nov., a
Change
(Frankland,
J.C.,
Cambridge.
[86] Smith, D.G. (1974) Tellurite reduction in
pombe. J. Gen. Microbiol. 83, 389^392.
and
[87] Challenger, F. (1945) Biological methylation. Chem. Rev. 36,
315^361.
[88] Thompson-Eagle, E.T., Frankenberger, W.T. and Karlson, U.
Alternaria alternata.
(1989)
type of anaerobic respiration. Int. J. Syst. Bacteriol. 43, 135^
Appl. Environ. Microbiol. 55, 1406^1413.
Volatilization
of
selenium
by
[89] Huysmans, K.D. and Frankenberger, W.T. (1991) Evolution
[73] Macy, J.M., Lawson, S. and Demolldecker, H. (1993) Bioremediation
of
water using
selenium
oxyanions
Thaueria selenatis
in
San
Joaquin
anaerobically
H.
and
nitrite reductase of
Macy,
sp. isolated from agricul-
in a biological reactor system.
[90] Oremland, R.S., Steinberg, N.A., Maest, A.S., Miller, L.G.
with
acetate
m ) of Thaueria
plus
selenate
or
J.M.
(1993)
and Hollibaugh, J.T. (1990) Measurement of in situ rates of
selenate removal by dissimilatory bacterial reduction in sediments. Environ. Sci. Technol. 24, 1157^1164.
[91] Oremland,
nitrate. Arch. Microbiol. 160, 295^298.
[75] Demolldecker,
Penicillium
tural evaporation pond water. Sci. Tot. Environ. 105, 13^28.
[74] Macy, J.M. and Lawson, S. (1993) Cell yield (Y
grown
of trimethylarsine by a
drainage
Appl. Microbiol. Biotechnol. 40, 588^594.
selenatis
N.
Schizosaccharomyces
member of the beta-subclass of proteobacteria with a novel
142.
Magan,
The
periplasmic
Thaueria selenatis may catalyze the reduc-
tion of selenite to elemental selenium. Arch. Microbiol. 160,
R.S.,
Steinberg,
N.A.,
Presser,
T.S.
and
Miller,
L.G. (1991) In situ bacterial selenate reduction in the agricultural drainage systems of Western Nevada. Appl. Environ.
Microbiol. 57, 615^617.
[92] Long, R.H.B., Benson, S.M., Tokunaga, T.K. and Yee, A.
241^247.
[76] Walter, E.G. and Taylor, D.E. (1992) Plasmid-mediated resistance to tellurite : expressed and cryptic. Plasmid 27, 52^64.
(1990) Selenium immobilization in a pond sediment at Kesterson Reservoir. J. Environ. Qual. 19, 302^311.
P.,
[93] Thompson-Eagle, E.T. and Frankenberger, W.T. (1992) Bio-
Hobman, J.L., Brown, N.L. and Rouch, D.A. (1994) Accu-
remediation of soils contaminated with selenium. In : Advan-
mulation and intracellular fate of tellurite in tellurite-resistant
ces in Soil Science (Lal, R. and Stewart, B.A., Eds.), pp. 261^
[77] Lloyd-Jones,
G.,
Escherichia coli :
Osborn,
a
model
A.M.,
for
the
Ritchie,
D.A.,
mechanism
of
Strike,
resistance.
FEMS Microbiol. Lett. 118, 113^120.
[78] Moore, M.D. and Kaplan, S. (1994) Members of the family
Rhodospirillaceae
reduce heavy-metal oxyanions to maintain
redox poise during photosynthetic growth. Am. Soc. Microbiol. News 60, 17^23.
[79] Bradley, D.E., Grewal, K.K., Taylor, D.E. and Whelan, J.
(1988) Characteristics of RP4 tellurite-resistance transposon
Tn521. J. Gen. Microbiol. 134, 2009^2018.
309. Springer Verlag, New York, NY.
[94] Frankenberger,
W.T.
and
Karlson,
U.
(1994)
Soil-manage-
ment factors a¡ecting volatilization of selenium from dewatered sediments. Geomicrobiol. J. 12, 265^278.
[95] Rael, R.M. and Frankenberger, W.T. (1996) In£uence of pH,
salinity and selenium on the growth of
Aeromonas veronii
in
evaporation agricultural drainage water. Water Res. 30, 422^
430.
[96] Thompson-Eagle,
E.T.,
Frankenberger,
W.T.
and
Longley,
[80] Taylor, D.E., Walter, E.G., Sherburne, R. and Bazett-Jones,
K.E. (1991) Removal of selenium from agricultural drainage
D.P. (1988) Structure and location of tellurium deposited in
water through soil microbial transformations. In : The Eco-
516
C. White et al. / FEMS Microbiology Reviews 20 (1997) 503^516
nomics and Management of Water and Drainage in Agriculture (Dinar, A. and Zilberman, D., Eds.), pp. 169^186.
Kluwer Academic, New York, NY.
[97] Kau¡man, J.W., Laughlin, W.C. and Baldwin, R.A. (1986)
Microbiological treatment of uranium mine waters. Environ.
Sci. Technol. 20, 243^248.
[98] Gerhardt, M.B., Green, F.B., Newman, D., Lundquist, T.J.,
Tresan, R. and Oswald, W.J. (1991) Removal of selenium
using a novel algal-bacterial process. Res. J. Water Pollut.
Con. Fed. 63, 799^805.