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Applied and Environmental Microbiology, March 2000, p. 1050-1056, Vol. 66, No. 3
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Reduction of Fe(III), Mn(IV), and Toxic Metals at
100°C by Pyrobaculum islandicum
Kazem
Kashefi and
Derek R.
Lovley*
Department of Microbiology, University of
Massachusetts, Amherst, Massachusetts 01003
Received 27 September 1999/Accepted 15 December 1999
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ABSTRACT |
It has recently been noted that a diversity of hyperthermophilic
microorganisms have the ability to reduce Fe(III) with hydrogen as the
electron donor, but the reduction of Fe(III) or other metals by these
organisms has not been previously examined in detail. When
Pyrobaculum islandicum was grown at 100°C in a medium
with hydrogen as the electron donor and Fe(III)-citrate as the electron acceptor, the increase in cell numbers of P. islandicum per
mole of Fe(III) reduced was found to be ca. 10-fold higher than
previously reported. Poorly crystalline Fe(III) oxide could also serve
as the electron acceptor for growth on hydrogen. The stoichiometry of
hydrogen uptake and Fe(III) oxide reduction was consistent with the
oxidation of 1 mol of hydrogen resulting in the reduction of 2 mol of
Fe(III). The poorly crystalline Fe(III) oxide was reduced to
extracellular magnetite. P. islandicum could not
effectively reduce the crystalline Fe(III) oxide minerals goethite and
hematite. In addition to using hydrogen as an electron donor for
Fe(III) reduction, P. islandicum grew via Fe(III) reduction
in media in which peptone and yeast extract served as potential
electron donors. The closely related species P. aerophilum
grew via Fe(III) reduction in a similar complex medium. Cell
suspensions of P. islandicum reduced the following metals
with hydrogen as the electron donor: U(VI), Tc(VII), Cr(VI), Co(III),
and Mn(IV). The reduction of these metals was dependent upon the
presence of cells and hydrogen. The metalloids arsenate and selenate
were not reduced. U(VI) was reduced to the insoluble U(IV) mineral
uraninite, which was extracellular. Tc(VII) was reduced to insoluble
Tc(IV) or Tc(V). Cr(VI) was reduced to the less toxic, less soluble
Cr(III). Co(III) was reduced to Co(II). Mn(IV) was reduced to Mn(II)
with the formation of manganese carbonate. These results demonstrate
that biological reduction may contribute to the speciation of metals in
hydrothermal environments and could account for such phenomena as
magnetite accumulation and the formation of uranium deposits at ca.
100°C. Reduction of toxic metals with hyperthermophilic
microorganisms or their enzymes might be applied to the remediation of
metal-contaminated waters or waste streams.
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INTRODUCTION |
Recent studies have suggested that
the capacity for dissimilatory Fe(III) reduction is a common
characteristic of hyperthermophilic Archaea and
Bacteria (58). However, these initial studies
only represented a very preliminary screening of the potential for dissimilatory metal reduction at high temperature. For example, growth
studies were only conducted on two organisms, Thermotoga maritima and Pyrobaculum islandicum. In those studies,
soluble Fe(III) citrate was provided as the electron acceptor whereas the environmentally relevant Fe(III) forms are insoluble Fe(III) oxides
(28). Furthermore, no stoichiometric data was available to
demonstrate that Fe(III) reduction was the sole sink for hydrogen consumption.
Further investigation of Fe(III) reduction at temperatures of ca.
100°C is warranted because of the potential environmental and
evolutionary significance of this form of respiration. For example, as
recently reviewed (62), common physiological characteristics of hyperthermophilic Bacteria and Archaea are
often considered to provide insights into the physiological properties
of the earliest microorganisms because hyperthermophiles are the extant
organisms most closely related to the last common ancestors of modern
life. Thus, the finding that all hyperthermophiles that have been
investigated have a constitutive ability to reduce Fe(III) has led to
the suggestion that early microorganisms had the capacity for Fe(III)
reduction (58). This concept is consistent with geochemical
evidence which suggests that conditions on pre-biotic Earth were
conducive to hydrogen oxidation coupled to Fe(III) reduction and that
Fe(III) reduction was one of the earliest forms of microbial
respiration (7, 11, 28, 60).
Geochemical evidence suggests that Fe(III) reduction also is, or has
been, an important process in hot biospheres other than early Earth.
For example, the recovery of larger quantities of ultrafine-grained
magnetite at depths of 5.5 to 6.7 km in the terrestrial subsurface, was
proposed as evidence for a modern deep, hot subsurface biosphere
(15) because the magnetite was morphologically similar to
magnetite known to be produced by dissimilatory Fe(III)-reducing
bacteria (27, 44). It was further speculated that there
could be similar hot biospheres below the surfaces of other planets
(15), and ultrafine-grained magnetite was subsequently found
in meteorite ALH84001, which some believe contains evidence of previous
life on Mars (46). Modern hydrothermal fluids generally contain high concentrations of Fe(II), which can be oxidized to Fe(III)
upon exposure to oxygen with the subsequent deposition of Fe(III)
oxides within hot anaerobic environments (3, 20, 21), and it
has been suggested that microbial Fe(III) reduction warrants "special
attention" to help better understand carbon and electron flow in
marine hydrothermal vents (21).
Many mesophilic microorganisms that have the ability use Fe(III) as a
terminal electron acceptor can also reduce a variety of metals and
metalloids other than Fe(III) (29, 33). After Fe(III),
Mn(IV) is the most abundant metal likely to be found as a potential
electron acceptor in sedimentary environments, and most Fe(III)
reducers have the capacity to reduce Mn(IV) (31, 33). Trace
metals reduced by Fe(III)-reducing microorganisms include the oxidized
forms of the radioactive metals uranium (41, 43) and
technetium (26), as well as the other trace metals and
metalloids, such as cobalt (6, 16), chromium
(29), arsenic (24), and selenium (50).
Many of these metals and metalloids are environmental contaminants, and
reduction of contaminant metals with Fe(III)-reducing microorganisms
has been shown to have potential for the removal of contaminant metals
from waters and waste streams and to immobilize metals in subsurface
environments (30, 32). Microbial reduction of some of these
metals may also play an important role in the formation of metal
deposits, which might be especially important in hot environments
containing metal-rich waters. A thermophilic Thermus species
was found to reduce the contaminant metals uranium, chromium, and
cobalt at 60°C (23). However, the potential for
hyperthermophiles to reduce metals other than Fe(III) does not appear
to have been previously evaluated.
P. islandicum is an anaerobic hyperthermophile that was
recovered from hydrothermal groundwater (19). It was
initially found to grow at an optimum temperature of 100°C with
hydrogen as the electron donor and S° as the electron acceptor or
with complex organics and a variety of sulfur compound electron
acceptors (19). Previous studies suggested that
Pyrobaculum islandicum us a suitable model organism for
studying Fe(III) reduction in hyperthermophilic Archaea
(58). The purpose of the studies reported here was to further investigate enzymatic reduction of Fe(III) oxides at 100°C with P. islandicum and to determine its potential for the
reduction of other metals. The results demonstrate that not only can
P. islandicum reduce Fe(III) oxide to Fe(II), it can reduce
a variety of other metals of environmental interest that might account
for important geological phenomena and have applications for
remediation of metal-contaminated waters.
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MATERIALS AND METHODS |
Source of organisms.
P. islandicum (DSM 4184) was
purchased from the German Collection of Microorganisms (DSM),
Braunschweig, Germany. P. aerophilum (DSM 7523) was a gift
from Imke Schroeder (Department of Microbiology and Molecular Genetics,
University of California, Los Angeles).
Culturing techniques.
Strict anaerobic techniques (2,
47) were used throughout, as previously described
(38). All incubations were 100°C in the dark, unless
otherwise specified. For routine maintenance of cultures, 10 ml of
medium was dispensed into anaerobic pressure tubes (Bellco Glass, Inc.,
Vineland, N.J.) and sparged with the appropriate gas mixture (as
described below) for 10 min in order to remove dissolved oxygen from
the medium. For the cell growth studies, 50 to 100 ml of medium was
dispensed into 120-ml serum bottles and sparged for ca. 30 min with the
appropriate gas mixture.
For growth of P. islandicum with hydrogen as the electron
donor and poorly crystalline Fe(III) oxide as the electron acceptor, DSM medium 390, which is suggested for growth P. islandicum,
was modified by replacing the thiosulfate with poorly crystalline Fe(III) oxide (100 mmol/liter) prepared as previously described (37). Yeast extract (0.01%) and sodium bicarbonate (1.93 g/liter) were added, and L-cysteine (0.25 mM) was
substituted for the sodium sulfide. Vitamins and trace minerals were
added from stock solutions (35). The headspace was
H2-CO2 (80:20, vol/vol). The pH of the autoclaved medium was 6.2.
For studies on the stoichiometry of hydrogen uptake and reduction of
poorly crystalline Fe(III) oxide, the headspace of the
medium was
N
2-CO
2 (80:20) and ca. 1 ml of hydrogen was
added to
initiate the study. Fe(II) and hydrogen were measured, as
described
below, at the start of the incubation and after most of the
hydrogen
had been
consumed.
For growth with organic compounds as the electron donor, the
bicarbonate was omitted from the medium described above, the
concentration of yeast extract was increased to 0.02% and 0.05%
peptone was added. The gas phase was N
2. The pH was 6.2. Fe(III)-citrate
was present at 20 mM. For comparison of the reduction
of various
Fe(III) oxides, goethite, hematite, or poorly crystalline
Fe(III)
oxide was provided at 100 mmol/liter as previously described
(
37).
Medium for evaluating the growth of
P. aerophilum on Fe(III)
was a modification of the peptone medium previously used to culture
this organism (
22). Fe(III) was provided as Fe(III) citrate
(20 mM). The pH was adjusted to 6.8 to 7.0 with HCl. The gas phase
was
N
2-CO
2 (80:20, vol/vol).
Cell suspension studies.
For cell suspension studies,
P. islandicum was grown in Fe(III)-citrate as the electron
acceptor and organic compounds as the electron donor in the medium
described above. Cells from 800-ml cultures grown in 1-liter bottles
were harvested under N2 with centrifugation. The cells were
suspended in 80 ml of anaerobic bicarbonate buffer (23 mM) under
N2-CO2 and repelleted with centrifugation, and
then this procedure repeated. The cells were resuspended in 8 ml of the
bicarbonate buffer under N2-CO2. In order to
determine the potential for the cells to reduce various metals, an
aliquot of the cell suspension (ca. 0.1 ml) was added to metal-amended bicarbonate buffer (10 ml; pH 6) under H2-CO2
to provide ca. 0.025 mg of cell protein per ml.
For studies on U(VI) reduction, U(VI) was provided as uranyl acetate.
Mn(IV) was added as MnO
2 (15 mmol/liter) synthesized
as
previously described (
38). Cr(VI) was added as potassium
chromate. Co(III)-EDTA was generated by oxidizing Co(II) in the
presence of MnO
2 and EDTA as previously described
(
16) and added
at a final concentration of 250 µM. Tc(VII)
was added as ammonium
pertechnetate to provide a final concentration of
250 µM. As(V)
was supplied as sodium arsenate (100 µM), and Se(VI)
was provided
as sodium selenate (100 µM). Incubations were done at
100°C in
the dark, except for the studies conducted with technetium,
in
which incubation was done at 90°C.
Analytical techniques.
Production of HCl-extractable Fe(II)
was measured with ferrozine as previously described (36).
For the studies on the stoichiometry of hydrogen uptake and Fe(III)
oxide reduction, Fe(III) and Fe(II) were determined with the anaerobic
oxalate extraction technique as previously described (51).
Hydrogen concentrations were monitored with gas chromatography as
previously described (34). Concentrations of U(VI) in cell
suspension studies were measured on filtrates (0.2-µm pore diameter)
injected into a Dionex DX-500 Ion Chromatograph with an HPIC-AS5 column
and 0.1 M MgSO4-0.05 M H2SO4 as
the eluent. U(VI) was monitored as A650
following an Arsenazo-III postcolumn derivitization (10).
For Mn(II) determinations, Mn(II) was solubilized in 0.5 N HCl and the
acidic extract was injected into a Dionex IonPac CS5A column with a
solution of 1.4 mM pyridine-2,6-dicarboxylic acid, 13.2 mM potassium
hydroxide, 1.12 mM potassium sulfate, and 14.8 mM formic acid as the
eluent. Mn(II) was detected at A530 after
postcolumn derivitization with a solution containing 1.0 M
2-dimethylaminoethanol, 0.5 M ammonium hydroxide, 0.3 M sodium
bicarbonate, and 0.06 g of 4-(2-pyridylazo)resorcinol per liter.
Co(II) was detected in a manner similar to that used for Mn(II). Cr(VI)
concentrations were monitored with the diphenylcarbazide method as
previously described (40). Technetium reduction was analyzed
with a PhosphorImager technique as previously described (26).
Cells were counted with acridine orange staining and epifluorescence
microscopy as previously described (
38). Particulate
iron
forms were dissolved by the oxalate method as previously
described
(
38), except that Fe(II) chloride (final concentrations,
ca.
5 mM) was added to the samples to accelerate
dissolution.
Protein concentrations were determined as previously described
(
55). Bovine serum albumin was the reference
protein.
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RESULTS |
Reduction of Fe(III).
P. islandicum grew in medium
with hydrogen as the electron donor and Fe(III)-citrate as the electron
acceptor (Fig.1). The increase in cell
numbers per mole of Fe(III) reduced was ca. 10-fold higher than the
cell yield reporter in a comparable previous study with this organism
(58). As discussed below, this difference was the result of
a calculation error in the earlier study. P. islandicum also
grew in medium in which peptone was provided as a potential electron
donor (Fig.2). The closely related
species P. aerophilum grew in a similar manner (K. Kashefi;
unpublished data). The number of cells of P. islandicum
produced per mole of Fe(III) reduced was higher in the complex medium
(Fig. 2) than in medium in which hydrogen served as the electron donor
for Fe(III) reduction (Fig. 1).
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FIG. 1.
Growth of P. islandicum in medium with
hydrogen as the electron donor and Fe(III)-citrate as the electron
acceptor. The medium also contained 0.01% yeast extract. The results
are the means of triplicate cultures.
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FIG. 2.
Growth of P. islandicum with peptone as the
electron donor and Fe(III)-citrate as the electron acceptor. The medium
also contained 0.02% yeast extract. The results are the means of
triplicate cultures.
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P. islandicum could also use poorly crystalline Fe(III)
oxide as the electron acceptor for hydrogen oxidation (Fig.
3). The
number of cells produced per mole
of Fe(III) reduced when Fe(III)
oxide was the electron acceptor was
comparable to that with Fe(III)-citrate.
Hydrogen did not abiotically
reduce the Fe(III) oxide, and in
the presence of cells, hydrogen was
required for Fe(III) reduction
and growth. Measurements of hydrogen
consumption and Fe(III) oxide
reduction in five replicate cultures
demonstrated that 2.06 ±
0.16 (mean ± standard error) mol
of Fe(III) was reduced per mol
of hydrogen consumed, which is
consistent with the stoichiometry
expected from the following reaction:
H
2 + 2 Fe(III)
2 Fe(II)
+ 2 H
+.
P. islandicum also reduced poorly crystalline Fe(III) oxide
when grown in the peptone-yeast extract medium (Fig.
4). In contrast,
the more crystalline
Fe(III) oxide forms goethite and hematite
were only poorly reduced, if
at all (Fig.
4).
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FIG. 3.
Growth of P. islandicum in medium with
hydrogen as the electron donor and poorly crystalline Fe(III) oxide as
the electron acceptor. The medium also contained 0.01% yeast extract.
The results are the means of triplicate cultures.
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FIG. 4.
Fe(III) reduction by P. islandicum grown on
various forms of Fe(III) in peptone-yeast extract medium. The results
are the means of duplicate cultures.
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Reduction of poorly crystalline Fe(III) oxide was associated with a
visible change in the iron. The nonmagnetic, reddish brown,
poorly
crystalline Fe(III) oxide was converted to a black magnetic
precipitate
(Kashefi, unpublished). X-ray diffraction analysis
indicated that this
precipitate is comprised of magnetite, and
electron microscopy revealed
that the magnetite is deposited extracellularly
(Kashefi,
unpublished).
Reduction of other metals.
Washed cell suspensions of
Fe(III)-grown P. islandicum were capable of reducing a
variety of other metals. For example, U(VI) was readily reduced with
hydrogen as the electron donor (Fig. 5).
When U(VI) was added at a more environmentally relevant initial concentration of 10 µM, the U(VI) was completely reduced within 1 h (Kashefi, unpublished). Hydrogen did not abiotically reduce U(VI) at 100°C, and there was no reduction of U(VI) when the cells were incubated at a temperature too low for enzymatic activity of
P. islandicum (Fig. 5). During U(VI) reduction, a dark
precipitate formed. X-ray diffraction analysis of this product
indicated that it contained the U(IV) mineral uraninite, which is
deposited outside the cell (Kashefi, unpublished).
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FIG. 5.
Reduction of U(VI) in cell suspensions of P. islandicum. The results are the means of duplicate incubations.
The cell protein concentration was 0.025 mg/ml.
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When Tc(VII) was added to cell suspensions of
P. islandicum
with hydrogen as the electron donor, the radioactivity added as
Tc(VII)
was recovered as a reduced form after overnight incubation
(Fig.
6). In contrast, the radioactivity
remained in the Tc(VII)
pool if the cell suspensions were incubated at
30°C or if the
cells were omitted from the incubation.
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FIG. 6.
PhosphorImager analysis of paper chromatograms of
supernatant from cell suspensions of P. islandicum incubated
overnight in the presence of Tc(VII). The cell protein concentration
was 0.012 mg/ml.
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Cell suspensions of
P. islandicum also rapidly reduced
Mn(IV) and Co(III)-EDTA, as evidenced by accumulation of Mn(II) and
Co(II) over time (Kashefi, unpublished). Mn(IV) reduction was
associated with rapid disappearance of the dark brown Mn(IV) oxide
and
formation of a white precipitate that was presumably the manganese
carbonate rhodochrosite. Attempts to grow
P. islandicum with
Mn(IV)
as the sole electron acceptor were not
successful.
Cr(VI) was also reduced in cell suspensions (Fig.
7). The yellow color, characteristic of
Cr(VI) in solution, disappeared
as the concentration of Cr(VI)
diminished, and there was the formation
of a white colloidal
suspension, characteristic of Cr(III) hydroxide.
This indicates that
the loss of Cr(VI) was the result of Cr(VI)
reduction to Cr(III). There
was no abiotic reduction of Cr(VI)
at 100°C and no reduction at
30°C in the presence of cells.
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FIG. 7.
Cr(VI) reduction in cell suspensions of P. islandicum. The results are the means of duplicate incubations.
The cell protein concentration was 0.025 mg/ml.
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DISCUSSION |
This study represents the first detailed study of metal reduction
by a hyperthermophilic microorganism. The results demonstrate that
P. islandicum can readily reduce poorly crystalline Fe(III) oxide with either hydrogen or complex organics as the electron donor
and is also capable of reducing a wide variety of trace metals of
geological and environmental significance. As detailed below, these
results provide further insight into the potential role of
hyperthermophiles in the reduction of Fe(III) in hot environments, suggest potential mechanisms for the deposition of minerals at high
temperatures, and may provide new potential approaches for the
bioremediation of metal contamination.
Energy conservation via Fe(III) reduction.
Although a
diversity of hyperthermophilic microorganisms have been shown to have
the capacity to reduce Fe(III) (58), to date, P. islandicum and P. aerophilum are the only
Archaea that have definitely been shown to conserve energy
to support growth from dissimilatory Fe(III) reduction.
Hydrogen-dependent growth of P. islandicum associated with
the reduction of soluble Fe(III) was previously demonstrated
(58). The increase in cell numbers reported here with
hydrogen as the electron donor and Fe(III) citrate as the electron
acceptor is ca. 10-fold higher than that previously reported under
similar conditions (58). This apparent difference is due to
a miscalculation in computing the previously reported cell numbers
(Kashefi, unpublished). A similar error was made in the calculation of
the growth of Thermatoga maritima in that previous study.
The increase in cell numbers of P. islandicum per Fe(III)
millimolar reduced reported here is comparable to the growth previously
reported for several other hydrogen-oxidizing, Fe(III)-reducing
mesophilic microorganisms (5, 9, 42).
The studies on the stoichiometry of hydrogen consumption and Fe(III)
reduction indicate that hydrogen can serve as the primary
electron
donor for Fe(III) reduction in
P. islandicum. P. islandicum has not been found to be capable of autotrophic growth
with hydrogen
and Fe(III), as small amounts of yeast extract are
required for
growth. This contrasts with the ability of this organism
to grow
autotrophically with hydrogen and S° as the electron acceptor
(
19). All of the mesophilic Fe(III)-reducing microorganisms
reported to data were also found to require the addition of carbon
sources for growth on Fe(III) with hydrogen as the electron donor
(
1,
5,
42). However, an autotrophic hydrogen-oxidizing,
Fe(III)-reducing hyperthermophile has recently been isolated (K.
Kashefi, J. M. Tor, and D. R. Lovley, unpublished
data).
P. islandicum produced more cells per mole of Fe(III)
reduced in a complex medium that contained peptone as a potential
electron
donor than in medium with hydrogen as the electron donor. This
is similar to the greater yield in cell numbers when mesophilic
Shewanella (
5,
42) and
Geobacter
(
6) species are grown
with organic electron donors rather
than
hydrogen.
This report also provides the first data on the growth of a
hyperthermophilic microorganism with Fe(III) oxide as an electron
acceptor. Such data are important because Fe(III) oxides are likely
to
be the dominant forms of Fe(III) available for microbial reduction
in
most environments (
28). The results presented here
demonstrate
that
P. islandicum readily reduces poorly
crystalline Fe(III)
oxides but that more crystalline Fe(III) oxides are
poorly reduced,
if at all. This result is similar to that observed with
many mesophilic
Fe(III) reducers (
28) and the thermophile
Deferribacter thermophilus (
17). The ability of
P. islandicum to reduce Fe(III) oxide contrasts
with a
thermophilic
Thermus species which only poorly reduced
Fe(III) oxide and did not grow with Fe(III) oxide as the electron
acceptor (
23). However, several other pure cultures of other
thermophilic
Bacteria (
17,
53), as well as
thermophilic enrichment
cultures (
25,
54), have been found
to reduce poorly crystalline
Fe(III)
oxide.
Geochemical implications.
The oxidation of hydrogen and
organic matter coupled to the reduction of Fe(III) oxide carried out by
P. islandicum provides a biological model for important
geochemical reactions on early Earth. As previously reviewed (7,
14, 60), ocean chemistry in the Archaean is likely to have been
dominated by hydrothermal systems and the oldest rocks on Earth contain
evidence for microbial reduction of Fe(III) to magnetite. It has been
proposed (7 and references therein) that prior to
development of life on Earth, there was production of Fe(III) and
hydrogen as high levels of UV radiation impinging on Archaean seas
hydrolyzed the abundant dissolved Fe(II) according to the following
reaction:
hv
2 Fe(II) + 2 H+ 2 Fe(III) + H2
Other potential sources of Fe(III) were Fe(III) emitted in
hydrothermal fluids (
7) and oxidation of Fe(II) by
abiotically
formed nitrogen oxides (
57). Hydrogen was also
available from
other geological sources (
59). Other
potential electron acceptors,
such as oxygen, nitrate, or sulfate, were
probably not abundant
(
8,
13,
61). If this geological
scenario is correct, then
conditions were highly favorable for the
development of a biological
entity that could take advantage of the
energy available from
hydrogen oxidation coupled to Fe(III) reduction.
Thus,
P. islandicum provides a pure-culture model of how
microbial life might have
benefited from environmental conditions on
early Earth, leading
to the massive accumulations of magnetite in the
earliest Banded
Iron
Formations.
The studies with
P. islandicum reported here also suggest
that hyperthermophilic Fe(III)-reducing microorganisms could be
growing
in modern hydrothermal environments. For example, submarine
hydrothermal vents emit high concentrations of dissolved Fe(II),
which
is oxidized in the oxygen-containing seawater, and the resulting
Fe(III) oxides precipitate in the nearby sediments (
20,
21,
52). Hot water percolating through these sediments may provide
appropriate conditions for the growth of Fe(III)-reducing
hyperthermophilic
microorganisms. Similar opportunities for the growth
of hyperthermophilic
Fe(III)-reducing microorganisms may exist near
terrestrial hot-spring
environments (
3).
The ultrafine-grained magnetite produced by
P. islandicum is
similar to the magnetite that has been recovered form the hot,
deep
terrestrial subsurface (
15). It was previously speculated
that the magnetite from the deep terrestrial subsurface was of
microbial origin (
15), but this study with
P. islandicum is
the first demonstration that such magnetite can be
produced during
the growth of a hyperthermophilic microorganism. The
apparent
production of rhodochrosite during Mn(IV) reduction by
P. islandicum provides evidence for the potential of other
minerals to be formed
as the result of microbial metal reduction at
100°C.
The discovery that uranium can be enzymatically reduced at 100°C
increases the known temperature range over which microorganisms
may
have an important influence on uranium geochemistry. Until
the
discovery of microbial U(VI) reduction at mesophilic temperatures,
uranium geochemistry in anaerobic environments was considered
to be
controlled by abiotic processes (
39,
41). However,
studies
on the relative significance of proposed abiotic processes
for U(VI)
reduction versus biological U(VI) reduction have led
to the suggestion
that microbial reductive precipitation of uranium
is an important
factor in geochemically important processes such
as the precipitation
of uranium in marine sediments, the formation
of uranium reduction
spots, and uranium ore accumulations (
39,
41,
43).
Reductive precipitation of uranium at ca. 100°C is known to have led
to the accumulation of important subsurface uranium deposits.
Typical
sandstone-type uranium deposits are considered to have
been formed at
100°C (
18). Another well-known example is the
naturally
generated Oklo nuclear reactor, in which U(VI) dissolved
in
groundwaters of 100 to 150°C was reduced to U(IV), which precipitated
and formed the large uranium accumulations in this environment
(
4). It is probably impossible to determine whether
microorganisms
were responsible for the initial precipitation of
uranium at this
site which took place in the PreCambrian period.
However, the
results presented here suggest that in the modeling of the
formation
of this and other, more recent, uranium deposits formed in a
similar
manner (
12), the possibility that microbial U(VI)
reduction
could be important should be considered. This is further
emphasized
by the finding that the lignite organic matter often
associated
with U(IV) deposits does not abiotically reduce U(VI) at
temperatures
below 120°C (
48).
The ability of
P. islandicum to reduce a variety of other
metals is also of potential significance to the geochemistry of
hydrothermal environments because hydrothermal fluids are typically
enriched in a variety of metals and metalloids. However, the results
indicate that hyperthermophilic microorganisms may not be able
to
reduce all metals and metalloids.
P. islandicum could not
reduce
As(V) or Se(VII). As(V) reduction at 100°C is of interest
because
arsenic can be an important metalloid constituent of
hydrothermal
fluids and arsenic adsorbs onto Fe(III) oxides as they
precipitate
near hydrothermal vents (
52). The inability of
P. islandicum to reduce As(V) is not unexpected, as many
mesophilic Fe(III)-reducing
microorganisms are also incapable of As(V)
reduction. Only one
Fe(III)-reducing microorganism,
Sulfurospirillum barnesii (formerly
strain SES-3), is known
to be capable of growing with As(V) as
the electron acceptor
(
24). The other known As(V)-reducing microorganisms
do not
reduce Fe(III) (
45,
49,
56).
Bioremediation implications.
Many mesophilic Fe(III)-reducing
microorganisms have the potential to reduce toxic metals, converting
them to less-soluble forms which are less mobile in groundwater or can
be precipitated from waste streams or soil washings (30,
32). Thus, microbial metal reduction may be a strategy for in
situ and ex situ remediation of metal contamination. A
Thermus sp. was found to reduce U(VI), Cr(VI), and Co(III)
at 60°C (23), and a fermentative microorganism enhanced
reduction of Cr(VI) and Co(III) at temperatures of up to 65°C
(63). The finding that P. islandicum can reduce
toxic and radioactive metals at 100°C increases the known temperature range at which bioremediation of such metals may be possible.
Subsurface disposal of high-level radioactive waste represents one
instance in which microbial reduction of U(VI), Tc(VII),
and Co(III) at
elevated temperatures could play an important role
in preventing
contaminant mobility. The environment around such
wastes can be
expected to have elevated temperatures (
4), and
thus,
hyperthermophilic metal-reducing microorganisms could help
prevent
migration of these contaminants by reducing them to less
mobile forms.
Hot radioactive or metal-containing industrial wastes
could potentially
be treated in bioreactors containing microorganisms
with a metabolism
like that of
P. islandicum or their
enzymes.
In summary, the results demonstrate that
P. islandicum has
the ability to conserve energy to support growth by using Fe(III)
as a
terminal electron acceptor and has the capacity to transfer
electrons
to a wide variety of other metals. These results expand
the known
temperature range over which dissimilatory metal-reducing
microorganisms may have an important impact on metal geochemistry.
Studies on the distribution and activity of hyperthermophilic
microorganisms in hot environments are warranted to determine
the
geochemical significance of this
metabolism.
| |
ACKNOWLEDGMENTS |
We thank John Lloyd and Betsy Blunt-Harris for technical assistance.
This research was supported by grant DEB-9714285 from the LExEN program
of the National Science Foundation.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Microbiology, University of Massachusetts, 203 Morrill Science Center IV, Amherst, MA 01003. Phone: (413) 545-9651. Fax: (413) 545-1578. E-mail: dlovley{at}microbio.umass.edu.
| |
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Abstract
Introduction
