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Previous Article | Next Article 
Applied and Environmental Microbiology, March 2000, p. 1050-1056, Vol. 66, No. 3
Department of Microbiology, University of
Massachusetts, Amherst, Massachusetts 01003
Received 27 September 1999/Accepted 15 December 1999
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.
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.
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.
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
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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 MnO2 (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 MnO2 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.| |
RESULTS |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
|
|---|
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).
|
|
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).
|
|
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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DISCUSSION |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
|
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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
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 |
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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.
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FOOTNOTES |
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* 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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Top
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Materials and Methods
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Discussion
References
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