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Applied and Environmental Microbiology, May 2000, p. 2248-2251, Vol. 66, No. 5
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Lack of Production of Electron-Shuttling Compounds
or Solubilization of Fe(III) during Reduction of Insoluble Fe(III)
Oxide by Geobacter metallireducens
Kelly P.
Nevin and
Derek R.
Lovley*
Department of Microbiology, University of
Massachusetts, Amherst, Massachusetts 01003
Received 20 December 1999/Accepted 2 March 2000
 |
ABSTRACT |
Studies with the dissimilatory Fe(III)-reducing microorganism
Geobacter metallireducens demonstrated that the common
technique of separating Fe(III)-reducing microorganisms and Fe(III)
oxides with semipermeable membranes in order to determine whether the Fe(III) reducers release electron-shuttling compounds and/or Fe(III) chelators is invalid. This raised doubts about the mechanisms for
Fe(III) oxide reduction by this organism. However, several experimental
approaches indicated that G. metallireducens does not
release electron-shuttling compounds and does not significantly solubilize Fe(III) during Fe(III) oxide reduction. These results suggest that G. metallireducens directly reduces insoluble
Fe(III) oxide.
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TEXT |
The mechanisms by which pure
cultures of dissimilatory Fe(III)-reducing microorganisms reduce
insoluble Fe(III) oxides is of interest because this may provide
insights into how Fe(III) oxides are microbially reduced in soils and
sediments. It is generally considered that if Fe(III) chelators or
electron-shuttling compounds are not added to the culture medium, then
Fe(III)-reducing microorganisms must establish direct contact with
Fe(III) oxides to reduce them (11). Circumstantial evidence
consistent with the need for direct contact with Fe(III) oxide is the
visual observation that Fe(III)-reducing microorganisms often seem to
be attached to, or at least closely associated with, Fe(III) oxides
(1, 14, 22). The only experimental evidence that has
appeared to directly support the need for direct contact between
Fe(III)-reducing microorganisms and Fe(III) oxides has come from
studies in which the Fe(III) reducers are physically separated from the
Fe(III) oxides by semipermeable membranes (1, 3, 14, 15, 20,
22). Fe(III) reduction is invariably inhibited. This result has
been interpreted as an indication that pure cultures of Fe(III)
reducers do not release compounds that can solubilize Fe(III) or act as
electron shuttles between Fe(III) reducers and Fe(III) oxides. The
assumption has been that if Fe(III) reducers did release such
compounds, then the compounds would diffuse through the membranes,
permitting Fe(III) reduction without direct contact. However, this
basic assumption does not appear to have been directly tested by
incorporating electron-shuttling compounds or Fe(III) chelators as
positive controls.
This potential shortcoming in previous studies with semipermeable
membranes is significant in view of several recent studies that have
suggested that direct contact between pure cultures of Fe(III) reducers
and Fe(III) oxides is not necessary for Fe(III) oxide reduction.
Selection for cells of Shewanella alga that did not attach
to Fe(III) oxide did not reduce the rate of Fe(III) reduction,
suggesting that attachment was not essential for Fe(III) reduction
(4). Another study suggested that Geobacter
sulfurreducens could reduce Fe(III) oxide by releasing an
extracellular cytochrome that could act as an electron shuttle, thus
eliminating the need for contact with the Fe(III) oxide
(21). Therefore, the validity of the semipermeable-membrane
approach was investigated further.
Potential for electron shuttling through semipermeable
materials.
Unless otherwise specified, G. metallireducens was grown in freshwater medium with acetate (20 mM) as the electron donor and poorly crystalline Fe(III) oxide (100 mmol/liter) as the electron acceptor under an atmosphere of
N2-CO2 (80:20) (14). In order to
evaluate the potential for electron shuttling through dialysis tubing,
the Fe(III) oxide was entrapped in Spectra/Por dialysis tubing
(molecular weight cutoff of 300,000; 18-cm length by 1-cm diameter),
the tubing was rinsed and added to anaerobic sterile medium, and the
culture vessels were aseptically flushed with N2-CO2 for 20 min for 3 consecutive days to
ensure that all of the oxygen was removed. This dialysis tubing was
chosen because it had the largest nominal pore sizes that were readily
available and preliminary studies with tubing with smaller pore sizes
gave comparable results.
When a 5% inoculum of G. metallireducens that had been
grown on acetate-Fe(III) oxide medium was added to medium in which the
Fe(III) oxide was free, G. metallireducens grew in and
reduced the Fe(III), as evidenced by an accumulation of HCl-extractable Fe(II) over time (Fig. 1), as previously
reported (14). In contrast, when the poorly crystalline
Fe(III) oxide was retained within the dialysis membrane, little Fe(II)
was detected outside the membrane. This was true even immediately after
the membranes were ruptured with a needle to release the iron within
(Fig. 1). However, once the Fe(III) was released, it was readily
reduced over time (Fig. 1). This demonstrated that the lack of Fe(III)
reduction in the presence of the membrane was not due to a toxic effect of the membrane on the organism.
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FIG. 1.
Concentrations of HCl-extractable Fe(II) when G. metallireducens was grown in medium with poorly crystalline
Fe(III) oxide as the electron acceptor with no additions or with AQDS
(50 µM) or NTA (4 mM) added. In some instances, the Fe(III) was
retained within a semipermeable membrane and released, as noted. The
results are the means of triplicate incubations for each treatment, in
some cases, symbols may obscure error bars. Symbols:  , free Fe(III)
oxide;  , Fe(III) oxide held within a semipermeable membrane which
was ruptured on day 5;  , Fe(III) oxide membrane ruptured on day
19.
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The addition of anthraquinone-2,6-disulfonate (AQDS; 50 µM) to the
medium stimulated the reduction of the free Fe(III) oxide
by
G. metallireducens (Fig.
1), as expected from previous studies
which
have demonstrated that AQDS serves as an electron shuttle
between
G. metallireducens and Fe(III) oxide (
12,
13).
The
unexpected result was that the addition of AQDS did not result
in
significant reduction of the Fe(III) within the membrane, as
evidenced
by the fact that Fe(II) did not accumulate over time
until after the
membrane had been ruptured (Fig.
2). When
the
membrane was ruptured to release the Fe(III), the Fe(III) was
readily reduced. The finding that AQDS did not promote the reduction
of
Fe(III) in the dialysis membrane in this manner indicates that
separation of Fe(III) oxide and Fe(III)-reducing microorganisms
with a
semipermeable membrane may not be an appropriate method
for evaluating
whether Fe(III)-reducing microorganisms release
electron-shuttling
compounds in order to reduce Fe(III).
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FIG. 2.
Concentration of HCl-extractable Fe(II) when G. metallireducens was grown with synthetic poorly crystalline
Fe(III) oxide entrapped in alginate beads in the presence and absence
of 50 µM AQDS. The results are the means of triplicate incubations
for each treatment. In some cases, symbols may obscure error bars.
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In order to evaluate other potential separation mechanisms to test for
the release of electron-shuttling compounds, poorly
crystalline Fe(III)
oxide was incorporated into microporous alginate
beads with a nominal
molecular mass cutoff of 12 kDa (
5). The
beads (diameter, 5 mm) were prepared as previously described (
2,
5): except
that Fe(III) oxide (500 mmol/liter) was added prior
to the
polymerization step. The amount of Fe(III) exposed on the
surface of
the beads was calculated to be 10% of the total Fe(III)
added, based
on the sizes of the beads and pores and the structure,
shape, and size
of the cross-linked alginate polymer. Beads were
added to
acetate-freshwater medium in order to provide Fe(III)
at 50 mmol/liter.
The production of Fe(II) was determined with
ferrozine (
14)
after the beads had been extracted for 12 h in
0.5 N
HCl.
G. metallireducens could only reduce less than 5 mmol of the
added Fe(III) per liter (Fig.
2), which corresponds to the amount
of
the Fe(III) oxide that is calculated to be exposed on the surface
of
the beads. However, when 50 µM AQDS was included in the medium,
nearly all of the Fe(III) in the beads was reduced. These results
suggest that
G. metallireducens reduced the AQDS to AHQDS,
which
then diffused into the bead, reducing the Fe(III) and
regenerating
AQDS. Each AQDS molecule must have been reduced multiple
times,
as the amount of Fe(III) reduced was ca. 500-fold higher than
the electron-accepting capacity of the added
AQDS.
These results indicate that incorporation of Fe(III) into microporous
beads is a suitable strategy to test for the release
of
low-molecular-weight electron-shuttling compounds. The finding
that
G. metallireducens did not reduce the Fe(III) oxide within
beads in the absence of AQDS suggests that
G. metallireducens does not release low-molecular-weight
electron-shuttling compounds
in order to promote Fe(III) oxide
reduction.
Alternative test for electron-shuttling compounds.
The
microporous beads would not be suitable for testing for the presence of
high-molecular-weight electron-shuttling compounds and might be
inappropriate for some compounds that might bind or otherwise react
with the beads in unknown ways. As an alternative test for
electron-shuttling compounds, the ability of culture filtrate of
G. metallireducens to stimulate reduction of Fe(III) oxide
by a washed cell suspension of G. metallireducens was
evaluated. G. metallireducens was grown on poorly
crystalline Fe(III) oxide (100 mmol/liter) and acetate (20 mM) in
freshwater medium (14). Cells were removed via filtration
(0.2 µm). This filtrate was oxidized by stirring for 1 h,
diluted in various proportions with freshwater medium, and made
anaerobic. Acetate (10 mM), Fe(III) oxide (10 mmol/liter), and a washed
cell suspension of G. metallireducens were added. Over time,
subsamples were taken anaerobically for analysis of HCl-extractable
Fe(II). Filtrates of the culture did not stimulate the reduction of
Fe(III) over the rate that was observed in fresh medium (Fig.
3). This contrasted with a significant stimulation of Fe(III) oxide reduction when only 10 µM AQDS was added. These results further suggest that G. metallireducens
does not release an extracellular electron-shuttling compound in order to reduce Fe(III) oxides, in accordance with other recent studies (10).
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FIG. 3.
Reduction of poorly crystalline Fe(III) oxide by a cell
suspension of G. metallireducens in freshwater medium or
various percentages of filtrate from a G. metallireducens
culture. The results are the means of duplicate incubations for each
treatment.
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Evaluation of the presence of Fe(III)-chelating compounds.
Previous studies have demonstrated that the addition of 4 mM
nitrilotriacetic acid (NTA) solubilizes Fe(III) from Fe(III) oxide and
that this stimulates Fe(III) reduction by G. metallireducens (17, 18). However, the addition of NTA did not promote the reduction of Fe(III) within the semipermeable membrane (Fig. 1). As in
the other studies, the Fe(III) was reduced once it was released from
within the membrane.
In order to determine if incorporation of Fe(III) oxide into
microporous beads would be a suitable strategy to test for the
presence
of Fe(III)-chelating compounds, NTA (4 mM) was added
to cultures in
which Fe(III) oxide was incorporated into the microporous
beads
described above. However, in contrast to the results with
AQDS, the
addition of NTA did not significantly stimulate Fe(III)
reduction (K. Nevin, unpublished data). Studies in which the Fe(III)-containing
beads
were incubated in medium with NTA in the absence of cells
demonstrated
that the chelator only solubilized Fe(III) from the
beads at a rate of
approximately 10 µM/day. This rate of Fe(III)
solubilization was
apparently too slow to sustain the growth and
activity of
G. metallireducens. Thus, incorporation of Fe(III)
oxide into
microporous beads does not appear to be a suitable
strategy for testing
for the release of chelating agents by Fe(III)-reducing
microorganisms.
As an alternative way to evaluate the possibility that
G. metallireducens might solubilize Fe(III) from Fe(III) oxides prior
to Fe(III) reduction, soluble Fe(III) in cultures of
G. metallireducens was measured with ion chromatography in a
anaerobic chamber. All
supplies were placed in an anaerobic chamber for
24 h before use.
The eluent was bubbled with nitrogen for 1 h
and vacuum degassed
for 20 min before use in analysis. Culture
filtrates (0.2-µm-diameter
pore size) were injected into a Dionex
DX-500 Ion chromatograph,
and Fe(II) and Fe(III) were separated on a
Dionex IonPac CS5A
column (
7).
The standard culture medium for the growth of
G. metallireducens (
14) has an NTA-containing trace metal
mixture that adds
59 µM NTA to the medium. Uninoculated medium that
contained the
trace metal mixture contained 1 to 3 µM soluble
Fe(III), whereas
no soluble Fe(III) was detected in medium to which the
trace metal
mixture had not been added. In order to avoid the apparent
solubilization
of Fe(III) by the NTA in the trace metal mixture,
G. metallireducens was grown in a medium in which the
NTA-containing trace metal
mixture was replaced with a trace metal
mixture with NTA omitted.
The growth of
G. metallireducens
was not adversely affected by
the lack of NTA in the trace metal
mixture. Attempts to grow
S. alga strain BrY (
3)
or
Geothrix fermentens (
6) in NTA-free
medium
with Fe(III) oxide as the electron acceptor were unsuccessful,
although
both grew in NTA-free medium with fumarate as the electron
acceptor.
This suggests that, unlike
G. metallireducens, these
two
organisms required the presence of NTA, possibly to solubilize
Fe(III),
to grow on Fe(III)
oxide.
During the growth of
G. metallireducens in NTA-free medium,
the accumulation of HCl-extractable total Fe(II) over time (Fig.
4A) was accompanied by an increase in
soluble Fe(II) (Fig.
4B)
for the first 3 days. After 3 days, soluble
Fe(II) decreased even
though the total Fe(II) increased over this
period. The decline
in soluble Fe(II) is attributed to increased
formation of Fe(II)
minerals such as siderite and magnetite, as
previously reported
(
14,
16). The increase in dissolved
Fe(II) was accompanied
by an apparent increase in soluble Fe(III),
which then decreased
in parallel with the decrease in soluble Fe(II)
(Fig.
4C). However,
when the measurements of soluble Fe(II) and Fe(III)
from this
and similar experiments were plotted together, it was found
that
the measurements of soluble Fe(III) were highly correlated
(
r2 = 0.94) with the measurements of
soluble Fe(II) (Fig.
4D). When
Fe(II) was added to uninoculated culture
medium, there was also
an increase in the measured dissolved Fe(III)
that followed a
similar pattern. These results suggest that the
measurements of
dissolved Fe(III) in the cultures are an artifact of
the analysis.
If Fe(III) was being solubilized as the result of
G. metallireducens releasing an Fe(III) chelator, it would
not be expected that there
should be such a consistent covariance of
dissolved Fe(II) and
Fe(III) concentrations. Furthermore, this would
not explain the
measurement of dissolved Fe(III) when Fe(II) was added
to uninoculated
medium. It may be that Fe(II) can form some type of
defined, soluble
complex with Fe(III), but we are unaware of any such
soluble Fe(II)-Fe(III)
complexes. A more likely explanation is that,
despite the care
taken to maintain anaerobic conditions and the fact
that there
was no evidence for on-column oxidation of Fe(II) standards,
there
was a small consistent oxidation of Fe(II) during the analysis
or
a less than perfect separation of Fe(II) and Fe(III) such that
a very
small fraction of the Fe(II) gave a secondary peak with
a retention
time similar to that of Fe(III). In any event, the
strong covariance of
measured dissolved Fe(III) with Fe(II) indicates
that it is unlikely
that Fe(III) is actually solubilized as the
result of the growth and
activity of
G. metallireducens.
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FIG. 4.
Concentrations of HCl-extractable Fe(II) and soluble
Fe(II) and Fe(III) during the growth of G. metallireducens
on synthetic poorly crystalline Fe(III) oxide in medium without NTA in
the trace metal mixture. The results are the means of duplicate
incubations for each treatment. Panels: A, total HCl-extractable
Fe(II); B, soluble Fe(II); C, soluble Fe(III); D, covariance of Fe(II)
and Fe(III) during the growth of G. metallireducens with
unchelated synthetic, poorly crystalline Fe(III) oxide and with
addition of Fe(II) to uninoculated medium.
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Implications for mechanisms for Fe(III) reduction.
The results
suggest that G. metallireducens does not reduce poorly
crystalline Fe(III) oxide by producing soluble reductants or
electron-shuttling compounds or by solubilizing Fe(III) prior to
reduction. This is the same conclusion that was previously reached on
the basis of studies with semipermeable membranes. However, as shown
here, such studies with semipermeable membranes are not suitable for
testing for the presence of electron-shuttling compounds or Fe(III)
chelators because G. metallireducens did not reduce Fe(III)
within the semipermeable membrane, even when an electron shuttle or
chelator was added to the cultures.
The results do suggest that incorporation of Fe(III) oxide into
alginate beads provides a suitable test for evaluating the
release of
electron-shuttling compounds. One limitation of this
approach is that
the nominal molecular mass cutoff of the beads
(12 kDa) would restrict
the movement of large electron-shuttling
compounds. However, if there
are Fe(III)-reducing microorganisms
that do release electron-shuttling
compounds, it seems probable
that the electron-shuttling compounds
would not be large. The
larger the molecule, the greater the energy
cost for synthesis.
Thus, it would be expected that the most
competitive Fe(III)-reducing
microorganisms would make
electron-shuttling compounds of low
molecular weight, if they produced
any shuttles at
all.
The lack of evidence for the release of electron-shuttling or
Fe(III)-chelating compounds suggests that
G. metallireducens directly transfers electrons to the surface of insoluble Fe(III)
oxides. Both
G. metallireducens (
9) and
G. sulfurreducens (
8,
19) have membrane-bound Fe(III)
reductase activities, and a
cytochrome in the outer membrane of
G. sulfurreducens has recently
been implicated in electron
transfer to insoluble Fe(III) oxides
(J. R. Lloyd and D. R. Lovley, unpublished data). The results
presented here suggest that
further studies on the mechanisms
for electron transfer from the
membrane-bound Fe(III) reductase
components to the Fe(III) oxide
surface are
warranted.
| |
ACKNOWLEDGMENTS |
This research was supported by grants from the NABIR program of the
Department of Energy and the Harbor Processes Program of the Office of
Naval Research.
| |
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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Applied and Environmental Microbiology, May 2000, p. 2248-2251, Vol. 66, No. 5
0099-2240/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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