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Applied and Environmental Microbiology, February 2001, p. 769-773, Vol. 67, No. 2
0099-2240/01/$04.00+0 DOI: 10.1128/AEM.67.2.769-773.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Mobilization of Selenite by Ralstonia
metallidurans CH34
Murielle
Roux,1
Géraldine
Sarret,2
Isabelle
Pignot-Paintrand,3
Marc
Fontecave,1 and
Jacques
Coves1,*
Laboratoire de Chimie et Biochimie des
Centres Redox Biologiques, CEA-Grenoble, DBMS/CB-CNRS-Université
Joseph Fourier,1 and Atelier de
Microscopie Electronique, IFR 27 INSERM,
CEA-Grenoble,3 38054 Grenoble Cedex 9, and
Laboratoire de Géophysique Interne et Tectonophysique,
Université Joseph Fourier, 38041 Grenoble
Cedex,2 France
Received 3 August 2000/Accepted 22 November 2000
 |
ABSTRACT |
Ralstonia metallidurans CH34 (formerly
Alcaligenes eutrophus CH34) is a soil bacterium
characteristic of metal-contaminated biotopes, as it is able to grow in
the presence of a variety of heavy metals. R. metallidurans
CH34 is reported now to resist up to 6 mM selenite and to reduce
selenite to elemental red selenium as shown by extended X-ray
absorption fine-structure analysis. Growth kinetics analysis suggests
an adaptation of the cells to the selenite stress during the lag-phase
period. Depending on the culture conditions, the medium can be
completely depleted of selenite. Selenium accumulates essentially in
the cytoplasm as judged from electron microscopy and energy-dispersive
X-ray analysis. Elemental selenium, highly insoluble, represents a
nontoxic storage form for the bacterium. The ability of R. metallidurans CH34 to reduce large amounts of selenite may be of
interest for bioremediation processes targeting selenite-polluted sites.
| |
INTRODUCTION |
In aerated environments, selenium
can exist in several redox forms, including the elemental form, Se(0),
which is a solid, and the oxidized forms, selenite
(SeO32
) and selenate
(SeO42), which are bioavailable, mobile, and
toxic for many organisms (5). Selenium is widely
distributed in virtually all materials of the earth's crust, but
accumulation of toxic compounds of selenium can also have an
anthropogenic source. Selenium and its derivatives are widely used in
industrial products, and the problem of selenium accumulation remains
in mind after the ecological disaster of Kesterson National Wildlife
Refuge, in California, due to agricultural drainage released in the
Kesterson Reservoir (19). Since microorganisms are
involved in the geochemical cycle of selenium, soil bacteria may thus
be used in bioremediation processes. Some of them are able to resist
high concentrations of a variety of metals and oxyanions
(16), and the reduction of selenite to selenium by the
common aerobic soil bacterium Bacillus subtilis
(10) or the phototrophic purple nonsulfur bacterium
Rhodospirillum rubrum (12) has been reported.
The accumulation of selenium by Rhodobacter sphaeroides has
been also reported very recently (23).
Ralstonia metallidurans CH34 (formerly Alcaligenes
eutrophus CH34) is a microorganism characteristic of
metal-contaminated biotopes (14). It has been previously
demonstrated to have detoxification pathways for a broad range of
metals, as it bears two megaplasmids controlling resistance against
Cd2+, Co2+, Zn2+, Tl2+,
Cu2+, Pb2+, Ni2+, Hg2+,
and CrO42. Resistance is due mainly to
plasmid-mediated efflux followed by postefflux events such as
bioprecipitation or biological sequestration (1, 7). In
this report, the ability of R. metallidurans CH34 to resist
also selenite is described for the first time. The physiological and
morphological changes resulting from the presence of selenite in the
culture medium were studied by using direct chemical assay for
selenite, electron microscopy, and electron-dispersive X-ray analysis.
The speciation of selenium was determined by X-ray absorption
spectroscopy techniques.
| |
MATERIALS AND METHODS |
Strain and growth media.
R. metallidurans CH34 was
grown under aerobic conditions at 29°C in the minimal mineral medium
described in reference 15. As this medium is buffered with
Tris, it is called Tris salt medium (TSM) herein. As previously
described (15), TSM was supplemented with the trace
element solution SL7 (2) and ferric ammonium citrate.
Gluconate was used as a carbon source at a 0.2% final concentration
for routine experiments. When high concentrations of cells were
required, TSM was supplemented with 1% gluconate. For the
determination of the selenite MIC, solid TSM-agar containing increasing
amounts of selenite was used. Colonies were counted after 5 days at
29°C.
Electron microscopy and EDX analysis.
Cells were first fixed
at room temperature in 2.5% glutaraldehyde in 0.1 M cacodylate buffer
(pH 7.2) for 60 min and then washed three times with the same
cacodylate buffer. The cell pellets were fixed for 60 min at 4°C in
1% OsO4 in cacodylate buffer before being dehydrated with
ethanol and embedded in Epon. Sections were realized with an
ultramicrotome (model S; Leica) equipped with a diamond knife. Uranyl
acetate and lead citrate were used as contrast agents. Observations
were done with an electron microscope (JEOL 1200EXII) working at 80 kV.
Energy-dispersive X-ray (EDX) analysis was performed on the same grids
with a scanning transmission electron microscope (JEOL 2000FX) working
at 200 kV and equipped with a Princeton Gamma-Tech analysis system.
X-ray absorption spectroscopy.
Selenium K-edge X-ray
absorption experiments were performed on the BM32 beamline at the
European Synchrotron Radiation Facility. Reference compounds including
hexagonal (i.e., gray) Se for Se(0), Na2SeO3
for Se(IV), and Na2SeO4 for Se(VI) were diluted
with inert BrN, and the mixture was pressed into 13-mm-diameter
pellets. The bacterial material was recorded in both the fresh and
freeze-dried states. Freeze-dried bacteria were ground in an agate
mortar and pressed into 13-mm-diameter pellets. Fresh bacteria were
loaded into a 7-mm-thick liquid sample holder, and the spectrum was
recorded immediately. All the spectra were recorded at room temperature in transmission mode. The acquisition time was about 45 min per spectrum. X-ray absorption near-edge structure (XANES) and extended X-ray absorption fine-structure (EXAFS) data extraction and analysis were performed using the WinXAS code (18). Normalized,
background-subtracted EXAFS spectra 
, expressed as a function of the
electron wave vector k, were multiplied by
k3 and Fourier transformed using a Bessel
window. The structural parameters for the first atomic shell around Se
(see Fig. 4) were determined by numerical simulation of the first-shell
contribution in the real space (in angstroms) and in the reciprocal
space (per angstrom) using theoretical FEFF (17) functions
calculated from the structure of hexagonal Se (11). The
parameters S02 (scaling factor) and
E0 (difference in threshold energy between theoretical reference functions and experimental spectra) were determined by simulation of the hexagonal Se spectrum and were fixed
for the simulation of the unknown spectrum. Errors, estimated for an
increase of the residual Q
(
{[k3(k)exp 
k3(k)theo]/k3(k)exp})
to 2Q, were 0.01 Å for R and 15% for
N.
Selenite content determination.
Selenite concentration was
determined by means of the absorbance at 377 nm of a
selenium-2,3-diaminonaphthalene complex in cyclohexane as described in
reference 12.
| |
RESULTS |
Resistance of R. metallidurans CH34 to selenite
stress.
Quantitative selenite susceptibility tests were performed
by culture on solid TSM-agar containing increasing concentrations of
selenite. The number of colonies was determined after 5 days of growth
at 29°C and did not vary during 5 additional days. The MIC, defined
as the lowest concentration of inhibitor preventing growth, was found
to be about 6 mM selenite under these conditions. During growth in the
presence of less than 6 mM selenite, all the colonies turned red, with
some delays occurring from one colony to another.
Figure 1 shows a typical growth curve of
R. metallidurans CH34 in TSM at 29°C. A lag phase of about
15 h was observed before the exponential growth phase. The lag
time increased when selenite was added to the culture medium (Fig. 1),
and this increase was a function of the selenite concentration (not
shown). This behavior was independent of the gluconate concentration.
On the other hand, during the exponential phase, bacteria in
selenite-complemented media grew at rates comparable to those of
bacteria grown in selenite-free media. Furthermore, maximal densities
were very similar whether or not selenite was present in the culture
medium. In order to know whether this capacity to resist selenite was
due to an adaptation to the environmental conditions during the lag
phase rather than a mutation, cells grown in the presence of 1 or 2 mM
selenite were plated on solid TSM-agar in the absence of selenite. Then the resulting colonies were grown again in the presence or in the
absence of selenite. The duration of the lag phase was still a function
of the selenite concentration, as described above. This result showed
that R. metallidurans CH34 adapted its metabolism to
selenite stress during the lag phase and strongly suggests that this
adaptation was not the consequence of a mutation.
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FIG. 1.
Time course of growth (filled symbols) and selenite
disappearance (open symbols) in R. metallidurans CH34. Cells
were grown in mineral medium containing 1% gluconate in the absence
( ) or in the presence ( ) of 2 mM selenite. Selenite (2 mM) was
added at zero time ( ) or, for the cultures inoculated in the absence
of selenite, at an absorbance at 600 nm of 0.7 ( ), 1.5 ( ), or 3.2 ( ). Arrows indicate when selenite was added.
|
|
The medium can be completely depleted of selenite.
Liquid TSM
containing 2 mM selenite was first inoculated with R. metallidurans CH34. Then the concentration of selenite in the
medium and cell growth were monitored as a function of time. The
decrease in selenite concentration started only at the end of the
exponential phase (A600 > 3) and then
accelerated during the transition between the exponential phase and the
stationary phase. The medium was then completely depleted of selenite
during the stationary phase (Fig. 1). In another experiment, 2 mM
selenite was added at different times during the exponential phase to
cell cultures initiated in the absence of selenite. The decrease in selenite concentration was again measured as a function of time (Fig.
1). In all cases, independently of the cell density at the moment of
the addition, introduction of 2 mM selenite had no or only a minor
effect on the cell growth rate (not shown) and the totality of the
selenite was removed from the medium once the stationary phase was
reached. The depletion rate of selenite from the culture medium seems
to be related mainly to the cell density. During the first two hours,
the concentration of selenite decreased by 0.23, 0.18, or 0.06 mM when
2 mM selenite was added at an absorbance of 3.2, 1.5, or 0.7, respectively. Moreover, when R. metallidurans CH34 was grown
in the presence of 0.2% gluconate and 2 mM selenite, the stationary
phase was reached with an absorbance at 600 nm of about 1 to 1.2 and
without a significant evolution of the selenite concentration (not
shown). The cell density was not high enough to allow an efficient
reduction of the selenite.
Finally, the decrease in selenite concentration was correlated with a
reddening of the cell suspension, suggesting an uptake
of the oxyanion
and its reduction to elemental
selenium.
The red color is due to the accumulation of elemental
selenium.
Cultures in liquid medium containing 1% gluconate as
the carbon source reached an absorbance at 600 nm of 4 to 5 and turned red during the transition between the exponential phase and the stationary phase. When red cultures were centrifuged, the coloration appeared to be associated with the cell pellet and the supernatant was
clear and colorless. Washing the cells did not remove the red color.
Electron microscopy allows the detection of electron-dense particles in
cells grown in the presence of selenite. Round bodies
were found
essentially in the cytoplasm (Fig.
2). It
was also
possible to observe these particles in the periplasm and very
rarely in both locations (not shown). In most cases, the dense
particles seemed to be associated with or close to a membrane
system,
but electron-dense granules were also observed without
any contact with
membranes. In some minor cases, dense deposits
were observed in the
culture medium, probably coming from dead
or damaged cells. However,
spoiled cells or cell-like structures
lacking internal organization
were very rarely observed. Finally
and still more scarcely, it was also
possible to observe multiple
dense bodies, apparently associated with
the exterior of the external
membrane. The presence of selenium in the
electron-dense particles
was unambiguously identified by EDX analysis
as the specific absorption
peaks at 1.37, 11.22, and 12.49 keV were
recorded (Fig.
2).
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FIG. 2.
EDX analysis of the electron-dense body contained in an
R. metallidurans CH34 cell grown in the presence of 2 mM
selenite. The emission lines specific for selenium are identified as
SeL (1.37 keV), SeK (11.22 keV), and SeK (12.49 keV).
|
|
The exact chemical form of selenium in
R. metallidurans CH34
was determined by Se K-edge XANES and EXAFS spectroscopies. XANES
and
EXAFS spectra for the fresh and freeze-dried material were
very similar
(Fig.
3) and strongly suggested that
Se(IV) initially
present in the growing culture was transformed into
Se(0). However,
the radial-structure functions for gray Se taken as a
model compound
and freeze-dried bacteria were very different (Fig.
4), thus suggesting
that the red form was
predominant. The structural parameters for
the first atomic shell of Se
in gray hexagonal Se and in the bacteria
were determined by numerical
simulation of the Fourier filtered
EXAFS spectra. The Se local
structure was composed of 2 ± 0.3
Se atoms at 2.37 ± 0.01 Å in hexagonal Se and of 1.8 ± 0.3 Se
atoms at 2.34 ± 0.01 Å in
R. metallidurans CH34. The Se-to-Se
distance for the
bacteria matches the crystallographic values
of red Se (
4,
9,
13) and not that of gray Se. Simulations
of the bacterial
spectrum by a C, O, N, or S shell were completely
out of fit, so the
presence of organic selenium such as selenium-containing
amino acids or
organic acids could be ruled out. Thus, EXAFS results
allow us to
conclude that the metal is present as red Se(0) in
the bacteria.
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FIG. 3.
Se K-edge XANES spectra (A) and Se K-edge EXAFS spectra
(B) for selenate [Se(VI)], selenite [Se(IV)], gray selenium
[Se(O)], and freeze-dried and fresh bacteria. a.u., arbitrary
units.
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FIG. 4.
Numerical simulation of the Fourier filtered
contribution of the first Se atomic shell for gray Se (A) and
freeze-dried bacteria (B), which allows the determinations of the
Se-to-Se interatomic distance R (in angstroms), of the
coordination number N, and of the Debye-Waller factor
 2 (in square angstroms), which accounts for the thermal
and static disorder. R, N, and 2
values obtained are 2.37 Å, 2 Se atoms, and 0.0040 Å2 for
hexagonal Se and 2.34 Å, 1.8 Se atoms, and 0.0040 Å2 for
R. metallidurans CH34. exp., experimental.
|
|
| |
DISCUSSION |
R. metallidurans CH34 has been found in the metal-rich
sediments of a zinc factory in Belgium and has been demonstrated to prevail in industrial anthropogenic biotopes such as metallurgic wastes
(14, 15). It harbors plasmid-borne multiple resistance to
heavy metals and oxyanions. This report describes a new capacity of
resistance for this strain as it is here demonstrated to resist up to 5 to 6 mM selenite when it is cultured in solid minimal mineral medium.
This value must be compared to the MICs determined for other naturally
occurring phototrophic and telluric species such as Rhodobacter
sphaeroides, Rhodospirillum rubrum, and B. subtilis, which range from about 2 to 5 mM depending on the growth conditions (10, 12, 16). R. metallidurans CH34
is thus highly resistant to selenite.
Among the different mechanisms of metal resistance, cation efflux is
widely represented (21, 22). However, in the case of
selenite, a reduction process seems to be involved. This process leads
to accumulation of elemental selenium as electron-dense round bodies
within the cells. X-ray absorption spectroscopy is particularly adapted
to determine the chemical forms of metals in natural and biological
systems without any sample pretreatment (20). Both XANES
and EXAFS analyses were previously used to monitor the reduction of
Se(IV) into Se(0) by B. subtilis (3). In that
study, XANES analysis allowed the identification of elemental selenium
whereas EXAFS analysis failed to distinguish between the gray and the
red forms, as the interatomic distances determined for red and gray
Se(0) did not correspond to crystallographic values. Only XANES
analysis was used in a very recent study addressing the fate of
selenate and selenite metabolized by R. sphaeroides (23). In the present study, EXAFS analysis was used to
provide evidence for the accumulation of red selenium in R. metallidurans CH34 cells. EXAFS spectra can be simulated using ab
initio calculations and allow determination of structural parameters
such as the nature and the number of neighboring atoms around Se and
the interatomic distances. The values deduced from the experiment with
bacteria and from the calculations fit perfectly those determined for
the different crystallographic forms of red selenium (4, 9, 13).
Most of the time, only one electron-dense particle of selenium per cell
was visible. The location of elemental selenium was mostly in the
cytoplasm, either close or not close to the inner membrane system. In
some cases, an electron-dense particle was found in the periplasm. As
it is difficult to imagine that such large particles can be transported
across the inner membrane and as we never observed a vesicular
mechanism of excretion, we suggest that selenite can be reduced either
in the periplasm or in the cytoplasm and that elemental selenium
accumulates where it is produced. As selenium is in a redox state of
(+IV) in selenite and of (II) in biomolecules or (0) in elemental
selenium, the question of the nature and of the specificity of the
reduction system arises. The chemical basis for the reduction of
selenite to selenium is largely unknown and is now under investigation.
R. metallidurans CH34 has already been used, at least at an
experimental level, in bioremediation processes leading to removal of
heavy metals from soil or liquid waste (6, 8, 14). As a
result of its insolubility, elemental selenium becomes essentially not
bioavailable and nontoxic. Thus, the finding that R. metallidurans CH34 can also resist selenite by reducing it to and
accumulating it as selenium granules makes this microorganism also a
candidate for the restoration of selenite-polluted biotopes.
| |
ACKNOWLEDGMENTS |
Thanks are due to Ariane Toussaint and Christophe Merlin for
fruitful discussions and advice. We have to acknowledge Laure Guétaz for EDX measurements and Jean-Louis Hazemann and Alain Manceau for their contribution to X-ray spectroscopies. Special thanks
go to Max Mergeay for introducing us to R. metallidurans CH34 and for constant friendly encouragement.
The research of M.R. has been made possible by the financial support of
the Agence de l'Environnement et de la Maîtrise de l'Energie
and the Commissariat à l'Energie Atomique.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Laboratoire de
Chimie et Biochimie des Centres Redox Biologiques, CEA-Grenoble,
DBMS/CB-CNRS-Université Joseph Fourier, 38054 Grenoble Cedex 9, France. Phone: 33-(0)4-76-88-91-22. Fax: 33-(0)4-76-88-91-24. E-mail:
jcoves{at}cea.fr.
| |
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Applied and Environmental Microbiology, February 2001, p. 769-773, Vol. 67, No. 2
0099-2240/01/$04.00+0 DOI: 10.1128/AEM.67.2.769-773.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
