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Appl Environ Microbiol, March 1998, p. 1013-1017, Vol. 64, No. 3
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Mercury Methylation and Demethylation in Anoxic
Lake Sediments and by Strictly Anaerobic Bacteria
K.-R.
Pak and
R.
Bartha*
Department of Biochemistry and Microbiology,
Cook College, Rutgers University, New Brunswick, New Jersey
08903-0231
Received 10 October 1997/Accepted 29 December 1997
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ABSTRACT |
After spiking anoxic sediment slurries of three acidic oligotrophic
lakes with either HgCl2 at 1.0 µg/ml or
CH3HgI at 0.1 µg/ml, both mercury methylation and
demethylation rates were measured. High mercury methylation potentials
were accompanied by high demethylation potentials in the same sediment.
These high potentials correlated positively with the concentrations of
organic matter and dissolved sulfate in the sediment and with mercury
levels in fish. Adjustment of the acidic sediment pH to neutrality
failed to influence either the methylation or the demethylation rate of
mercury. The opposing methylation and demethylation processes converged
to establish similar Hg2+-CH3Hg+
equilibria in all three sediments. Because of their metabolic dominance
in anoxic sediments, mercury methylation and demethylation in pure
cultures of sulfidogenic, methanogenic, and acetogenic bacteria were
also measured. Sulfidogens both methylated and demethylated mercury,
but the methanogen tested only catalyzed demethylation and the acetogen
neither methylated nor demethylated mercury.
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INTRODUCTION |
Mercury from nonpoint atmospheric
sources reaches even pristine lakes and, after its biomethylation,
accumulates in fish. This process is especially pronounced in
oligotrophic acidic lakes (19-21). The determination of
mercury levels at or above the 1-µg/g regulatory limit for fish has
led to the introduction of economically damaging sport fishing
restrictions on wide areas of Canada and the midwestern United States
(19). Similar contamination of fish by mercury was recently
reported in the Pine Barrens region of southern New Jersey
(14). The Pine Barrens is a partially wooded, sparsely
populated area straddling the Kirkwood-Cohansee aquifer
(10). Due to its natural and water resources, it enjoys some
measure of ecological protection, and the discovery of mercury contamination of fish in this relatively pristine area was particularly disturbing. No point sources of mercury discharge were identified, and
the mercury contamination is believed to be mainly of atmospheric origin, related to distant incinerators and the burning of fossil fuels. Clearly, the balance of microbial mercury methylation and demethylation activities in the lakes is critical, since only the
hydrophobic methylmercury accumulates in fish to levels that require
regulatory attention (19, 21). Inhibitor experiments clearly
tied the methylation of inorganic mercury in anoxic aquatic sediments
to the activities of certain sulfidogenic bacteria (8, 9,
12). The types of bacteria that demethylate methylmercury in
sediments were found to be more diverse, and their activities could not
be demonstrated unequivocally in pure culture (15). The
factors that influence the balance of the opposing methylation and
demethylation processes and are thus responsible for the overall environmental methylmercury concentrations are as yet insufficiently understood (20, 21). For these reasons, we conducted mercury methylation and demethylation experiments in sediments of some affected Pine Barrens lakes, attempting to correlate these activities with the prevailing environmental parameters, such as sulfate and
sulfide concentrations, pH, and sediment organic matter level. In an
effort to interpret our results, the mercury transformation potentials
of sulfidogenic, methanogenic, and acetogenic bacteria in pure culture
were also reexamined.
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MATERIALS AND METHODS |
Collection, processing, and incubation of sediments.
Sediment cores were collected from lakes in the Pine Barrens area of
southern New Jersey from May to November 1996. Atlantic City Reservoir,
Batsto Lake, and East Creek Lake were selected for sampling because, in
an earlier survey, some fish from these lakes exceeded the 1-µg/g
regulatory limit for mercury (12). The three lakes were
similar in character, all being retained by artificial dams at their
outflow. They are relatively shallow and have mostly sandy sediments
and moderately acidic (pH 5.5 to 6.0) water that is dark because of
humic substances. All three lakes are relatively pristine, being
situated in wooded nonresidential areas, but are accessible by paved
roads. None has received sewage discharges.
The lake sediments were collected at the deepest (3 to 4 m)
portions of the lakes by using a Wildco (Saginaw, Mich.) corer with
acrylic liners. The 5- by 20-cm cores were immediately sealed into
their liners without air pockets, transported to the laboratory, and
placed, within 3 h of collection, in an anaerobic chamber (PACE
6500; Labline Instruments, Melrose Park, Ill.) with an atmosphere of
5% H2, 5% CO2, and 90% N2. All
subsequent operations were performed within this chamber. The sediment
cores were pooled, slurried with deaerated lake water, and passed
through a no. 18 sieve (1-mm-diameter openings) to remove vegetation,
stones, and woody debris. The resulting slurries had approximately 350 mg of sediment per ml. The sediments were divided into two batches. One
batch was adjusted to pH 7.0, using NaOH and an electronic pH meter.
The other batch was left at its original pH. The two batches were
subdivided once more and spiked with either 1.0 of µg
HgCl2 or 0.1 µg of CH3HgI per ml. With
continuous stirring and the use of a tilting repeater dispenser
(Kontes, Vineland, N.J.), 20-ml amounts of the spiked slurries,
containing about 7 g of sediment each, were placed into 50-ml
anaerobic vials. The vials were sealed with butyl rubber stoppers and
aluminum crimp seals. They were subsequently incubated at 27°C,
approximating the maximum summer temperature of the lakes. Abiotic
(autoclaved) sediment controls were included.
Gas samples from the sediment of Atlantic City Reservoir were collected
during the coring process. The gas bubbles rising
from the disturbed
sediment were captured by means of a submerged
inverted funnel.
Connected to the funnel was a 60-ml disposable
plastic syringe (Becton
Dickinson, Franklin Lakes, N.J.) that
could be closed with a stainless
steel valve (Popper & Sons, New
Hyde Park, N.Y.). The captured gas was
drawn into the syringe,
and the valve was closed prior to the
disconnection of the funnel.
The gas sample was analyzed within 24 h of collection.
Pure-culture experiments.
Desulfovibrio desulfuricans
LS was isolated in our laboratory (8). D. desulfuricans ND-132, selected for its high Hg2+
methylation activity, was kindly donated by C. Gilmore (Academy of
Natural Sciences of Philadelphia). The purity of the cultures was
ascertained by repeated single-colony isolations from agar shake
tubes in media B and E (16). The identification of the cultures was verified by their fluorescence under UV illumination (due
to desulfoviridin), their morphology, and their substrate utilization
range (16). Methanococcus maripaludis ATCC 4300 (2) was kindly donated by the laboratory of W. B. Whitman, University of Georgia, Athens. It was maintained and
pregrown for experiments in ATCC medium 1439 (2) under
an atmosphere of 80% H2 and 20% CO2. The
acetogen Eubacterium limosum ATCC 8486 (2) was
kindly donated by the laboratory of L. Young, Rutgers University, New
Brunswick, N.J. It was grown in ATCC medium 1019 under an atmosphere of
30% CO2 and 70% N2. For mercury methylation and demethylation experiments, the sulfidogens were pregrown in low-sulfate medium D with pyruvate as the carbon and energy source (16). The methanogen and the acetogen were grown in their
recommended ATCC media (2). Anaerobic vials (50 ml)
containing 20 ml of the appropriate medium were spiked with either 1.0 µg of HgCl2 or 0.1 µg of CH3HgI per ml,
inoculated at 5% (vol/vol) with 2-day-old precultures, and incubated
at 37°C with slow reciprocal shaking. Methylation and demethylation
experiments were always conducted simultaneously with matched cell
suspensions. Unless an inhibitor was present, the initial inoculum
increased 15- to 20-fold during incubation.
Specific inhibitors of sulfidogens (sodium molybdate, 2 mM) and
methanogens (bromoethane sulfonate [BES], 0.5 mM), employed
in
earlier sediment experiments (
8,
9,
15), were added
in some
of our pure-culture incubations to verify their effects
on mercury
methylation and demethylation. Strict anaerobic processes
were
observed, just as in the sediment experiments. Abiotic (uninoculated)
controls were included.
Analytical procedures.
At appropriate time intervals, the
methylmercury contents of replicate vials were extracted in their
entirety for analysis, using the procedure of Longbottom et al.
(13). This procedure converts all of the methylmercury in
the sample to monomethylmercury. Monomethylmercury is the principal
alkylmercury species present in sediments and fish (21).
Dimethylmercury, if detectable at all, is present only in trace
amounts. Sediment samples were extracted immediately after being
spiked, as well as after appropriate incubation periods. Methylation
and demethylation were stopped by injecting 2.0-ml aliquots of a
1.0 M CuSO4 solution into the serum vials containing sediment slurry or culture suspension. After solvent extraction and cleanup, monomethylmercury levels were measured with
a Hewlett-Packard model 5890 gas chromatograph equipped with a model
AT-35 macrobore capillary column (0.53-mm internal diameter, 15 m
long; Alltech, Deerfield, Ill.). Operating conditions were as
follows: 95:5 Ar-CH4 (vol/vol) carrier gas (Matheson
Gas Products, East Rutherford, N.J.) delivered at 35 ml/min, injector
at 150°C, oven at 100°C, and electron capture detector at 250°C.
Monomethylmercury peak areas (retention time, 1.25 min) were recorded
by a Hewlett-Packard 3392A integrator that had been calibrated with
monomethylmercury (CH3HgI) standards (American Tokyo Kasei,
Inc., Portland, Oreg.). The detection limit for monomethylmercury was 1 ng/ml of sediment slurry or culture suspension.
In sediment experiments, the number of time points analyzed did not
allow the replication of every point, but several time
points in each
experiment were analyzed in triplicate. The standard
deviations for
these time points are shown as error bars in the
figures below. Similar
standard errors need to be assumed for
the nonreplicated time points
that have no error bars. In the
pure-culture experiments, the time
points were not replicated.
The collected gas from the Atlantic City Reservoir sediment was
analyzed for its methane content by using a model 1200 gas
partitioner
(Fisher Co., Springfield, N.J.) operated at 50°C with
30 ml of helium
carrier per min. The sample volumes analyzed were
250 µl, and the
instrument was calibrated with methane gas standards
(Fisher Co.).
Organic matter content was determined as weight loss on ignition
(600°C, overnight) of dried (100°C) sediment samples. Acid-labile
sulfide was determined iodometrically in 50-g (wet weight) sediment
samples (
1). For sulfate measurements, sediments were
vigorously
agitated after addition of an equal volume of distilled
water
and then centrifuged. Sulfate in the clear supernatant was
determined
gravimetrically after precipitation with barium
(
1). Organic-matter
and sulfide concentrations are reported
on a dry-sediment basis,
while the concentration of sulfate, which is
assumed to be in
the dissolved state, is reported per milliliter of
pore water
in the undiluted sediments (see Table
1).
Each experiment was repeated at least once, and results were considered
valid if the time curves were reproduced within the
error limits.
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RESULTS AND DISCUSSION |
Mercury methylation and demethylation in lake sediments.
Lake
sediment characteristics of potential relevance to methylation and
demethylation of mercury are listed in Table
1. Free sulfide was not detectable in the
sediments, and gas bubbles rising to the surface during core sampling
were indicative of methanogenic activity in all three lake sediments.
Gas evolution during coring was particularly abundant in Atlantic City
Reservoir. The gas collected at this location contained 72.4% methane
by volume. The organic matter and sulfate concentrations were the
highest in the Atlantic City Reservoir sediment and somewhat lower in the East Creek Lake and Batsto Lake sediments. The differences in pH
and in acid-labile sulfide values were slight.
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TABLE 1.
Physicochemical characteristics of three Pine Barrens
lakes with relevance to mercury methylation and demethylation
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When the lake sediment slurries were spiked with 1.0 µg of
HgCl
2 per ml and were incubated for 15 days, 15 to 22 ng of
methylmercury
per ml was formed (Fig.
1).
Initial synthesis was rapid and approached
equilibrium after 5 to 10 days. At time zero, only the Atlantic
City Reservoir sediment slurry
contained a detectable amount of
methylmercury (4 ng/ml). When spiked
with 0.1 µg of methylmercury
per ml, the same sediments showed a
rapid decrease in methylmercury
concentration to 16 to 40 ng/ml. Again,
most of this decrease
occurred in the first 5 days of incubation.
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FIG. 1.
Methylation and demethylation of mercury in sediments of
Atlantic City Reservoir (A), Batsto Lake (B), and East Creek Lake (C)
spiked with either 1.0 µg of HgCl2 or 0.10 µg of
CH3HgI per ml. In methylation experiments, triplicate
samples were analyzed on days 0, 5, and 15; in demethylation
experiments, triplicate samples were analyzed on days 0, 10, and 15. The error bars (±1 standard deviation) were omitted when smaller than
the symbols. For the rest of the time points, only single samples were
analyzed, but similar standard errors must be assumed. Note that the
CH3Hg+ concentration scales for the mercury
methylation and demethylation experiments differ.
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Both the mercury methylation and demethylation activities were most
extensive in the Atlantic City Reservoir sediment, where
equilibrium
concentrations of 18 to 22 ng of methylmercury per
ml were attained
during the experimental period, regardless of
the initial spiking
material used. Both the methylation and demethylation
processes were
slightly less extensive in the Batsto Lake and
East Creek Lake
sediments. In these two lakes, a complete methylmercury
concentration equilibrium was not attained during the 15-day
incubation
period, although a trend toward such an equilibrium was
discernable.
The high mercury methylation and demethylation activities
in Atlantic
City Reservoir sediments appeared to correlate positively
with
the level of organic matter in the sediment, the concentration
of
dissolved sulfate in the pore water (Table
1), and the concentration
of
mercury in fish (
14). The parameters and activity levels
in
the other two lakes were too similar to each other to reveal
any trend.
Largemouth bass (
Micropterus salmoides) from Atlantic City
Reservoir were found to contain 3.0 to 8.9 µg of mercury/g, while
the
same species from Batsto Lake contained 0.7 to 1.3 µg/g
(
14).
This fish species was not obtained from East Creek
Lake, but the
chain pickerel (
Esox niger), which occupies a
trophic level similar
to that of the largemouth bass, contained 0.8 to
2.8 µg of mercury/g.
Since practically all of the mercury found in
fish is present
in the form of methylmercury, mercury methylation rates
may be
expected to correlate with elevated mercury levels in fish
(
21).
Previously, the level of organic matter was found to be positively
correlated with mercury methylation activity in estuarine
sediments
(
5), and this correlation appears to exist also in
the case
of the three freshwater lakes investigated here. Virtually
all mercury
methylation in anoxic aquatic sediments has been tied
to the activity
of sulfidogens (
8,
9,
11). Yet, because
of the reaction of
H
2S with Hg
2+ to form HgS, which is virtually
unavailable for methylation,
sulfate concentrations of estuarine
sediments were found to correlate
inversely with mercury methylation
activity (
3,
9). At the
much lower sulfate concentrations of
freshwater lakes, addition
of sulfate to the 200 mM level was found to
stimulate Hg
2+ methylation (
11,
12). The sulfate
concentrations measured
by us in the Pine Barrens lakes were only
slightly higher, and
thus a positive correlation of sulfate levels with
mercury methylation
in these lakes was not unexpected.
Because of the known association of low pH with mercury accumulation in
fish (
21), the effects of pH on the balance of mercury
methylation and demethylation were the subject of several studies.
Ramlal et al. (
17) and Steffan et al. (
18) found
that demethylation
was relatively insensitive to pH changes but that
acidification
of the anoxic lake sediments to pH 5.0 or lower
essentially stopped
methylmercury synthesis. The authors demonstrated a
decrease in
Hg
2+ availability for methylation in the
acidified sediments. The
postulated mechanisms were HgS formation by
acid-mobilized H
2S
and increased Hg
2+
adsorption. Of course, these results did not explain the accumulation
of mercury in fish at low pH.
The unresolved state of the pH effect on the balance of mercury
methylation and demethylation prompted us to reexamine this
question by
using Pine Barrens lake sediments. To avoid the possibility
of
H
2S mobilization, we adjusted the naturally acidic (pH 5.5
to 6.0) lake sediments upward only to pH 7.0. Neither methylation
nor
demethylation rates were affected by this modest pH adjustment
(Fig.
1). Our results confirm the opinion (
17,
18,
21) that
mercury accumulation in fish at low pH is not caused directly
by
stimulation of the methylation or inhibition of the demethylation
process.
Methylation and demethylation of mercury by pure cultures of
strictly anaerobic sediment bacteria.
Historically, the
identification of sediment bacteria responsible for mercury
methylation and demethylation followed a two-step process.
Sediments were treated with a selective inhibitor of sulfate
reduction (molybdate) or methanogenesis (BES), and the effects of these
treatments on mercury methylation or demethylation were measured.
Subsequently, pure cultures of the purportedly involved bacteria were
isolated and their mercury methylation or demethylation potentials were
confirmed. This approach tied over 95% of the mercury methylation in
anoxic sediments to the activities of sulfidogens (8, 9),
and the process was verified in pure cultures of D. desulfuricans (8). By a similar approach, Oremland et
al. (15) investigated bacterial populations involved in
demethylation of monomethylmercury. On the basis of inhibition experiments, they concluded that in anoxic freshwater sediments, both
methanogens and sulfidogens participated in methylmercury demethylation, but in estuarine and hypersaline sediments, only the
contributions of sulfidogens were significant. However, these authors
had little success in verifying methylmercury demethylation in pure
cultures of sulfidogens and methanogens. While their sediment samples
typically decomposed 35 to 70% of the added methylmercury, their pure
cultures decomposed less than 3% of the radiolabeled methylmercury,
which contained 2% radiochemical impurities. Assuming that these
inconclusive results were due to culture selection or test conditions,
we embarked on reexamining the ability of strict anaerobes to decompose
methylmercury in pure culture.
Figure
2 shows mercury methylation and
demethylation in pure cultures of
D. desulfuricans LS.
Intentionally presented on the
same scale as the sediment experiments
of Fig.
1, a comparison
shows that the mercury methylation and
demethylation activities
of this sulfidogen very closely resemble those
measured in lake
sediments. The addition of 2 mM molybdate
completely inhibited
both the methylation and demethylation
activities, supporting
the results of specific-inhibitor approaches
used in earlier sediment
experiments (
8,
9,
15). A
comparison of the relative mercury
methylation and
demethylation rates of
D. desulfuricans LS with
those of
D. desulfuricans ND 138 (data not shown) indicated
that
these activities may vary independently. While the demethylation
activity of
D. desulfuricans ND 138 was almost identical to
that
of
D. desulfuricans LS, the mercury methylation
activity of the
former was four times higher than that of strain LS. It
is relevant
that
D. desulfuricans ND 138 was selected from
numerous isolates
for its high net methylmercury synthesis activity.
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FIG. 2.
Methylation and demethylation of
mercury in pure cultures of D. desulfuricans LS
spiked with either 1.0 µg of HgCl2 or 0.10 µg of
CH3HgI per ml ( ), and the same in the presence of 2.0 mM
sodium molybdate ( ). For ease of comparison, the presentation
matches the sediment experiments of Fig. 1 except for the time
scale.
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Figure
3 shows that
M. maripaludis was unable to methylate inorganic mercury but
demethylated methylmercury at a rate comparable
to that of the
sulfidogens. The presence of 0.5 mM BES completely
stopped
demethylation, again supporting the outcome of earlier
sediment work with specific inhibitors (
15).
E. limosum, an
acetogen, was unable to either methylate or
demethylate mercury.
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FIG. 3.
Methylation and demethylation of
mercury in pure cultures of M. maripaludis spiked
with either 1.0 µg of HgCl2 () or 0.1 µg of
CH3HgI () per ml, and demethylation of
mercury by M. maripaludis in the presence of 0.5 mM BES
( ). The methylation and demethylation time curves of
E. limosum (not shown) were identical to those of
HgCl2 and BES, respectively.
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|
Although earlier specific-inhibitor experiments have implicated
sulfidogens and methanogens as being demethylators of
methylmercury
in sediments (
15), the present study has
led to the first conclusive
report of methylmercury
demethylation in pure cultures of these
obligate
anaerobes. It provides a necessary confirmation of the
methylmercury
demethylation potential attributed to these
microorganisms
in their anoxic-sediment environments. Oremland et al.
(
15)
successfully reproduced methylmercury
demethylation by pure cultures
of facultative
anaerobes such as
Escherichia coli. Such microorganisms,
which were active mainly in aerobic sediments, evolved
14CH
4 from
14CH
3Hg
+, but little evolution of
14CH
4 was measured in either freshwater or
estuarine sediments under
anoxic incubation conditions (
15).
In anoxic sediments, the
principal gaseous product of
14CH
3Hg
+ decomposition was
14CO
2, leading the authors to question the
identity of the biochemical
oxidative pathway which converts
the methyl groups of monomethylmercury
to carbon dioxide
(
15).
In our laboratory, the
D. desulfuricans LS mercury
methylation process was shown to be enzymatically catalyzed
(
6), with
methylcobalamin serving as the methyl donor
(
4), and the acetyl
coenzyme A synthase reaction was
implicated in Hg
2+ methylation (
7). Running
forward, this reaction seems to generate
CH
3Hg
+
as an incidental side product. Running backward, the same reaction
could release the methyl carbon as CO
2. This proposition,
while
clearly only a hypothesis, is consistent with the results of
Oremland
et al. (
15) concerning the participation of
sulfidogens and
methanogens as principal demethylators of methylmercury
in anoxic
sediments and also accounts for CO
2 being the
major product of
methylmercury demethylation in such
environments.
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ACKNOWLEDGMENTS |
We thank C. Gilmore (Academy of Natural Sciences of Philadelphia)
for the culture of D. desulfuricans ND-132 and L. Young (Agbiotech Center, Rutgers University) for E. limosum and
for the use of her gas partitioner for methane analysis. Our special thanks are expressed to R. England and B. Ruppert of the New Jersey Department of Environmental Protection for generously devoting time and
facilities to our sediment collection needs.
This work was supported by the New Jersey Department of Environmental
Protection, by the New Jersey Water Resources Institute, and by state
funds.
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FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Biochemistry and Microbiology, Lipman Hall, Room 322, Cook College,
Rutgers University, P.O. Box 231, New Brunswick, NJ 08903-0231. Phone: (732) 932-9763, ext. 322. Fax: (732) 932-8965.
New Jersey Agricultural Experiment Station publication no.
D-01408-01-97.
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Abstract
Introduction
