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Applied and Environmental Microbiology, August 1998, p. 2966-2969, Vol. 64, No. 8
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Microbial Dechlorination of
2,3,5,6-Tetrachlorobiphenyl under Anaerobic Conditions in the Absence
of Soil or Sediment
Leah
Cutter,1
Kevin R.
Sowers,2 and
Harold D.
May1,*
Department of Microbiology and Immunology,
Medical University of South Carolina, Charleston, South
Carolina,1 and
Center of Marine
Biotechnology, University of Maryland Biotechnology Institute,
Baltimore, Maryland2
Received 23 January 1998/Accepted 22 May 1998
 |
ABSTRACT |
Bacterial enrichment cultures developed with Baltimore Harbor (BH)
sediments were found to reductively dechlorinate
2,3,5,6-tetrachlorobiphenyl (2,3,5,6-CB) when incubated in a minimal
estuarine medium containing short-chain fatty acids under anaerobic
conditions with and without the addition of sediment. Primary
enrichment cultures formed both meta and ortho
dechlorination products from 2,3,5,6-CB. The lag time preceding
dechlorination decreased from 30 to less than 20 days as the cultures
were sequentially transferred into estuarine medium containing dried,
sterile BH sediment. In addition, only ortho dechlorination
was observed following transfer of the cultures. Sequential transfer
into medium without added sediment also resulted in the development of
a strict ortho-dechlorinating culture following a lag of
more than 100 days. Upon further transfer into the minimal medium
without sediment, the lag time decreased to less than 50 days. At this
stage all cultures, regardless of the presence of sediment, would
produce 2,3,5-CB and 3,5-CB from 2,3,5,6-CB. The strict
ortho-dechlorinating activity in the sediment-free cultures has remained stable for more than 1 year through several
transfers. These results reveal that the classical microbial enrichment
technique using a minimal medium with a single polychlorinated biphenyl (PCB) congener selected for ortho dechlorination of
2,3,5,6-CB. Furthermore, this is the first report of sustained
anaerobic PCB dechlorination in the complete absence of soil or
sediment.
| |
INTRODUCTION |
Anaerobic dechlorination of
polychlorinated biphenyls (PCBs) has been demonstrated in situ and with
laboratory microcosms containing sediment (reviewed in reference
1a). However, sustained PCB dechlorination has never
been shown to occur in the absence of soil or sediments. Morris et al.
(6) demonstrated a sediment requirement for the stimulation
of PCB dechlorination within freshwater sediment slurries. Wu and
Wiegel have recently described PCB-dechlorinating enrichments which
required soil for the successful transfer of PCB-dechlorinating
activity (9). In addition, no anaerobic microorganisms that
dechlorinate PCBs have been isolated or characterized, and this may be
due in part to the soil or sediment requirement. The inability to
isolate dechlorinating organisms or maintain dechlorination without
sediment has limited biogeochemical and physiological investigations
into the mechanisms of PCB dechlorination.
Dechlorination (ortho, meta, and para)
of single PCB congeners has been observed following anaerobic
incubation of Baltimore Harbor (BH) sediment under estuarine or marine
conditions (2). While sediments from several sites within BH
are contaminated with PCBs (1, 5), background contamination
of sediment is not necessarily a prerequisite for the development of
PCB dechlorination in laboratory microcosms. Wu et al. (8)
recently demonstrated meta and ortho
dechlorination of Aroclor 1260 when it was added to the same BH
sediments. These results showed that more than one dechlorinating
activity could be developed with these sediments. It has been proposed
that discrete microbial populations are responsible for specific PCB
dechlorinations (1a). Consistent with this idea, the
ortho dechlorination observed with BH sediments may be
catalyzed by discrete microbial populations. In addition, these organisms may be able to couple PCB dechlorination with growth. Therefore we have attempted to select for ortho
PCB-dechlorinating organisms by enrichment under minimal
conditions with high levels of 2,3,5,6-tetrachlorobiphenyl. We also
speculated that given the proper conditions, a PCB-dechlorinating
population could be maintained in an actively dechlorinating state in
the absence of sediment. Here we report that a distinct
PCB-dechlorinating activity, namely, ortho dechlorination,
was selected for through sequential transfer initiated with sediments
from BH and sustained in the absence of soil or sediment. This is the
first report of sustained anaerobic PCB-dechlorinating activity
in the total absence of sediment.
| |
MATERIALS AND METHODS |
Sediment samples.
Sediment samples were collected with a
petite Ponar grab sampler from a subsurface depth of 9.1 m in the
northwest branch of BH (39°16.8'N, 76°36.1'W). An oily slick and
gas bubbles formed at the surface immediately after the sampler
disturbed the sediments. Sediments had a black coloration, a gelatinous
texture, and a strong petroleum odor. The combined contents of the
sampler were transferred to 0.95-liter canning jars (Ball Corporation,
El Paso, Tex.). The jars were filled to the top and immediately sealed with dome tops and ring seals to exclude air. The samples were stored
at ambient temperature in the dark prior to use.
Culture conditions.
All sterile media in these experiments
included an estuarine salts medium without sulfate (E-Cl) and were
prepared anaerobically in an atmosphere that contained
N2-CO2 (4:1) as previously described by Berkaw
et al. (2). Briefly, the medium contained the following constituents, in grams per liter of demineralized water:
Na2CO3, 3.0; Na2HPO4,
0.6; NH4Cl, 0.5; cysteine-HCl · H2O,
0.25; Na2S · 9H2O, 0.25;
MgCl2 · 6H2O, 0.1;
CaCl2 · 6H2O, 0.1; and resazurin, 0.001. In addition, vitamin and trace element solutions (1% [vol/vol] each)
were added (7). The final pH of the medium was 6.8. Media were dispensed into anaerobic culture tubes (18 by 160 mm; Bellco Glass, Inc., Vineland, N.J.) or 150-ml serum bottles (Wheaton, Millville, N.J.) sealed with Teflon-lined butyl stoppers (The West Co.,
Lionville, Pa.) that were secured with aluminum crimp seals (Wheaton).
Primary sediment enrichment cultures were generated in culture tubes by
adding 2 ml of BH sediment to 8 ml of sterile E-Cl medium
(approximately 5%, wt/vol [dry weight], sediment concentration), plus a mixture of sodium acetate, propionate, and butyrate to final
concentrations of 2.5 mM each. Congener 2,3,5,6-tetrachlorobiphenyl (2,3,5,6-CB) was solubilized in acetone and added to each culture to a
final concentration of 173 µM (50 ppm), and this resulted in a 0.1%
(vol/vol) concentration of acetone. Cultures were incubated under
strict anaerobic conditions at 30°C in the dark. Killed-cell controls
were sterilized in an autoclave at 121°C for a total of 3 h (two
1.5-h treatments). Sequential transfers of sediment-containing cultures
were made as follows. The entire sediment-containing culture was made
into a suspension by shaking, and then the particulate matter was
allowed to settle for approximately 1 min. Supernatant material was
then transferred in order to minimize the amount of sediment passed to
the next vessel. Sequential transfers (10% [vol/vol]) from primary
enrichment cultures were made into E-Cl medium with dried BH sediment
(0.1%, wt/vol [dry weight], unless stated otherwise) that was then
sterilized in an autoclave at 121°C for a total of 3 h (two
1.5-h treatments). Subsequent transfers were made under identical
conditions every 2 to 5 months. Sequential transfers (10% [vol/vol])
for the establishment of sediment-free cultures were made every 2 to 5 months into identical media without sediment. Following the first two
transfers, the amount of sediment passed was negligible.
Spectrophotometric analysis.
Growth in sediment-free
cultures was monitored by measuring the increase in optical density at
600 nm (OD600) with a Spectronic 20D spectrophotometer
(Milton Roy, Rochester, N.Y.).
Sampling and PCB analysis.
Aliquots were withdrawn
anaerobically once at each time point from shaken cultures by using the
reverse end of a 5-ml glass pipette (front end for sediment-free
samples). Samples were extracted in ethyl acetate and passed over a
Florisil-copper column as previously described by Berkaw et al.
(2). Analysis was conducted with a Hewlett-Packard 5890A gas
chromatograph (GC) equipped with an electron capture detector (ECD) and
an RTX-1 capillary column as previously described (2).
Standards for 2-, 3-, 4-, 2,3-, 2,5-, 2,6-, 3,5-, 2,3,5-, 2,3,6- and
2,3,5,6-CB were purchased from AccuStandard (New Haven, Conn.). PCB
congeners were identified by retention time and quantified with a
16-point calibration curve for each congener according to the method of
Berkaw et al. (2).
| |
RESULTS AND DISCUSSION |
Selection of ortho dechlorination.
Reductive
dechlorination of 2,3,5,6-CB was observed to occur in primary
enrichment cultures incubated with BH sediment under anaerobic
conditions. GC-ECD analysis revealed various meta and ortho dechlorination products. Large amounts of
transient 3,5-CB, along with smaller amounts of 2,5-CB and
2,6-CB, were observed, while 3-CB eventually became the dominant
product (Fig. 1). No dechlorination
products were ever observed in killed-cell controls (sterilized
sediment and media) or no-inoculum controls.
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FIG. 1.
Dechlorination of 2,3,5,6-CB by a primary enrichment
culture with BH sediment (5.0%, wt/vol [dry weight]). Mole percent
and chlorines-per-biphenyl data are from a single culture. Symbols:
 , mole percent for 3-CB;  , 2,5-CB;  , 2,6-CB;  , 3,5-CB;  ,
2,3,5-CB;  , 2,3,6-CB; and  , 2,3,5,6-CB.  , chlorines per
biphenyl.
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|
Sequential transfers (10% [vol/vol]) from the primary culture were
made into E-Cl medium containing 0.1% (wt/vol [dry weight])
sterile
BH sediment. Selection of
ortho dechlorination reactions
with a loss of
meta reactions was observed after the first
transfer.
Further transfer resulted in cultures that exclusively
ortho dechlorinated
2,3,5,6-CB to 3,5-CB within 50 days,
with 2,3,5-CB as the only
intermediate detected by GC-ECD analysis
(Fig.
2). In contrast
to the large
accumulation of 3-CB observed in primary cultures,
virtually all of the
2,3,5,6-CB was transformed to 3,5-CB in the
transferred cultures, with
no other end products observed. This
pattern of strict
ortho
dechlorination of the 2,3,5,6-CB remained
the same through five
sequential transfers (made once every 3
to 5 months) beyond the primary
enrichment cultures. In addition,
no monochlorobiphenyl arose, even
after extensive incubation lasting
up to a year.
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FIG. 2.
Dechlorination of 2,3,5,6-CB after the first transfer of
the supernatant from the primary enrichment culture into E-Cl medium
with BH sediment (0.1% wt/vol [dry weight]). Mole percent and
chlorines-per-biphenyl data are from a single culture. Symbols: ,
mole percent for 3-CB; , 3,5-CB; , 2,3,5-CB; and , 2,3,5,6-CB.
, chlorines per biphenyl.
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|
Microbial dechlorination of 2,3,5,6-CB in the absence of
sediment.
Sequential transfers (10% [vol/vol]) from the primary
cultures containing 5% (wt/vol [dry weight]) BH sediment were made
into E-Cl medium with no added sediment. By the second transfer, the sediment was no longer visible to the naked eye and a low rate of
dechlorination was observed. A mixed culture dominated by blunt-end rod-shaped cells and small vibrio-shaped cells developed. Each transfer
culture was started at an OD600 between 0.01 and 0.05 and
was transferred after the OD600 was >0.1, regardless of
the degree of dechlorinating activity. Congener 2,3,5,6-CB was added to
a final concentration of 173 µM, which is significantly above its
aqueous solubility limit (3). However, reasonable recoveries of the PCB, 80% on average, could be made by vigorously mixing the
culture with a pipette before sampling. It was assumed that the PCBs
were sorbing to or partitioning into the biomass.
The objective at this point was to detect a significant amount of
dechlorination product in the sediment-free culture series.
Significant
amounts (mole percent) of 2,3,5-CB and 3,5,-CB began
to accumulate in
the fourth-sequential-transfer cultures following
extensive incubation
(Fig.
3). After more than 200 days, when
ortho dechlorination had been clearly established and the
culture
had become more turbid (OD
600 > 0.2), these
sediment-free cultures
were transferred again. This
fifth-sequential-transfer culture
had a shortened lag time of less than
50 days (Fig.
3). No dechlorination
was observed with sterile
(killed-cell) or no-inoculum controls.
Only
ortho
dechlorination of the 2,3,5,6-CB to 2,3,5-CB and 3,5-CB
was observed at
all times with all of these cultures. Since the
establishment of stable
dechlorination, we have been able to routinely
transfer these cultures
into identical sediment-free media and
still maintain dechlorinating
activity.
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FIG. 3.
Chlorines-per-biphenyl data for fourth- and
fifth-sequential-transfer cultures without sediment. Mole percent data
are given for the fourth-transfer culture. All data are given as the
averages from duplicate cultures. Symbols: , mole percent for
3,5-CB; , 2,3,5-CB; and , 2,3,5,6-CB. , chlorines per biphenyl
of fourth-sequential-transfer culture;  , chlorines per biphenyl of
fifth-sequential-transfer culture.
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|
The appearance of dechlorination at the fourth transfer of the
sediment-free cultures after an incubation period exceeding
that of
earlier cultures in the transfer series suggests that
the transfers
were made too quickly (at low cell density) during
the early part of
the enrichment process. OD data for a later
set of active sediment-free
cultures (Fig.
4) revealed that
significant
dechlorination does not occur until the OD
600
exceeds 0.2. This
observation supports our conclusion that the ability
to maintain
good dechlorination earlier on in the sediment-free
enrichment
series was hindered by premature transfer of the cultures at
low
turbidity. Perhaps the earlier transfers at lower turbidity had
prevented the development of hearty dechlorinating cultures and
sustainability was simply an issue of low numbers of dechlorinators
among the total population. The possibility that the organisms
responsible for the dechlorination needed an extensive amount
of time
to adjust to the altered conditions (lack of sediment)
before being
able to carry out the dechlorination also exists.
This latter
possibility may be associated with the uptake (availability)
of the PCB
or supply of a nutrient. It is also possible that during
this lengthy
process we enriched for a prototroph that no longer
requires a
component of the sediment in order to dechlorinate
a PCB.
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FIG. 4.
OD () and chlorines-per-biphenyl () data from
duplicate fifth-sequential-transfer cultures without sediment.
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|
Sediment stimulation of ortho dechlorination.
The
above results demonstrate that ortho dechlorination is
independent of the sediment. However, several results show the sediment
to have a stimulatory effect. The first suggestion of this was observed
with the decrease in the rate and extent of ortho
dechlorination that accompanied the shift from
meta-and-ortho to strictly ortho
dechlorination (Fig. 1 and 2). This occurred after a primary culture
had been transferred to a medium with far less sediment (5.0 to 0.1%,
wt/vol [dry weight]). This change in activity could have been due to
the decrease in the amount of sediment present. To examine this, a
range of sediment concentrations was tested under the conditions
described above. In order to be certain of the sediment concentration,
the supernatant from the primary culture was transferred (10%
[vol/vol]) into vessels containing E-Cl medium with the different
amounts of BH sediment to be tested. After 4 months of incubation,
transfers were made from these cultures into identical medium and the
results of this second set of cultures are presented in Fig.
5. While dechlorinating activity could be maintained regardless of the sediment concentration, the lag preceding dechlorination increased to more than 100 days when the sediment concentration was lowered to 0.05% (dry wt). The cultures incubated with 1.0% (dry wt) sediment exhibited a higher rate of dechlorination and a shorter lag time than did those incubated with lesser amounts of
sediment. Killed-cell controls (sterilized sediment cultures) exhibited
no dechlorination. From a qualitative perspective, dechlorination did
not change with sediment concentration and remained strictly ortho. Additional experiments with sediment-free cultures
also demonstrated that the sediment could be stimulatory.
Pre-dechlorination sediment-free cultures (in this case the
fourth sequential sediment-free transfer cultures before the
onset of dechlorination) were transferred into E-Cl medium with and
without 1.0% (dry weight) BH sediment (sterile). The
pre-dechlorination transfer cultures with sediment showed a quicker
recovery of dechlorination than did transfer cultures maintained
without sediment (Fig. 6). Once again, no dechlorination was observed with killed-cell controls. This confirmed the existence of a factor(s) in the sediment that was stimulatory but
not required for dechlorination.
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FIG. 5.
Cultures with 2,3,5,6-CB and 1.0% (), 0.1% (),
and 0.05% () (wt/vol [dry weight]) sterilized BH sediment.
Supernatant from a 5.0% sediment culture was sequentially transferred
with 1.0, 0.1, and 0.05% (wt/vol [dry weight]) BH sediment in E-Cl
medium, incubated for 4 months, and transferred again under identical
conditions. The data presented represent the second set of transferred
cultures. The chlorines-per-biphenyl data for the killed-cell control
with 1.0% sterilized BH sediment are for a single culture (). The
data from the live BH cultures are the average of duplicates.
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FIG. 6.
Effect of sediment added to a pre-dechlorination
sediment-free culture. The fourth-sequential-transfer sediment-free
cultures (pre-dechlorination) were transferred to medium with () and
without () 1.0% sterilized BH sediment. , killed-cell control.
All data are for triplicate cultures. Error bars indicate standard
deviations.
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|
The mode of action of the sediment stimulation of PCB dechlorination
has not been determined. Humic acids (Aldrich Chemical
Co., Milwaukee,
Wis., and other sources) and anthraquinone-2,6-disulfonic
acid (AQDS)
have been shown to act as intermediate electron acceptors
in the
facilitation of biological Fe
3+ reduction (
4).
Similarly, humic substances or AQDS might stimulate
ortho
PCB dechlorination. However, substitution of two different
commercial
humic acids at 0.1% (wt/vol [dry weight]) (Burlington
Chemical Co.,
Long Island, N.Y., and Aldrich Chemical Co.) or
3 mM AQDS (Aldrich
Chemical Co.) did not provide the same degree
of stimulation of PCB
dechlorination to the cultures as BH sediment
(data not shown). In
fact, the Aldrich humic acids and the AQDS
completely inhibited
dechlorination. The results from these experiments
do not define
the stimulatory role of the sediment, but they do
demonstrate the
utility of the sediment-free cultures in addressing
such questions.
Other possible roles for the BH sediment include
stimulation due to
additional carbon and energy or micronutrients,
facilitation of the
availability of the PCB to the microorganisms
(this could also
prevent toxicity due to PCBs), supply of a more
suitable
attachment site for microbial colonization, or supply
of an
extracellular catalytic intermediate similar to AQDS which
may
facilitate the dechlorination.
Concluding remarks.
PCB dechlorination can occur in the
absence of sediment, albeit more slowly than with sediment, indicating
that whatever is contributed by the sediment is not essential or
irreplaceable. We have now been able to sequentially transfer the
ortho-dechlorinating culture eight times over a 33-month
period in the minimal, sediment-free medium described here. Further,
with the use of nearly identical enrichment procedures and patience, we
have recently established enrichment cultures which actively
para dechlorinate 2,3,4,5-CB in the absence of sediment.
These cultures are incapable of dechlorinating 2,3,5,6-CB. We are still
pursuing a meta-dechlorinating sediment-free enrichment
culture.
Perhaps the most significant contribution of the findings presented
here is that the sediment-free cultures offer opportunities
to address
questions of mechanism, cell structure, and identity
that were not
approachable in the past. For example, with the
ability to make
microscopic observation and determine OD, etc.,
questions concerning
growth and whether it can be coupled to PCB
dechlorination can now be
more easily addressed. Isolation and
characterization of the
microorganisms present in these cultures
can now proceed at a faster
pace since the organisms are in a
defined medium. We are taking
advantage of this by investigating
a broader group of electron donors
and acceptors, individually,
without interference from unknown
substances in the sediment while
monitoring the microbial population
through molecular identification.
The development of the actively dechlorinating sediment-free cultures
provides a unique opportunity for further experimentation
concerning
the identification of the stimulating factors in the
sediment. In
addition, the sediment-free cultures can act as a
model system to
investigate biochemical and geochemical mechanisms
internal and
external to the cell which may contribute to PCB
dechlorination.
Finally, studies of how to grow these organisms
free of soil or
sediment may lead to the ability to mass culture
such organisms. This
is needed in order to advance investigation
of the biochemical
mechanism of PCB dechlorination and could also
be important for
bioaugmentation studies of PCB-contaminated sediments.
| |
ACKNOWLEDGMENTS |
This work was supported by grants from the Office of Naval
Research (ONR), U.S. Department of Defense (DOD), to H.M. (grant N00014-96-1-0116) and to K.S. (grant N00014-96-1-0115). L.C. was supported by a DOD award (Augmentation Awards for Science and Engineering Research Training) from ONR to H.M. (grant
N00014-96-1-1033).
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Medical
University of South Carolina, Dept. of Microbiology & Immunology, 171 Ashley Ave., 225 BSB, Charleston, SC 29425-2230. Phone: (803) 792-7140. Fax: (803) 792-2464. E-mail: mayh{at}musc.edu.
| |
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Applied and Environmental Microbiology, August 1998, p. 2966-2969, Vol. 64, No. 8
0099-2240/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
