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Applied and Environmental Microbiology, March 1999, p. 1335-1339, Vol. 65, No. 3
0099-2240/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Contrasting Effects of a Nonionic Surfactant on the
Biotransformation of Polycyclic Aromatic Hydrocarbons to
cis-Dihydrodiols by Soil Bacteria
Christopher C. R.
Allen,1,*
Derek R.
Boyd,2
Francis
Hempenstall,2
Michael J.
Larkin,3 and
Narain D.
Sharma2
The QUESTOR Centre1
and School of Chemistry,2 The Queen's
University of Belfast, Belfast BT9 5AG, and School of
Biology and Biochemistry, The Queen's University of Belfast,
Medical Biology Centre, Belfast BT9 7BL,3
Northern Ireland
Received 25 September 1998/Accepted 22 December 1998
 |
ABSTRACT |
The biotransformation of the polycyclic aromatic hydrocarbons
(PAHs) naphthalene and phenanthrene was investigated by using two
dioxygenase-expressing bacteria, Pseudomonas sp. strain
9816/11 and Sphingomonas yanoikuyae B8/36, under conditions
which facilitate mass-transfer limited substrate oxidation. Both of
these strains are mutants that accumulate cis-dihydrodiol
metabolites under the reaction conditions used. The effects of the
nonpolar solvent 2,2,4,4,6,8,8-heptamethylnonane (HMN) and the nonionic
surfactant Triton X-100 on the rate of accumulation of these
metabolites were determined. HMN increased the rate of accumulation of
metabolites for both microorganisms, with both substrates. The
enhancement effect was most noticeable with phenanthrene, which has a
lower aqueous solubility than naphthalene. Triton X-100 increased the rate of oxidation of the PAHs with strain 9816/11 with the effect being
most noticeable when phenanthrene was used as a substrate. However, the
surfactant inhibited the biotransformation of both naphthalene and
phenanthrene with strain B8/36 under the same conditions. The
observation that a nonionic surfactant could have such contrasting
effects on PAH oxidation by different bacteria, which are known to be
important for the degradation of these compounds in the environment,
may explain why previous research on the application of the surfactants
to PAH bioremediation has yielded inconclusive results. The surfactant
inhibited growth of the wild-type strain S. yanoikuyae B1
on aromatic compounds but did not inhibit B8/36 dioxygenase enzyme
activity in vitro.
| |
TEXT |
Polycyclic aromatic hydrocarbons
(PAHs) are a major cause of concern as anthropogenic pollutants in the
environment. They arise from diverse sources, including petrochemical
products and the combustion of fossil fuels (3). Concern
arises for two reasons, first because many are recalcitrant, and second
because of the health hazards associated with these compounds. Many,
such as benzo[a]pyrene, chrysene, and
benz[a]anthracene, are also carcinogens in animals.
One approach that has been considered for enhancing PAH bioremediation
in contaminated soils is the application of nonionic surfactants
(26). The theoretical justification for this solution is
based upon two hypotheses, first that surfactant micelles may sequester
PAHs which are sorbed to the soil matrix, and second that the
surfactant micelles may increase the concentration of PAHs in the
aqueous phase because the PAHs are more soluble in the micelles. Where
the rate of PAH degradation is limited by mass transfer from the solid
phase to the aqueous phase, the PAH oxidation rates by microorganisms
may then be enhanced (11, 23). Furthermore, there is also
some evidence to suggest that certain microorganisms may absorb PAHs
directly from surfactant micelles (27).
A number of studies to test these hypotheses have been carried out, but
the results have been inconclusive. While some reports suggest that
surfactants may increase PAH biodegradation rates (20, 26, 28,
29), others have shown that the effect of their application may
be negligible or even detrimental (19, 26, 28, 29).
To date, the typical approach to evaluating surfactants in laboratory
studies with monocultures has involved the analysis of their effect on
microbial growth characteristics, such as specific growth rate and
cellular yields, with PAHs as growth substrates (11).
However, the conclusions may not be wholly applicable because this type
of study excludes those microorganisms present in the environment which
can oxidize the PAHs by cometabolism (i.e., concomitant metabolism of
growth and nongrowth substrates). For many PAHs, especially those with
four or more aromatic rings, cometabolism may serve as the main route
for their degradation (10, 15, 22, 23). Furthermore, growth
of monocultures in these experiments (where specific growth rates are
relatively high) may not be limited by the same factors in situ, where
specific growth rates of bacteria are likely to be much lower. If the
results from experiments using monocultures are to be used to optimize surfactant use in bioremediation, then the effect of the surfactants on
the rate of PAH oxidation by the di- and mono-oxygenase enzymes involved in the initial degradation of these molecules might prove to
be more useful.
In this study, a comparison was made between two groups of
microorganisms which play an important role in the degradation of
aromatic hydrocarbons in the environment. Sphingomonads have been shown
to metabolize a number of PAHs, including the larger molecules, such as
benzo[a]pyrene (10) and chrysene
(2). Pseudomonads are known to be particularly important in
the biodegradation of monocyclic aromatic hydrocarbons, such as toluene
and benzene (7, 8, 30), and of the smaller PAHs, such
as naphthalene and phenanthrene (5, 12, 17).
In this paper, we propose that the inconclusive observations which have
resulted from the earlier surfactant-PAH bioremediation studies can be
explained if the surfactants were inhibitory to PAH degradation by some
bacteria while enhancing the rate of PAH degradation in others. If this
were the case, then the composition of the microbial population in a
PAH-contaminated site would determine the effectiveness of such
nonionic surfactants in PAH bioremediation applications.
We would then expect that when different PAH-degrading microorganisms
are used to biotransform PAHs, they will show varying responses to the
addition of nonionic surfactants. This is because if a surfactant is
not toxic to a microorganism under conditions where PAH oxidation is
limited by substrate mass transfer, then an increase in the rate of PAH
oxidation is expected. If the PAH is toxic, then inhibition of PAH
oxidation should occur.
The aim of the work presented here was to investigate the effect of a
common surfactant on PAH oxidation by arene dioxygenase enzymes in two
different microorganisms, which can convert the PAHs to their
corresponding cis-dihydrodiol metabolites. The enzymes are
expressed in mutant strains of bacteria which do not have cis-dihydrodiol dehydrogenase enzyme activity and therefore
accumulate the cis-dihydrodiols. This work therefore
provided an opportunity to test the explanation proposed above. One
advantage of this approach is that any conclusions drawn may be
applicable to degradation processes that involve cometabolism.
The bacteria used were the wild-type Sphingomonas
yanoikuyae B1 (9, 16) and a mutant (B8/36) derived
from this strain. The mutant accumulates cis-dihydrodiol
metabolites when grown under experimental conditions, facilitating the
expression of a biphenyl dioxygenase (BPO) enzyme (25). Also
used were Pseudomonas sp. strain NCIMB 9816 (5)
and a mutant strain, 9816/11, which also accumulates
cis-dihydrodiol metabolites under conditions that facilitate
expression of a naphthalene dioxygenase enzyme (NDO) (25).
Pseudomonas sp. strain NCIMB 9816 was obtained from the
National Collection of Industrial and Marine Bacteria Ltd., Aberdeen,
United Kingdom.
Biotransformation of PAHs in a two-phase HMN-water system.
Surfactant solutions at concentrations above the critical micelle
concentration (CMC) can be considered "two-phase" systems, where
the secondary phase is made up of the surfactant micelle pseudophase
(11).
We investigated the biotransformation of the PAHs naphthalene and
phenanthrene by the two mutant strains in a two-phase system to
establish conditions under which PAH degradation was mass transfer limited. We would then expect to see an increased yield of PAH cis-dihydrodiol metabolites in this system, where the
substrates are dissolved in a suitable nonpolar solvent. The solvent
2,2,4,4,6,8,8-heptamethylnonane (HMN) was chosen (24).
In biotransformation experiments, the concentration of the products,
cis-1R,2S-dihydroxy-1,2-dihydronaphthalene
(naphthalene cis-1,2-dihydrodiol) and
cis-3S,4R-dihydroxy-3,4-dihydrophenanthrene (phenanthrene cis-3,4-dihydrodiol), was determined.
Naphthalene is converted to naphthalene cis-1,2-dihydrodiol
by both of the two strains (12), and phenanthrene is
converted to a mixture of phenanthrene cis-3,4-diol (95%
relative yield) and
cis-1R,2S-dihydroxy-1,2-dihydrophenanthrene (phenanthrene cis-1,2-dihydrodiol; 5% relative yield)
(13, 18). By analysis of biotransformation crude extracts
using 1H-nuclear magnetic resonance (500 MHz,
CDCl3), we have found the same relative yields of the 3,4- and 1,2-dihydrodiols produced in phenanthrene biotransformations with
both S. yanoikuyae B8/36 and Pseudomonas sp.
strain 9816/11. Both of these compounds coeluted when they were
detected in time course biotransformations by reverse-phase high-pressure liquid chromatography (HPLC). Purified phenanthrene cis-3,4-dihydrodiol was therefore used as a standard. For
quantification by HPLC, the cis-dihydrodiol standards were
prepared by using published methods (1, 13).
The results of these time course studies are shown in Fig.
1. At the end of the experiments, the
concentration of
cis-dihydrodiol
in the HMN phase was
determined, and the partition coefficient
of phenanthrene
cis-dihydrodiol concentration in the organic phase
versus
the concentration in the aqueous phase was found to be
approximately
0.1 for both
cis-dihydrodiols. This indicated that
most of
the
cis-dihydrodiol metabolites produced were present
in the
aqueous phase.
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FIG. 1.
Effect of HMN on the biotransformation of naphthalene by
Pseudomonas sp. strain 9816/11 (a) and S. yanoikuyae B8/36 (b) and of phenanthrene by Pseudomonas
sp. strain 9816/11 (c) and S. yanoikuyae B8/36 (d). HMN was
added at a ratio of 5 ml per 100 ml of cell suspension ( ). Control
flasks ( ) had no HMN added. Strains were grown using published
methods (induction being required for expression of dioxygenase enzymes
for both biotransformation and enzyme assay experiments)
(25). For all biotransformation experiments, cells were
resuspended in 0.1 M potassium phosphate buffer (pH 7.5;
A600 = 1.1). Sodium succinate (31 mM) was used
as a cosubstrate, and (unless otherwise stated) PAH substrates were
added at a concentration of 0.9 g liter 1. All
biotransformations were conducted in triplicate; data points show the
mean concentrations of cis-dihydrodiol metabolites in the
aqueous phase. HPLC analysis using an octyldecyl silane 15-cm
reverse-phase column (50 to 70% methanol-water gradient over 30 min, 0.5 ml min1 flow rate) of phenanthrene metabolites
was performed at 260 nm, and analysis of naphthalene metabolites was
performed at 265 nm.
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These data clearly show that in all cases HMN increased the yield of
cis-dihydrodiols accumulating over the period of the
experiment. The effect was most noticeable with the phenanthrene
biotransformations, but this might be expected, as phenanthrene
is
considerably less soluble in water (1.3 mg liter
1) than
naphthalene (31.7 mg liter
1) at ambient temperature
(
21). Therefore, where biotransformation
rates are limited
by mass transfer of the PAH from the solid phase
via the liquid phase
to the biocatalyst, the large increase in
interfacial area which
results from dissolving the PAHs in HMN
would be expected to increase
the rate of microbial
oxidation.
It is interesting to note that there were some differences
between biotransformations with the two microorganisms. Similar
concentrations of the
cis-dihydrodiol were observed
for the naphthalene
biotransformations with both microorganisms
when HMN was added.
However,
S. yanoikuyae B8/36 accumulated
the
cis-dihydrodiol of
phenanthrene at approximately four
times the amount of that achieved
with the 9816/11
strain.
Effect of Triton X-100 on PAH biotransformations.
Having
established that two-phase systems can be used to enhance the yields of
PAH metabolites under mass-transfer limited biotransformation
conditions with the two strains, the effect of a surfactant was then
determined. We chose to use Triton X-100 in these experiments because a
number of reports suggest that it is effective in PAH bioremediation
and also relatively nontoxic to microorganisms (19, 20, 29).
The surfactant was tested by using the same biotransformation
conditions as in the earlier experiments and at a number of
concentrations above the cited CMC of 0.17 mM (20). The
results from these experiments are shown in Fig.
2.
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FIG. 2.
Effect of Triton X-100 on biotransformation of
naphthalene by Pseudomonas sp. strain 9816/11 (a) and
S. yanoikuyae B8/36 (b) and of phenanthrene by
Pseudomonas sp. strain 9816/11 (c) and S. yanoikuyae B8/36 (d). Triton X-100 (variable concentrations as
described, prepared in a filter-sterilized 100 mM stock solution) was
added to final concentrations of 0.2 mM (), 0.5 mM (), 1.0 mM
( ), and 2.0 mM ( ). All biotransformations were conducted in
triplicate; data points show the total mean concentrations of
cis-dihydrodiol metabolites present.
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|
If the effects of the surfactant on
Pseudomonas sp. strain
9816/11 are considered, it is clear that there is a significant
enhancement of
cis-dihydrodiol accumulation with both PAHs
in
the presence of increasing concentrations of the surfactant.
Furthermore,
it should be noted that the effect with phenanthrene was
again
greater than that with naphthalene. The concentration of
phenanthrene
cis-dihydrodiol which accumulated in
biotransformations with this
strain at the maximum surfactant
concentration studied was greater
than that which was observed with the
same microorganism and HMN,
and with
S. yanoikuyae B8/36 in
the absence of any secondary phase.
These results point to the
conclusion that where surfactants are
not toxic, significant
enhancement of the PAH oxidation rate may
be facilitated where the rate
is otherwise limited by mass
transfer.
Although other studies have shown that surfactants can increase the
rate of growth of microorganisms on PAHs (
11,
28),
here we
show conclusively that they also increase the rate of
oxidation of PAHs
by dioxygenase enzymes in vivo. The scale of
this enhancement is likely
to be influenced by factors such as
the solubility of the PAHs in both
the aqueous phase and the surfactant
pseudophase and also by the
concentration of surfactant present.
Cox and Williams (
4)
investigated the effect of surfactants
on the oxidation of naphthalene
to naphthalene
cis-1,2-dihydrodiol
by an NDO-expressing
P. putida mutant. In that study, a mixture
of the
surfactants Tergitol NP-10 and Neodol 25-3A was used, and
the rates of
substrate oxidation by the bacteria in the presence
of the surfactant
mixture were approximately three times that
of the control. However it
should be noted that the surfactant
concentrations used in those
experiments (1% [vol/vol]) were significantly
higher than those
employed
here.
In contrast, it was apparent that the surfactant inhibited the
biotransformation of both substrates with
S. yanoikuyae
B8/36,
with the maximum concentrations of metabolites occurring at
levels
less than those observed without a second phase (Fig.
1).
Therefore,
we can conclude that Triton X-100 was toxic to this
microorganism
under these experimental conditions. The data presented
here show
conclusively that the effect of a nonionic surfactant on PAH
transformation
by dioxygenase-expressing microorganisms is greatly
affected by
the type of bacteria involved. It therefore strongly
supports
the earlier proposal that the inconclusive results of
bioremediation
studies may be explained by differences in the
population of PAH-degrading
bacteria present. This observation is
especially important if
we consider that
Sphingomonas spp.
have been implicated in the
biodegradation of a number of the larger
recalcitrant PAHs (
2,
10,
22), and that therefore they may
play an important role
in the biodegradation of these compounds in
nature.
Effect of Triton X-100 on growth of bacteria with aromatic
substrates.
The observation that a surfactant should have
different effects on the S. yanoikuyae and
Pseudomonas sp. oxidations was considered novel in the
context of biodegradation and was investigated further. Table
1 shows the effect of the surfactant on
the specific growth rate of the wild-type S. yanoikuyae B1
when it was grown on a variety of carbon sources under otherwise
identical conditions. The data corroborate the conclusion that the
surfactant inhibits oxidation of phenanthrene in S. yanoikuyae B8/36. Furthermore, the data show that Triton X-100
also inhibited growth of this organism on the aromatic substrates
biphenyl, phenanthrene, and sodium benzoate. However, there was no
growth inhibition when sodium pyruvate was used as a growth substrate.
These data might indicate that while the inhibitory effect was not
specific for a particular aromatic pathway, neither was it a general
toxic effect. In the control experiments, the effect of the surfactant was determined on the growth of the wild-type Pseudomonas
sp. strain NCIMB 9816 with naphthalene, sodium benzoate, and sodium succinate provided as carbon sources. In this case, no detrimental effect of the surfactant on growth was found.
Effect of Triton X-100 on dioxygenase enzyme activity.
One
explanation for the observed effects of the surfactant on strain B1 may
be that the surfactant inhibits arene dioxygenase enzymes in this
organism. To test this hypothesis, cell extracts of both S. yanoikuyae B8/36 and Pseudomonas sp. strain 9816/11 were assayed for their ability to oxidize 14C-labelled
naphthalene by using an assay for NDO activity (6), in both
the presence and absence of the surfactant. The specific activity of
the dioxygenase in strain B8/36 towards naphthalene was 0.17 nmol
min1 mg1; in the presence of 1 or 2 mM
Triton X-100, there was no noticeable effect on this activity (specific
activity estimates were 0.19 and 0.18 nmol min1
mg1, respectively; in all assays, these activities are
the means of duplicate measurements). The specific activity of the
dioxygenase in strain 9816/11 towards naphthalene was 4.84 nmol
min1 mg1. In the presence of Triton X-100,
the activity of this enzyme actually increased, to 7.05 (1 mM) and 7.69 (2 mM) nmol min1 mg1. These data show that
the surfactant had no inhibitory effect on dioxygenase activity in
either strain. This would indicate that the site of inhibition in the
Sphingomonas sp. is not at the dioxygenase but elsewhere. A
supply of electrons (via NADH or NADPH) is critical for dioxygenase
activity in vivo, and therefore any disruptive effects on the cell
membrane of the Sphingomonas cell would cause loss of
dioxygenase enzyme activity. The structure of the cell wall in this
microorganism is quite different from that in pseudomonads
(14), and this should be considered a possible site of inhibition.
An unexpected observation from these experiments was that enzyme
activity in
Pseudomonas sp. strain 9816/11 was increased
in
the presence of low levels of the surfactant. Negative control
experiments, in which the assay was repeated in the absence of
any cell
extract and in the absence of NADH, clearly indicated
that this effect
was enzyme mediated and also NADH dependent.
The reason for this
increase in activity is at present uncertain
and warrants further
investigation.
In summary, the results in this report have shown that the surfactant
Triton X-100 can have quite opposite effects on the
biotransformation
of PAHs by resting cells of PAH-degrading bacteria.
While inhibition of
biotransformation occurred with the
S. yanoikuyae B8/36
mutant, the surfactant was also found to prevent growth
of the
wild-type
S. yanoikuyae B1 strain with aromatic substrates.
Furthermore, our results suggest that the site of this inhibition
is
not the PAH-dioxygenase
enzyme.
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ACKNOWLEDGMENTS |
This work was supported in part by grants from The Queen's
University of Belfast Environmental Science and Technology Research (QUESTOR) Centre (to C.C.R.A.) and the Biotechnology and Biological Sciences Research Council (BBSRC) (to N.D.S.).
We thank David T. Gibson for supplying S. yanoikuyae B1 and
B8/36 and Pseudomonas sp. strain 9816/11.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: The QUESTOR
Centre, The Queen's University of Belfast, David Keir Building,
Stranmillis Road, Belfast BT9 5AG, Northern Ireland. Phone:
(0232)335577/8. Fax: (0232)1661462. E-mail:
C.ALLEN{at}QUB.AC.UK.
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Applied and Environmental Microbiology, March 1999, p. 1335-1339, Vol. 65, No. 3
0099-2240/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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