Fenpropathrin biodegradation pathway in bacillus sp. DG-02 and its potential for bioremediation of pyrethroid-contaminated soils

Article abstract of DOI:10.1021/jf404908j

The widely used insecticide fenpropathrin in agriculture has become a public concern because of its heavy environmental contamination and toxic effects on mammals, yet little is known about the kinetic and metabolic behaviors of this pesticide. This study reports the degradation kinetics and metabolic pathway of fenpropathrin in Bacillus sp. DG-02, previously isolated from the pyrethroid-manufacturing wastewater treatment system. Up to 93.3% of 50 mg L^-1 fenpropathrin was degraded by Bacillus sp. DG-02 within 72 h, and the degradation rate parameters q_max, K_s, and K _i were determined to be 0.05 h^-1, 9.0 mg L^-1, and 694.8 mg L^-1, respectively. Analysis of the degradation products by gas chromatography-mass spectrometry led to identification of seven metabolites of fenpropathrin, which suggest that fenpropathrin could be degraded first by cleavage of its carboxylester linkage and diaryl bond, followed by degradation of the aromatic ring and subsequent metabolism. In addition to degradation of fenpropathrin, this strain was also found to be capable of degrading a wide range of synthetic pyrethroids including deltamethrin, λ-cyhalothrin, β-cypermethrin, β-cyfluthrin, bifenthrin, and permethrin, which are also widely used insecticides with environmental contamination problems with the degradation process following the first-order kinetic model. Bioaugmentation of fenpropathrin-contaminated soils with strain DG-02 significantly enhanced the disappearance rate of fenpropathrin, and its half-life was sharply reduced in the soils. Taken together, these results depict the biodegradation mechanisms of fenpropathrin and also highlight the promising potentials of Bacillus sp. DG-02 in bioremediation of pyrethroid-contaminated soils.

Full text of DOI:10.1021/jf404908j

Article
pubs.acs.org/JAFC
Fenpropathrin Biodegradation Pathway in Bacillus sp. DG-02 and Its
Potential for Bioremediation of Pyrethroid-Contaminated Soils
†
,§,‡
†,§
†,§
§
§
†,‡
Shaohua Chen,
Changqing Chang, Yinyue Deng, Shuwen An, Yi Hu Dong, Jianuan Zhou,
†
,†
,†,§,‡
Meiying Hu, Guohua Zhong,* and Lian-Hui Zhang*
†College of Natural Resources and Environment, South China Agricultural University, Guangzhou 510642, People’s Republic of
China
§
Institute of Molecular and Cell Biology, Proteos, 61 Biopolis Drive, Singapore 138673, Republic of Singapore
‡
Guangdong Province Key Laboratory of Microbial Signals and Disease Control, South China Agricultural University, Guangzhou
510642, People’s Republic of China
*
S Supporting Information
ABSTRACT: The widely used insecticide fenpropathrin in agriculture has become a public concern because of its heavy
environmental contamination and toxic effects on mammals, yet little is known about the kinetic and metabolic behaviors of this
pesticide. This study reports the degradation kinetics and metabolic pathway of fenpropathrin in Bacillus sp. DG-02, previously
isolated from the pyrethroid-manufacturing wastewater treatment system. Up to 93.3% of 50 mg L− fenpropathrin was degraded
1
−1
by Bacillus sp. DG-02 within 72 h, and the degradation rate parameters q , K , and K were determined to be 0.05 h , 9.0 mg
max
s
i
−1
−1
L , and 694.8 mg L , respectively. Analysis of the degradation products by gas chromatography−mass spectrometry led to
identification of seven metabolites of fenpropathrin, which suggest that fenpropathrin could be degraded first by cleavage of its
carboxylester linkage and diaryl bond, followed by degradation of the aromatic ring and subsequent metabolism. In addition to
degradation of fenpropathrin, this strain was also found to be capable of degrading a wide range of synthetic pyrethroids
including deltamethrin, λ-cyhalothrin, β-cypermethrin, β-cyfluthrin, bifenthrin, and permethrin, which are also widely used
insecticides with environmental contamination problems with the degradation process following the first-order kinetic model.
Bioaugmentation of fenpropathrin-contaminated soils with strain DG-02 significantly enhanced the disappearance rate of
fenpropathrin, and its half-life was sharply reduced in the soils. Taken together, these results depict the biodegradation
mechanisms of fenpropathrin and also highlight the promising potentials of Bacillus sp. DG-02 in bioremediation of pyrethroid-
contaminated soils.
KEYWORDS: Bacillus sp. DG-02, fenpropathrin, bioremediation, metabolites, biodegradation pathway, kinetics
INTRODUCTION
widespread environmental contamination situation also in-
creases the potential of human exposure to the insecticide.
■
12−16
Synthetic pyrethroids (SPs) are the chemical analogues of
pyrethrins, which are natural chemicals derived from the
flowers of Chrysanthemum cinerariaefolium. The usage of SPs
has been increasing steadily over the past two decades, and
these insectcides have now become one of the most widely
used classes of pesticides. Especially with the ban or restricted
Although SPs are considered safer than organophosphorous
insecticides, evidence is accumulating that developmental
exposure to fenpropathrin may cause severe toxic effects on
human beings, including reproductive damages, neurotoxicity,
1
17−20
2
immunotoxicity, endocrine disruption, and carcinogenesis.
Furthermore, fenpropathrin is also highly toxic to fish and
use of organophosphates in more and more countries, SPs have
generally been regarded as the suitable replacement, and their
commercial production and usage are anticipated to be further
21
invertebrates. Thus, effective measures for reducing this
contamination problem are critically needed to ensure that
human health and environmental sustainability will not be
compromised by the continued use of fenpropathrin.
3
4
increased. Currently, they are the dominant insecticides,
5
contributing to >25% of worldwide insecticide sales. Most
pyrethroids contain cyclopropanecarboxylic acid moieties (or
an equivalent group) linked to aromatic alcohols through a
central ester (or ether) bond (Figure 1).
Fenpropathrin [α-cyano-3-phenoxybenzyl 2,2,3,3-tetrame-
thylcyclopropanecarboxylate] is one of the most popular SPs,
Microorganism-based bioremediation is the most promising
and efficient strategy for removal of environmental pollutants
compared to the conventional physicochemical methods such
as photodecomposition, fenton degradation, ozonation, and
adsorption, which are known for high operating cost and low
22−24
6
efficiency.
There is a growing body of evidence that
used for the control of a broad spectrum of insect pests.
However, a consequence of the increased use of this insecticide
is widespread environmental pollution problems, leading to
Received: October 31, 2013
Revised: February 20, 2014
Accepted: February 20, 2014
Published: February 20, 2014
7,8
serious damages to nontarget organisms. Recent studies
showed that fenpropathrin was detected in nearly all tested
3,4,9−11
agricultural and residential runoff samples.
Such a
©
2014 American Chemical Society
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Figure 1. Molecular structures of SPs.
−
1
xenobiotic compounds can be successfully eliminated by diverse
concentration of 10 g L , and stored in dark bottles at 4 °C prior to
use. The stock solutions were sterilized by membrane filtration and
rationed into medium to get the desired concentrations. At high
concentrations, polysorbate 80 was used as emulsifier to disperse the
possible precipitate in the liquid medium. All other chemicals and
solvents used in this study were of analytical grade.
25−29
microorganisms belonging to different taxonomic groups.
24
Recently, Cycon
isolated from sandy soil successfully removed thiophanate-
26
́
et al. reported that Bacillus sp. TDS-2
−1
methyl (100 mg kg ) from soils within 24 days. Chen et al.
reported that about 80% of the initial dose of β-cypermethrin
Bacterium Used in This Study. The mineral salt medium (MSM)
containing (g L ) (NH ) SO , 2; MgSO ·7H O, 0.2; CaCl ·2H O,
−1
(
50 mg kg ) was removed from the sterilized soils by
−1
4
2
4
4
2
2
2
Streptomyces aureus HP-S-01 within 10 days. A few bacterial
0
.01; FeSO ·7H O, 0.001, Na HPO ·12H O, 1.5; and KH PO , 1.5,
4 2 2 4 2 2 4
30
species, including Sphingobium sp. JZ-2, Sphingobium sp.
was used for the isolation of potential degrading strains. The final pH
was adjusted to 7.5. The bacterial strain DG-02, which was deposited
in the China Center for Type Culture Collection (collection no.
CCTCC M 20111382), was isolated from a pyrethroid-manufacturing
wastewater treatment system using an enrichment culture technique.
In this study, the bacterium was further identified by API 50 CHB
systems (bioMerieux Inc., France) according to the instructions of the
manufacturer.
3
1
32
JQL4-5, Clostridium sp. ZP3, and Ochrobactrum trtici pyd-
3
3
1,
have been reported for the degradation of fenpropathrin.
However, these isolates commonly degraded only a couple of
pyrethroid insecticides, which may limit their use in
bioremediation as various regions are usually contaminated by
34
3
,4,9−11
́
multiple pyrethroid compounds.
Furthermore, little is
known about the biodegradation pathway and catalytic
mechanisms of fenpropathrin.
Inoculum Preparation. The bacterial strain was stored in 15%
glycerol at −80 °C. Before each experiment the strain was thawed and
grown in 250 mL Erlenmeyer flasks containing 50 mL of sterile Luria−
In our previous study, Bacillus sp. DG-02 was isolated from
34
the pyrethroid-manufacturing wastewater treatment system.
−1
Bertani (LB) medium (containing tryptone, 10 g L ; yeast extract, 5 g
In the present study, we demonstrated that strain DG-02 was
capable of degrading not only fenpropathrin but also other
related SPs. The aims of this study were to investigate the
biodegradation kinetics and to determine the bacterial
metabolic products of fenpropathrin. Finally, our findings
highlight the promising potentials and advantages of Bacillus sp.
DG-02 for bioremediation of pyrethroid-contaminated environ-
ments.
−1
−1
L ; NaCl, 10 g L ). At 30 °C, the flasks were placed on a platform
shaker at 180g. The bacterial cells in the late-exponential growth phase
were harvested by centrifugation (5 min, 4000g) at 4 °C and washed
twice in 0.9% normal saline (N-saline) before inoculation. Unless
otherwise stated, the densities of strain DG-02 were adjusted with
sterile N-saline to approximately 1.0 × 10 colony-forming units
CFU) mL . One percent of this suspension was used as the inocula
for the subsequent studies.
Growth and Degradation Experiments. For the growth and
degradation experiments, triplicate cultures were grown in MSM
8
−1
(
MATERIALS AND METHODS
−1
■
supplemented with 50 mg L of fenpropathrin as the sole carbon
Chemicals. Deltamethrin (98%), fenpropathrin (93%), λ-cyhalo-
thrin (95%), β-cypermethrin (94.8%), β-cyfluthrin (95%), bifenthrin
source at 30 °C and 180g on a rotary shaker. A noninoculated culture
served as a control. Samples were collected periodically from the
cultures. The bacterial growth was monitored by counting the CFU
per liter of serial dilutions, and the amount of residual fenpropathrin
was determined by high-performance liquid chromatography (HPLC)
as described below.
(
98%), and permethrin (95%) were obtained from Zhongshan Aestar
Fine Chemical Inc., Ltd., China. The chromatographic grade
acetonitrile were purchased from Sigma-Aldrich, USA. The chemicals
were dissolved in dimethyl sulfoxide (DMSO) or acetone at a stock
2
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−
1
Figure 2. Degradation and utilization of fenpropathrin (50 mg L ) during growth of strain DG-02: (□) fenpropathrin control; (■) fenpropathrin
degradation by strain DG-02; (▲) cell growth. Error bars indicate the standard deviation of three replicates.
The mineral salt media containing different final concentrations of
introduced in triplicate into the soils by drip irrigation to give a final
8
−1
fenpropathrin (25, 50, 100, 200, 400, 600, 800, 1000, and 1200 mg
bacterial count of approximately 1.0 × 10 CFU g of soil. The
triplicate samples of sterile and nonsterile soils without strain DG-02
were kept as controls, respectively. The same amount of pesticide was
applied to these soils. The water contents were adjusted to
approximately 40% of water-holding capacity by the addition of sterile
−1
L ) were inoculated respectively with strain DG-02 and incubated at
0 °C and 180g on a rotary shaker. Each treatment was performed in
triplicate, and fenpropathrin residues were measured at an interval of
2 h.
3
1
2
4
Identification of Metabolites during Fenpropathrin Degra-
deionized water. All of the soil samples were incubated in a darkened
thermostatic chamber maintained at 30 °C for 15 days. Soil treatments
(20 g) were removed aseptically at 0, 3, 6, 9, 12, and 15 days for the
determination of fenpropathrin concentrations.
dation. The metabolic products of fenpropathrin in cell-free filtrates
of strain DG-02 cultures containing different concentrations of
−1
fenpropathrin (50, 100, and 200 mg L ) were extracted and identified
by gas chromatopraphy−mass spectrometry (GC-MS) (Agilent
Chemical Analyses. Pyrethroid quantification was performed on
an Agilent 1100 HPLC equipped with a ternary gradient pump,
programmable variable-wavelength UV detector, column oven, electric
sample valve, and C18 reversed-phase column (Hypersil ODS2 5 μm ×
4.6 mm × 250 mm) with array detection from 190 to 400 nm (total
scan) based on retention time and peak area of the pure standard. The
samples were performed using a mobile phase of 90:10 acetonitrile/
water. Sample injection volume was 10 μL, and mobile phase was
6
890N/5975, USA). The cell-free filtrates were taken at an interval
of 12 h. The same bacterial culture supernatants lacking fenpropathrin
were used as a negative control, and noninoculated control containing
the same amount of fenpropathrin was included as well. The
metabolites were extracted with ethyl acetate from the cell-free
filtrates after acidification to pH 2 with 2 M HCl. The organic layer
3
0,35
was dehydrated, dried, and redissolved in methanol.
After filtration
−1
36,37
with a 0.45 μm membrane (Millipore, USA), the samples were
subjected to GC-MS as described below. The metabolites identified by
mass spectrometry analysis were matched with authentic standard
compounds from the National Institute of Standards and Technology
NIST, USA) library database.
Degradation Kinetics of Various SPs. To determine its ability to
programmed at a flow rate of 1 mL min .
The metabolites of fenpropathrin were confirmed on an Agilent
6890N/5975 GC-MS system equipped with an autosampler and on-
column, split/splitless capillary injection system, with a HP-5MS
capillary column (30.0 m × 250 μm × 0.25 μm) with array detection
from 30 to 500 nm (total scan). The operating conditions were as
follows: the column was held initially at a temperature of 90 °C for 2
(
degrade various SPs, strain DG-02 was inoculated into fresh MSM
−
1
−1
−1
supplemented with 50 mg L deltamethrin, λ-cyhalothrin, β-
cypermethrin, β-cyfluthrin, bifenthrin, and permethrin, respectively.
Triplicate cultures were grown in MSM at 30 °C. Degradation
measurements were carried out periodically as described above.
Biodegradation of Fenpropathrin in Soils. The soil samples
were collected from the top 0−20 cm from a farm in South China
Agricultural University, Guangzhou, southern China, that had never
been treated with fenpropathrin or organic and inorganic fertilizers.
min, then raised at 6 °C min to 150 °C for 1 min, at 10 °C min to
1
−
180 °C for 4 min, and finally at 20 °C min to 260 °C for 10 min.
The temperatures corresponding to the transfer line and the ion trap
were 280 and 230 °C, respectively, and the ionization energy was 70
eV. The injection volume was 1.0 μL with splitless sampling at 250 °C.
−1
38
Helium was used as a carrier gas at a flow rate of 1.5 mL min .
Kinetics Analyses. The substrate inhibition model (eq 1) was
used to fit the specific degradation rate (q) at different initial
concentrations of fenpropathrin.
−1
The detailed physicochemical properties of the soils were (g kg of
dry weight): organic matter, 10.5; total N, 0.5; total P, 0.4; total K,
1
8.2; and pH, 6.9. The soils have a sandy loam texture (sand, 65.0%;
qmax
S
34
q =
silt, 28.0%; clay, 7.0%). In the laboratory, the soils were gently air-
dried to the point of soil moisture suitable for sieving. After sieving to
a maximum particle size of <2 mm, the soils were used in the
bioremediation experiments.
The bioremediation experiment with strain DG-02 was performed
in sterile and nonsterile soils. In the first case, soils were sterilized by
autoclaving for 1 h at 121 °C. The stock solution of fenpropathrin was
sprayed on the surface of 200 g of sterile and nonsterile soils. The
applied dose of insecticide corresponded to a soil concentration of 50
mg kg . After thorough mixing, the bacterial suspension was
2
S + K + (S /K )
(1)
s
i
−
1
qmax is the maximum specific fenpropathrin degradation rate (h ), K
i
−1
is the substrate inhibition constant (mg L ), K is the half-saturation
s
−1
−1
constant (mg L ), and S is the inhibitor concentration (mg L ).
The disappearance of fenpropathrin and other pyrethroids in MSM
or soils was fitted to the first-order kinetic model (eq 2).
2
4
−
kt
−1
C = C × e
(2)
t
0
2
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Figure 3. Relationship between initial fenpropathrin concentration and specific degradation rate by strain DG-02.
C is the amount of substrate at time zero, C is the amount of
substrate at time t, and k and t are the degradation rate constant (h )
and degradation period in hours, respectively.
The algorithm as expressed in eq 3 was used to determine the
theoretical half-life (t1/2) values of fenpropathrin and other
pyrethroids.
Biodegradation of Fenpropathrin with Different
Initial Concentrations. To test the effect of fenpropathrin
concentration on its degradation, strain DG-02 was inoculated
to the media containing various initial fenpropathrin concen-
trations ranging from 25 to 1200 mg L (Figure S1 in the
Supporting Information). Strain DG-02 rapidly degraded and
0
t
−1
−1
ln(2)
k
utilized the added fenpropathrin up to the concentration of
t1/2
=
−1
(3)
1
200 mg L , and a lag period was observed at higher
−1
fenpropathrin concentrations. At a concentration of 25 mg L ,
the residual level of fenpropathrin could not be detected in just
over 72 h. Further loading of the organic compound in
subsequent experiments demonstrated that strain DG-02 was
capable of degrading about 93.3 and 90.4% of fenpropathrin at
a dose of 50 and 100 mg L− in 72 h, respectively, and the strain
completely degraded the added doses in approximately 120 h.
When the concentration was increased to 200, 400, and 600 mg
L , respectively, about 87.6, 84.7, and 80.5% degradations of
this compound were observed in 72 h, respectively, and
complete degradation occurred after a prolonged culture. Over
this time period the cells could utilize only 75.8, 67.2, and
61.2% of fenpropathrin when it was given 800, 1000, and 1200
mg L , respectively. These findings suggest that increased
concentration of fenpropathrin has a slight effect on
biodegradation performance of strain DG-02 with a modest
increase in the duration of lag phase, but did not lead to
complete inhibition or cell death. Previous studies showed that
the pyrethroid-degrading strains usually transform the added
−1
ln 2 is the natural logarithm of 2, and k is the rate constant (h ).
RESULTS AND DISCUSSION
■
Identification of Strain DG-02 Using API Systems. In
our previous studies, stain DG-02 was tentatively identified as
Bacillus sp. based on the morphology and 16S rDNA gene
1
3
4
analysis. In this study, the bacterium was further classified as
Bacillus cereus by API 50 CHB systems (bioMerieux Inc.,
−1
́
France) according to the instructions of the manufacturer, with
good identification (95.3%). It was positive in tests such as
glycerol, maltose, ribose, trehalose, adonitol, cellobiose,
gluconate, and N-acetylglucosamine. It was negative in tests
such as erythritol, sannose, sorbose, rhamnose, melibiose, 5-
keto-D-gluconate, and methyl α-D-mannoside. Detailed bio-
chemical properties of strain DG-02 are presented in Table S1
in the Supporting Information.
Utilization of Fenpropathrin as a Growth Substrate by
Strain DG-02. The growth of strain DG-02 on fenpropathrin
and the ability of this bacterium to degrade fenpropathrin are
shown in Figure 2. Strain DG-02 degraded fenpropathrin
rapidly with about 82% of the initial dose being eliminated
within 48 h. During this time, the number of strain DG-02 cells
was increased to its maximum level. After incubation for 72 h,
approximately 93.3% of the added fenpropathrin was degraded
by strain DG-02 when fenpropathrin was used as the growth
substrate. It is worth mentioning that partial bacterial strain
DG-02 perhaps utilize their dead cells for growth. Finally, the
residual amount of the pesticide was not detectable by HPLC at
−1
−1
39,40
pesticides with a concentration lower than 200 mg L .
At
higher concentrations, however, the metabolic activity of the
reported pyrethroid-degrading strains was subject to complete
41
catabolite repression. Noticeably, our results suggest this
particular isolate could tolerate and degrade fenpropathrin up
−1
to a concentration as high as 1200 mg L . This feature gives
the pesticide degrader a competitive advantage in variable
environments, as they could survive and utilize the pollutants
42
even exposed to a high concentration.
The decrease in fenpropathrin degradation rate following an
increase in the initial fenpropathrin concentration implies that
fenpropathrin may act as a partial inhibitor to strain DG-02. To
address this possibility, the substrate inhibition model (eq 1)
adapted from Luong was used to fit the specific degradation
1
20 h post incubation (data not shown). In contrast with
previous studies, the current study showed that the strain DG-
2 could efficiently degrade fenpropathrin, suggesting this
isolate may be an ideal candidate for bioremediation of a
fenpropathrin-contaminated environment. In the control test,
no significant change in fenpropathrin concentration was
observed in the uninoculated medium.
0
43
rate (q) at different initial concentrations. The relationship
between q and S is shown in Figure 3. The kinetic parameters
of strain DG-02 determined from nonlinear regression using
2
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Table 1. Chromatographic Properties of Metabolites of Fenpropathrin during Degradation by Strain DG-02
matrix laboratory (MATLAB) software package (version 7.8)
with formation of seven new compounds (Figure 4b−h). The
changes in fenpropathrin peak area over time are shown in
Figure S2 in the Supporting Information. The seven
compounds were characterized as 2,2,3,3-tetramethylcyclopro-
panecarboxylic acid phenyl ester, 3,4-dihydroxybenzoic acid, 3-
phenoxybenzoate, 3,4-dimethoxyphenol, 3-phenoxybenzalde-
hyde, α-hydroxy-3-phenoxybenzeneacetonitrile, and phenol,
respectively, on the basis of the similarity of their fragment
retention times and molecular ions to those of corresponding
authentic compounds in the NIST library database (Figure S3
in the Supporting Information). Among these products, 3-
phenoxybenzaldehyde, 3-phenoxybenzoate, and 3,4-dimethox-
ybenzoic acid were also reported during the degradation of
−1
−1
were qmax = 0.05 h and K = 9.0 mg L . The inhibitory effect
s
of fenpropathrin was considered to occur in a linear manner at
−
1
K = 694.8 mg L . The critical inhibitor concentration (S )
i
m
−1
was established to be 78.9 mg L by calculating the square root
of K × K . The coefficient of determination (R ) was 0.9549,
2
i
s
which indicates that the experimental data were well correlated
with the model. As shown in Figure 3, when the initial
−1
concentration of fenpropathrin was <78.9 mg L , the q value
was gradually increased. At higher concentrations, inhibition by
fenpropathrin became substantial and the q value was
proportionally decreased in a dosage-dependent manner. This
reveals that the fenpropathrin degradation activity of strain DG-
02 could be partially inhibited at a high concentration of
3
0,33
fenpropathrin in previous studies,
but the other four
fenpropathrin but may not lead to a complete repression.
Degradation Products and Degradation Pathway of
Fenpropathrin. The predicted chemical structures, retention
times (RT), and characteristic ions of the mass spectra (m/z)
are summarized in Table 1. Compound A, with a RT of 17.293
min, showed a prominent protonated molecular ion at m/z 349,
which is similar to the characteristic parental ion of
fenpropathrin (Figure 4a). Additionally, compound A also has
the same RT as the authentic fenpropathrin. Therefore,
compound A was identified as fenpropathrin. Along with the
degradation process, compound A disappeared concomitantly
metabolic products of fenpropathrin were detected for the first
time in this study. These metabolite concentrations were very
low. We also noted that these metabolites were transient,
suggesting that fenpropathrin was completely degraded by the
strain DG-02 without any noncleavable metabolites at the end
of the experiment. In the negative control lacking fenpropa-
thrin, none of these metabolites was detected. In the
noninoculated control containing the same amount of
fenpropathrin, only fenpropathrin was detected (Figure S4 in
the Supporting Information).
2
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Figure 4. continued
2
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Figure 4. GC-MS analysis of the metabolites produced from fenpropathrin degradation by strain DG-02. (a−h) Characteristic ions of compounds
A−H in GC-MS. The retention times of the compounds were 17.293, 15.919, 11.034, 9.744, 9.576, 8.025, 7.907, and 4.392 min, respectively, which
were identified as fenpropathrin, 2,2,3,3-tetramethylcyclopropanecarboxylic acid phenyl ester, 3,4-dihydroxybenzoic acid, 3-phenoxybenzoate, 3,4-
dimethoxyphenol, 3-phenoxybenzaldehyde, α-hydroxy-3-phenoxybenzeneacetonitrile, and phenol, respectively.
On the basis of the chemical structures of fenpropathrin and
the metabolic products formed during fermentation, we
propose a degradation pathway of fenpropathrin in strain
DG-02 (Figure 5). According to this pathway, fenpropathrin
was initially hydrolyzed by cleavage of the carboxylester linkage
to produce α-hydroxy-3-phenoxybenzeneacetonitrile and
2
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Figure 5. Proposed pathway for degradation of fenpropathrin in strain DG-02.
Figure 6. Degradation kinetics of various SPs by strain DG-02: (◆) deltamethrin; (◇) fenpropathrin; (●) β-cypermethrin; (△) β-cyfluthrin; (▲)
λ-cyhalothrin; (□) permethrin; (■) bifenthrin. Error bars indicate the standard deviation of three replicates.
2
,2,3,3-tetramethylcyclopropanecarboxylic acid phenyl ester.
zoate, which was then subject to diaryl cleavage, resulting in the
formation of 3,4-dihydroxybenzoic acid, 3,4-dimethoxyphenol,
and phenol. However, these compounds were transient.
Eventually, no persistent accumulative product was detected
by GC-MS analysis, indicating that these compounds under-
The intermediate product α-hydroxy-3-phenoxybenzeneaceto-
nitrile was unstable in the environment, which was sponta-
neously converted to 3-phenoxybenzaldehyde. Subsequent
oxidization of 3-phenoxybenzaldehyde yielded 3-phenoxyben-
2
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went aromatic ring cleavage and further metabolism. Very
interestingly, in our previous studies we demonstrated that
strain DG-02 also degraded 3-phenoxybenzoic acid to give 3,4-
neously degrade methyl parathion and fenpropathrin in
MSM. Clostridium sp. ZP3 was reported to be capable of
31
degrading fenpropathrin in liquid medium with the presence of
34
32
dihydroxybenzoic acid, 3,4-dimethoxyphenol, and phenol.
an extra carbon source (glucose). One recently isolated
Clearly, the bacterial strain appears to harbor a complete
metabolic pathway for degradation and metabolism of
fenpropathrin, indicating that the isolate could be an ideal
candidate for bioremediation of the environments contami-
nated by fenpropathrin and the related pyrethroid insecticides.
It was evident from the results that strain DG-02 degrades
fenpropathrin by first cleavage of the carboxylester linkage and
diaryl bond of fenpropathrin. Similar findings were also
observed in biodegradation of other pyrethroid insecticides
fenpropathrin-degrading strain, O. trtici pyd-1, could also utilize
fenpropathrin as a growth substrate and degrade approximately
90% of 100 mg L− of the pesticide in 72 h in liquid culture.
1
33
However, these strains either could degrade only a limited
number of pyrethroids or showed a low degradation efficiency,
which limits their use in bioremediation of environments
contaminated with multiple pyrethroids. It is noteworthy that
strain DG-02 could degrade not only fenpropathrin but also
other pyrethroids, which is rarely seen in other microorganisms.
Previous papers suggest that the bacterial isolates from
Bacillus genus could be the most metabolically active
microorganisms, as they are capable of degrading a wide
variety of xenobiotic aromatic compounds, including thiopha-
3
8,42
such as cyfluthrin and cypermethrin.
were very different from the previous findings of Zhang et al.,
However, our results
32
who reported that Clostridium sp. ZP3 degraded fenpropathrin
with an oxidization process to yield 3,5-dimethylamphetamine,
benzenemethanol, and benzyl alcohol. It was generally regarded
that ester hydrolysis via carboxylesterases was the primary
degradation pathway of various pyrethroids in a multitude of
24
29
46
nate-methyl, chlorpyrifos, and 4-chloro-2-nitrophenol.
The results from this study further expand the metabolic list
of the Bacillus species. In our previous studies, strain DG-02
was found to be highly efficient in degrading 3-phenoxybenzoic
3
0,40,44,45
species, from mammals to insects to microorganisms.
34
The fenpropathrin degradation pathway in strain DG-02
appears to be similar to the initial steps of most environmental
isolates in pyrethroid biodegradation processes, in which
pyrethroids were converted to 2,2,3,3-tetramethylcyclopropa-
necarboxylic acid and 3-phenoxybenzoic acid through hydrol-
acid. 3-Phenoxybenzoic acid is a major product common to
47
most of the pyrethroids. Degradation of this compound by
the same strain that degrades pyrethroids is very important
because 3-phenoxybenzoic acid is generally antimicrobial, and it
would be accumulated if not degradable, which prevents further
3
0,35,39
37
ysis of the carboxylester linkage.
Unfortunately, however,
degradation and may cause growth arrest. Importantly, the
it is not clear whether these microorganisms are capable of
further metabolism of pyrethroids. In this study, we showed
that strain DG-02 could further metabolize the intermediate 3-
phenoxybenzoate by cleavage of the diaryl bond (Figure 5),
leading to complete degradation of the pesticide, which is rarely
seen in other pyrethroid-degrading strains.
ability of strain DG-02 in degrading a wide range of pyrethroids
suggests that this particular isolate has promising potentials and
advantages as a bioremediation organism in removing
pyrethroid residues from various environments as most
contaminated regions were affected by multiple pyrethroid
3
,4,9−11
compounds.
To predict the ability of strain DG-02 in biodegradation of
various substrates in environment, the degradation process was
fitted to the first-order kinetic model (eq 2). The kinetic
parameters for all runs calculated from the equations are
presented in Table 2. In these studies, the degradation rate and
Degradation Kinetics of Various SPs. The abilities of
strain DG-02 to degrade various pyrethroids are shown in
Figure 6. The strain was capable of utilizing all of the
pyrethroids tested. As shown in Figure 6, degradation of all
tested compounds started rapidly at the beginning of
incubation with no apparent lag period. Deltamethrin and
fenpropathrin were the most preferred substrates, with
degradation rates of 94.1 and 93.3% within 72 h of incubation,
respectively. β-Cypermethrin, β-cyfluthrin, and λ-cyhalothrin
were degraded relatively more slowly than deltamethrin and
fenpropathrin, with degradation rates of 89.2, 85.6, and 82.7%,
respectively. Bifenthrin and permethrin were the most
persistent; only 65.1 and 63.6% of the added substrates were
degraded under the same experimental conditions, suggesting
that absence of the cyano group may cause a substantial
reduction in the hydrolysis rate. These results contrast with the
previous findings that degradation reduction in pyrethroid
Table 2. Kinetic Parameters of Degradation of Various SPs
by Strain DG-02
treatment
regression eq
k (h−1)
t1/2 (h)
R2
deltamethrin
fenpropathrin
β-cypermethrin
β-cyfluthrin
λ-cyhalothrin
bifenthrin
C = 52.0e−
0.0355t
0.0355
0.0315
0.0286
0.0277
0.0234
0.0155
0.0160
19.5
22.0
24.2
25.0
29.6
44.7
43.3
0.9826
0.9735
0.9657
0.9688
0.9564
0.9574
0.9718
t
C = 52.3e−
0.0315t
0.0286t
0.0277t
0.0234t
0.0155t
0.0160t
t
Ct = 54.8e−
Ct = 53.2e−
Ct = 51.9e−
Ct = 52.0e−
Ct = 50.7e−
permethrin
33
compounds with a cyano group is due to its toxic effect. Our
results provide a strong endorsement to the previous view that
different capacities of various microorganisms to utilize
pyrethroid compounds could be attributed to a number of
factors, including the differences in substrate transportation,
enzyme specificity, and molecular structures of these
the substrate concentration were in direct proportion, and the
degradation process corresponded to the first-order kinetic
2
model, with an R ranging from 0.9564 to 0.9826, indicating
that the experimental data were well-correlated with the model.
The degradation process was characterized by a k ranging from
3
4
−1
compounds.
0.0160 to 0.0355 h and a t1/2 varying from 19.5 to 43.3 h
Several papers on the microbial degradation of fenpropathrin
have been published. Sphingobium sp. JZ-2 could use
fenpropathrin as the sole carbon source in MSM and could
degrade >80% of the added pesticide at a concentration of 50
mg L after 4 days of incubation. A genetically engineered
microorganism named JQL4-5-mpd was also able to simulta-
(Table 3). Given that the reported t1/2 values for various
pyrethroids in water or soil are usually between 17 and 600
1
days, addition of strain DG-02 significantly shortened the t
1
/2
for pyrethroids, suggesting that this strain is suitable for the
efficient and rapid degradation of pyrethroid residues and
cleanup of contaminated environments.
−1
30
2
155
dx.doi.org/10.1021/jf404908j | J. Agric. Food Chem. 2014, 62, 2147−2157

Journal of Agricultural and Food Chemistry
Article
Table 3. Kinetic Parameters of Degradation of
Fenpropathrin in Sterile and Nonsterile Soils Inoculated
with Strain DG-02
AUTHOR INFORMATION
Corresponding Authors
(G.Z.) E-mail: guohuazhong@scau.edu.cn
(L.-H.Z.) Phone: +86-20-85288229. Fax: +86-20-85280292.
E-mail: lianhui@imcb.a-star.edu.sg.
■
*
*
k
t1/2
treatment
regression eq
(day−1) (days)
R2
sterile soils +
C = 49.8e−
0.0098t
0.0098
0.0187
0.0981
70.7
37.1
7.1
0.9791
Funding
t
fenpropathrin
Financial support for some of this research was received from
the Guangdong Hopson-Pearl River Education Development
Foundation (HPEDF).
nonsterile soils +
fenpropathrin
C = 49.9e−
0.00187t
0.0981t
0.9913
0.9849
t
sterile soils +
fenpropathrin +
DG-02
C = 51.6e−
t
Notes
The authors declare no competing financial interest.
nonsterile soils +
fenpropathrin +
DG-02
C = 51.0e−
0.1281t
0.1281
5.4
0.9916
t
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