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Journal of Hazardous Materials 297 (2015) 17–24 Journal of Hazardous Materials 297 (2015) 17–24 View metadata, citation and similar papers at core.ac.uk brought to you by CORE Contents lists available at ScienceDirect provided by Elsevier - Publisher Connector Journal of Hazardous Materials journal homepage: www.elsevier.com/locate/jhazmat Rapid biodegradation of organophosphorus pesticides by Stenotrophomonas sp. G1 Shuyan Deng a, Yao Chen a, Daosheng Wang b, Taozhong Shi a, Xiangwei Wu a, Xin Ma a, Xiangqiong Li a, Rimao Hua a,∗, Xinyun Tang b, Qing X. Li c a Key Laboratory of Agri-food Safety of Anhui Province, Lab of Quality & Safety and Risk Assessment for Agro-products on Storage and Preservation (Hefei), Ministry of Agriculture, School of Resource and Environment, Anhui Agricultural University, Hefei 230036, China b School of Life Science, Anhui Agricultural University, Hefei 230036, China c Department of Molecular Biosciences and Bioengineering, University of Hawaii at Manoa, 1955 East–West Road, Honolulu, HI 957822, USA highlights graphical abstract • Stenotrophomonas sp. G1 was iso- lated from chlorpyrifos contaminated sludge. • Strain G1 is closest to Stenotrophomonas acidaminiphila. • Strain G1 can efficiently degrade 8 organophosphorus pesticides (OPs). • Intracellular methyl parathion hydrolase is responsible for the OP degradation. • Three factors were orthogonally opti- mized for degradation of methyl parathion. article info abstract Article history: Organophosphorus insecticides have been widely used, which are highly poisonous and cause serious Received 19 September 2014 concerns over food safety and environmental pollution. A bacterial strain being capable of degrading O,O- Received in revised form 14 April 2015 dialkyl phosphorothioate and O,O-dialkyl phosphate insecticides, designated as G1, was isolated from Accepted 17 April 2015 sludge collected at the drain outlet of a chlorpyrifos manufacture plant. Physiological and biochemical Available online 20 April 2015 characteristics and 16S rDNA gene sequence analysis suggested that strain G1 belongs to the genus Stenotrophomonas. At an initial concentration of 50 mg/L, strain G1 degraded 100% of methyl parathion, Keywords: methyl paraoxon, diazinon, and phoxim, 95% of parathion, 63% of chlorpyrifos, 38% of profenofos, and 34% Biodegradation of triazophos in 24 h. Orthogonal experiments showed that the optimum conditions were an inoculum Bioremediation ◦ Chlorpyrifos volume of 20% (v/v), a substrate concentration of 50 mg/L, and an incubation temperature in 40 C. p- Methyl parathion hydrolase Nitrophenol was detected as the metabolite of methyl parathion, for which intracellular methyl parathion Organophosphorus pesticides hydrolase was responsible. Strain G1 can efficiently degrade eight organophosphorus pesticides (OPs) and Stenotrophomonas sp. G1 is a very excellent candidate for applications in OP pollution remediation. © 2015 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). ∗ Corresponding author. Tel.: +86 551 65786320; fax: +86 551 65786296. E-mail address: [email protected] (R. Hua). http://dx.doi.org/10.1016/j.jhazmat.2015.04.052 0304-3894/© 2015 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 18 S. Deng et al. / Journal of Hazardous Materials 297 (2015) 17–24 1. Introduction 2. Materials and methods 2.1. Sludge sample and cultivation media Some organophosphorus pesticides (OPs) are highly toxic and are still widely used for pest insect control. Wide use of OPs A sludge sample was collected at the outlet of wastewater causes serious concerns over food safety and environmental drainage system in a chlorpyrifos manufacture plant, Nantong pollution. In the recent years, various bacterial strains were iso- City, Jiangsu Province, China. Mineral salt medium (MSM), beef lated and reported for biodegradation of OPs. Serratia sp. SPL-2 extract-peptone medium, and chlorpyrifos-selective medium were can degrade methidathion [1]. Pseudomonas aeruginosa Is-6 can prepared for isolation and screening of chlorpyrifos-degrading bac- degrade acephate, methamidophos, methyl parathion, dimethoate, teria [24]. and malathion [2]. Biodegradation of chlorpyrifos by soil bacterial communities comprising seven different isolates of Pseudomonas, 2.2. Reagents and pesticides Agrobacterium and Bacillus has been investigated [3]. Bacillus cereus, Bacillus subtilis, Brucella melitensis, Klebsiella species, Pseudomonas N,O-Bis (trimethylsilyl) trifluoroacetamide was purchased from aeroginosa, Pseudomonas fluorescence, and Serratia marcescens are Aladdin Reagents Co., Ltd., Shanghai, China. The rTaq DNA capable of degrading 46–72% of chlorpyrifos as a sole carbon polymerase and DNA marker were purchased from Takara Biotech- source in an aqueous medium after an incubation of 20 days [4]. nology Co., Ltd., Dalian, China. Chlorpyrifos (48%) emulsifiable Many factors can affect bacterial degradation of OPs, which include concentrate was purchased from Jiangsu Baoling Chemical Co., Ltd., water-holding capacity of soil, temperature, pH, and even aging Nantong, China. Chlorpyrifos (95%) was purchased from Shandong of pesticides in soils prior to inoculation. In a study of Enter- Kunfeng Biochemical Co., Ltd., Binzhou, China. Parathion (99.4%), obacter sp., aging of chlorpyrifos resulted in approximately 10% p-nitrophenol (99%), methyl parathion (98.9%), acephate (99%), of it being persistent in soil [5]. The diazinon-degrading Serratia methamidophos (99%), isocarbophos (99%), malathion (97.4%), and marcescens can degrade chlorpyrifos, fenitrothion, and parathion profenofos (96.9%) were purchased from Beijing Helishun Technol- [6]. Stenotrophomonas sp. SMSP-1 can completely degrade methyl ogy Co., Ltd., Beijing, China. Phoxim (98%), methyl paraoxon (98%), parathion, fenitrothion and ethyl parathion, and degrade 37.8% of triazophos (98%), chlorpyrifos (99%), and diazinon (98%) were pur- fenthion and 59.7% of phoxim, but cannot degrade chlorpyrifos chased from Dr. Ehrenstorfer GmbH, Germany. All other reagents at 20 mg/L [7]. Stenotrophomonas sp. PF32 can efficiently degrade were of analytical grade. methyl parathion as well as phoxim, fenthion, sumithion, tri- azophos, and chlorpyrifos. Strain PF32 degraded about 99% of 2.3. Screening, isolation, and purification of 100 mg/L methyl parathion, fenthion in 24 h, 99% of 100 mg/L fen- chlorpyrifos-degrading bacteria itrothion at 18 h, 99% of 100 mg/L phoxim in 30 h, 97% of 100 mg/L triazophos in 42 h, and 97% of 100 mg/L chlorpyrifos in 48 h [8]. The sludge sample in 5 mL was transferred into 95 mL of liquid Stenotrophomonas maltophilia MHF ENV20 can degrade chlorpyri- MSM containing 100 mg/L chlorpyrifos emulsifiable concentrate, fos with a half-life of 96 h and its metabolite trichlorophenol as followed by incubation at 28 ◦C on a rotary shaker at 120 r/min. well as diethyl thiophosphate salt [9]. Stenotrophomonas sp. YC-1 After cultivation for 5 days, an aliquot of culture solution was can also utilize chlorpyrifos as a sole carbon source, but cannot fur- sampled, diluted and spread on the chlorpyrifos-selective medium ther degrade its metabolite trichlorophenol. YC-1 can completely agar plates containing 500 mg/L of chlorpyrifos. After incubation degrade 100 mg/L of chlorpyrifos in 24 h [10]. Stenotrophomonas at 28 ◦C, single colonies with a clearing zone were picked asepti- sp. DSP-4 can completely degrade 100 mg/L chlorpyrifos in 24 h cally for further plate cultivation until single colonies of uniform [11]. morphology were obtained. The substrate specificity varies among bacterial species. Methyl parathion hydrolase is an important organophosphorus 2.4. Degradation of chlorpyrifos and other OPs hydrolase that exists in many bacterial species. To date, the hydrolase has been found in methyl parathion-degrading Pseu- The isolates showing a clearing zone were transferred into liq- daminobacter salicylatoxidans mp-1, Achromobacter xylosoxidans uid beef extract-peptone medium and grown to a stationary phase. mp-2, Ochrobactrum tritici mp-3, B. melitensis mp-7, Plesiomonas sp. Cells were harvested by centrifugation of 20-mL culture solution for M6, Sphingopyxis sp. DLP-2, Pseudomonas stutzeri HS-D36 [12–15], 5 min, washed twice with normal saline, and then re-suspended ␮ chlorpyrifos-degrading Cupriavidus sp. DT-1 [16] and phoxim- in 20 mL of MSM. An aliquot of 50 L of chlorpyrifos solution degrading Delftia sp. XSP-1 [17]. Different bacteria species have (5 mg/mL in petroleum ether) was added to the bottom of test tube. different specificity of substrate utilization. Methyl parathion is After complete volatilization of petroleum ether, 4.5 mL of MSM and 0.5 mL of bacterial cell suspension were added, followed by the optimum substrate for methyl parathion hydrolase purified ◦ from Pseudomonas sp. WBC-3 [18], which can degrade chlorpyri- incubation at 37 C. Samples were taken for determination of chlor- fos, ethyl parathion, and sumithion [19,20]. Burkholderia sp. FDS-1 pyrifos degradation. Strain G1 was selected for further degradation can degrade methyl parathion, parathion and sumithion, but not studies. chlorpyrifos, methamidophos, phoxim and triazophos [21]. Methyl After growth in liquid beef extract-peptone medium for 24 h, parathion hydrolase is an intracellular enzyme in some strains G1 cells were harvested by centrifugation, washed twice with nor- [21,22] and cell membrane
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