Abstract
A bacterial strain NSA02, isolated from contaminated soil and identified as Pseudomonas nitroreducens based on partial 16S rDNA gene sequence analysis and BIOLOG microbiology analysis, was used to study biodegradation of nicosulfuron in the culture medium. The optimal degradation conditions were determined to be 30 °C and pH 7.0. Batch tests were performed for seven different initial substrate concentrations to observe substrate degradation and associated cell growth. The biodegradation kinetics was found to follow a first-order model with regression values greater than 0.98. Specific degradation rate and specific growth rate of bacterial cells were observed to follow substrate inhibition kinetics, and the maximum values of both rates were observed at 100 mg L−1 of nicosulfuron concentration. Kinetic parameters of three substrate inhibition models (Haldane, Aiba–Edwards and Teissier–Edwards) were fitted to the relationship between those rates and substrate concentrations. With the date obtained, Haldane and Teissier–Edwards models provide better representation when compared to Aiba–Edwards model. Inoculating nicosulfuron-treated soil samples with strain NSA02 resulted in a 5–6 times higher rate of nicosulfuron removal than that in non-inoculated soil. Five metabolites of nicosulfuron degradation were detected and identified by liquid chromatography mass spectrometry, and three possible biotransformation pathways were proposed. These results highlight the potential of the isolated bacterium to be used in the bioremediation of nicosulfuron-contaminated soils.
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References
Arora PK, Bae H (2014) Biotransformation and chemotaxis of 4-chloro-2-nitrophenol by Pseudomonas sp. JHN. Microb Cell Fact 13(1):110. https://doi.org/10.1186/s12934-014-0110-7
Arora PK, Srivastava A, Singh VP (2014) Degradation of 4-chloro-3-nitrophenol via a novel intermediate, 4-chlororesorcinol by Pseudomonas sp. JHN. Sci Rep 4(3):4475. https://doi.org/10.1038/srep04475
Battaglin WA, Furlong ET, Burkhardt MR, Peter CJ (2000) Occurrence of sulfonylurea, sulfonamide, imidazolinone, and other bherbicides in rivers, reservoirs and groundwater in the midwestern United States, 1998. Sci Total Environ 248:123–133. https://doi.org/10.1016/S0048-9697(99)00536-7
Brusa T, Ferrari F, Bolzacchini E, Rindone B (2001) Study of the microbiological degradation of bensulfuronmethyl. Ann Microbiol 51(2):189–199
Carles L, Joly M, Bonnemoy F, Leremboure M, Batisson I, Besse-Hoggan P (2017) Identification of sulfonylurea biodegradation pathways enabled by a novel nicosulfuron-transforming strain Pseudomonas fluorescens SG-1: toxicity assessment and effect of formulation. J Hazard Mater 324:184–193. https://doi.org/10.1016/j.jhazmat.2016.10.048
Castro-Gutiérrez V, Masís-Mora M, Caminal G, Vicent T, Carazo-Rojas E, Mora-López M, Rodríguez-Rodríguez CE (2016) A microbial consortium from a biomixture swiftly degrades high concentrations of carbofuran in fluidized-bed reactors. Process Biochem 51(10):1585–1593. https://doi.org/10.1016/j.procbio.2016.07.003
Cycoń M, Mrozik A, Piotrowska-Seget Z (2017) Bioaugmentation as a strategy for the remediation of pesticide-polluted soil: a review. Chemosphere 172:52–71. https://doi.org/10.1016/j.chemosphere.2016.12.129
Ding F, Liu W, Li N, Zhang L, Sun Y (2010) Complex of nicosulfuron with human serum albumin: a biophysical study. J Mol Struct 975(1):256–264. https://doi.org/10.1016/j.molstruc.2010.04.033
Edwards VH (1970) The influence of high substrate concentration on microbial kinetics. Biotechnol Bioeng 12:679–712. https://doi.org/10.1002/bit.260120504
Gu LF, Jiang JD, Li XH, Ali SW, Li SP (2007) Biodegradation of ethametsulfuron-methyl by Pseudomonas sp. SW4 isolated from contaminated soil. Curr Microbiol 55:420–426. https://doi.org/10.1007/s00284-007-9011-x
Haldane JBS (1930) Enzymes. Longman, London
He YH, Shen DS, Fang CR, Zhu YM (2006) Rapid biodegradation of metsulfuron-methyl by a soil fungus in pure cultures and soil. World J Microb Biot 22(10):1095–1104. https://doi.org/10.1007/s11274-006-9148-y
Hernández M, Villalobos P, Morgante V, González M, Reiff C, Moore E, Seeger M (2008) Isolation and characterization of a novel simazine-degrading bacterium from agricultural soil of central Chile, Pseudomonas sp. MHP41. FEMS Microbiol Lett 286(2):184–190. https://doi.org/10.1111/j.1574-6968.2008.01274.x
Hussain S, Arshad M, Saleem M, Khalid A (2007) Biodegradation of α- and β-endosulfan by soil bacteria. Biodegradation 18(6):731–740. https://doi.org/10.1007/s10532-007-9102-1
Joly P, Bonnemoy F, Charvy JC, Bohatier J, Mallet C (2013) Toxicity assessment of the maize herbicides S-metolachlor, benoxacor, mesotrione and nicosulfuron, and their corresponding commercial formulations, alone and in mixtures, using the Microtox(®) test. Chemosphere 93(10):2444–2450. https://doi.org/10.1016/j.chemosphere.2013.08.074
Karpouzas DG, Morgan JA, Walker A (2000) Isolation and characterisation of ethoprophos-degrading bacteria. FEMS Microbiol Ecol 33(3):209–218. https://doi.org/10.1111/j.1574-6941.2000.tb00743.x
Kong J, Wang H, Liang L, Li L, Xiong G, Hu Z (2017) Phenanthrene degradation by the bacterium Pseudomonas stutzeri JP1 under low oxygen condition. Int Biodeterior Biodegrad 123:121–126. https://doi.org/10.1016/j.ibiod.2017.06.001
Koutny M, Ruzicka J, Chlachula J (2003) Screening for phenol-degrading bacteria in the pristine soils of south Siberia. Appl Soil Ecol 23(1):79–83. https://doi.org/10.1016/S0929-1393(03)00005-2
Lafontaine Y, Beauvais C, Cessna AJ, Gagnon P, Hudon C, Poissant L (2014) Sulfonylurea herbicides in an agricultural catchment basin and its adjacent wetland in the St. Lawrence River basin. Sci Total Environ 479–480:1–10. https://doi.org/10.1016/j.scitotenv.2014.01.094
Lakshmi CV, Kumar M, Khanna S (2008) Biotransformation of chlorpyrifos and bioremediation of contaminated soil. Int Biodeterior Biodegrad 62:204–209. https://doi.org/10.1016/j.ibiod.2007.12.005
Leboulanger C, Rimet F, de Lacotte M, Bérard A (2001) Effects of atrazine and nicosulfuron on freshwater microalgae. Environ Int 26:131–135. https://doi.org/10.1016/S0160-4120(00)00100-8
Lima D, Viana P, Chelinho S, Costa C, Ribeiro R, Sousa JP, Fialho AM, Viegas CA (2009) Evaluating a bioremediation tool for atrazine contaminated soils in open soil microcosms: the effectiveness of bioaugmentation and biostimulation approaches. Chemosphere 74(2):187–192. https://doi.org/10.1016/j.chemosphere.2008.09.083
Lu XH, Kang ZH, Tao B, Wang YN, Dong JG, Zhang JL (2012) Degradation of nicosulfuron by Bacillus subtilis YB1 and Aspergillus niger YF1. Appl Biochem Microbiol 48:460–466. https://doi.org/10.1134/S0003683812050079
Ma JP, Wang Z, Lu P, Wang HJ, Ali SW, Li SP, Huang X (2009) Biodegradation of the sulfonylurea herbicide chlorimuron-ethyl by the strain Pseudomonas sp. LW3. FEMS Microbiol Lett 296:203–209. https://doi.org/10.1111/j.1574-6968.2009.01638.x
Mandelbaum RT, Allan DL, Wackett LP (1995) Isolation and characterization of a Pseudomonas sp. that mineralizes the s-triazine herbicide atrazine. Appl Environ Microbiol 61(4):1451–1457
Martino CD, López NI, Iustman LJR (2012) Isolation and characterization of benzene, toluene and xylene degrading Pseudomonas sp. selected as candidates for bioremediation. Int Biodeter Biodegr 67(2):15–20. https://doi.org/10.1016/j.ibiod.2011.11.004
Molina MC, González N, Bautista LF, Sanz R, Simarro R, Sánchez I, Sanz JL (2009) Isolation and genetic identification of PAH degrading bacteria from a microbial consortium. Biodegradation 20(6):789–800. https://doi.org/10.1007/s10532-009-9267-x
Oliveira RS, Koskinen WC, Ferreira FA (2001) Sorption and leaching potential of herbicides on Brazilian soils. Weed Res 41:97–110. https://doi.org/10.1046/j.1365-3180.2001.00219.x
Pandey G, Dorrian SJ, Russell RJ, Oakeshott JG (2009) Biotransformation of the neonicotinoid insecticides imidacloprid and thiamethoxam by Pseudomonas sp. 1G. Biochem Biophys Res Commun 380(3):710–714. https://doi.org/10.1016/j.bbrc.2009.01.156
Regitano JB, Koskinen WC (2008) Characterization of nicosulfuron availability in aged soils. J Agric Food Chem 56(14):5801–5805. https://doi.org/10.1021/jf800753p
Saikia N, Das SK, Patel BK, Niwas R, Singh A, Gopal M (2005) Biodegradation of beta-cyfluthrin by Pseudomonas stutzeri strain S1. Biodegradation 16(6):581–589. https://doi.org/10.1007/s10532-005-0211-4
Sarmah AK, Sabadie J (2002) Hydrolysis of sulfonylurea herbicides in soils and aqueous solutions: a review. J Agric Food Chem 50(22):6253–6265. https://doi.org/10.1021/jf025575p
Song J, Gu J, Zhai Y, Wu W, Wang H, Ruan Z, Shi Y, Yan Y (2013) Biodegradation of nicosulfuron by a Talaromyces flavus LZM1. Bioresour Technol 140:243–248. https://doi.org/10.1016/j.biortech.2013.02.086
Tang Q, Zhao Z, Liu Y, Wang N, Wang B, Wang Y, Zhou N, Liu S (2012) Augmentation of tribenuron methyl removal from polluted soil with Bacillus sp. strain BS2 and indigenous earthworms. J Environ Sci 24(8):1492–1497. https://doi.org/10.1016/S1001-0742(11)60947-9
Wang L, Chi X, Zhang J, Sun D, Zhou N (2014) Bioaugmentation of a methyl parathion contaminated soil with Pseudomonas sp. strain WBC-3. Int Biodeter Biodegr 87:116–121. https://doi.org/10.1016/j.ibiod.2013.11.008
Wang L, Zhang X, Li Y (2016) Degradation of nicosulfuron by a novel isolated bacterial strain Klebsiella sp. Y1: condition optimization, kinetics anddegradation pathway. Water Sci Technol 73:2896–2903. https://doi.org/10.2166/wst.2016.140
Xu J, Li X, Xu Y, Qiu L, Pan C (2009) Biodegradation of pyrazosulfuron-ethyl by three strains of bacteria isolated from contaminated soils. Chemosphere 74(5):682–687. https://doi.org/10.1016/j.chemosphere.2008.09.078
Ye G, Zhang W, Cui X, Pan C, Jiang S (2006) Determination of ten sulfonylurea herbicides in soil samples by liquid chromatography with electrospray ionization mass spectrometric detection. Chin J Anal Chem 34(9):1207–1212. https://doi.org/10.1016/S1872-2040(07)60001-2
Zang H, Yu Q, Lv T, Cheng Y, Feng L, Cheng X, Li C (2016) Insights into the degradation of chlorimuron-ethyl by Stenotrophomonas maltophilia D310-3. Chemosphere 144:176–184. https://doi.org/10.1016/j.chemosphere.2015.08.073
Zhang C, Wang S, Yan Y (2011) Isomerization and biodegradation of beta-cypermethrin by Pseudomonas aeruginosa CH7 with biosurfactant production. Bioresour Technol 102(14):7139–7146. https://doi.org/10.1016/j.biortech.2011.03.086
Zhang H, Mu W, Hou Z, Wu X, Zhao W, Zhang X, Pan H, Zhang S (2012) Biodegradation of nicosulfuron by the bacterium Serratia marcescens N80. J Environ Sci Health B 47:153–160. https://doi.org/10.1080/03601234.2012.632249
Zhang J, Chen Y, Fang T, Zhou N (2013) Co-metabolic degradation of tribenuron methyl, a sulfonylurea herbicide, by Pseudomonas sp. strain NyZ42. Int Biodeter Biodegr 76:36–40. https://doi.org/10.1016/j.ibiod.2012.06.019
Zhao W, Wang C, Xu L, Zhao C, Liang H, Qiu L (2015) Biodegradation of nicosulfuron by a novel Alcaligenes faecalis strain ZWS11. J Environ Sci 35:151–162. https://doi.org/10.1016/j.jes.2015.03.022
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The work was supported by the Innovative Scientific Research Fund of Sichuan Province (No. 2014CXSF-022).
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Zhao, H., Zhu, J., Liu, S. et al. Kinetics study of nicosulfuron degradation by a Pseudomonas nitroreducens strain NSA02. Biodegradation 29, 271–283 (2018). https://doi.org/10.1007/s10532-018-9828-y
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DOI: https://doi.org/10.1007/s10532-018-9828-y