Dissipation of butachlor by a new strain of Pseudomonas sp. isolated from paddy soils

Document Type : Original Research Paper

Authors

1 Department of Soil Science, Faculty of Agricultural Engineering and Technology, College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran

2 Department of Plant Protection, Faculty of Agricultural Science and Engineering, College of Agriculture and Natural Resources, University of Tehran, Karaj, Iran

Abstract

Butachlor (BUT) is a chloroacetanilide herbicide widely applied to rice paddies to control annual grass and broad-leaf weeds. A BUT-degrading bacterial strain (PK) was isolated from paddy soils. Biochemical and 16S rRNA sequencing characteristics confirmed the strain as Pseudomonas aeruginosa (99% resemblance). The isolate dissipated BUT (100 μg/mL) in an M9 liquid medium with a rate of 0.5 ± 0.03 day-1 and DT50 and DT90 of 1.38 ± 0.10 days and 4.58 ± 0.32 days, respectively. Soil dissipation of BUT was investigated under flooded conditions. In sterile soils, the isolate increased the dissipation of BUT (200 μg/g) (DT50 = 12.38 ± 1.83 days, DT90 = 41.12 ± 6.09 days, k = 0.06 ± 0.01 day-1) compared to sterile non-inoculated samples (DT50 = 26.87 ± 2.82 days, DT90 = 89.25 ± 9.36 days, k = 0.03 ± 0.00 day-1). In non-inoculated non-sterile soil experiments, the dissipation of BUT was faster (DT50 = 15.17 ± 2.11 days, DT90 = 50.38 ± 7.02 days, k = 0.05 ± 0.00 day-1) compared to non-inoculated sterile ones, and inoculating the isolate accelerated the removal of BUT in non-sterile soils significantly (DT50 = 8.03 ± 1.20 days, DT90 = 26.68 ± 3.97 days, k = 0.09 ± 0.01 day-1). BUT inhibited soil respiration (SR) initially for 5 days, followed by an increase until day 20. The increase in SR was more pronounced in the co-presence of BUT and the isolate. The results of this research suggest P. aeruginosa PK as a suitable candidate for BUT bioremediation.

Keywords


Abd-Alrahman, S. H. and Salem-Bekhit, M. M. (2013). Microbial biodegradation of butachlor pollution (obsolete pesticide Machete 60% EC). Afr. J. Microbiol. Res., 7(4); 330-335.
Akan, J. C., Inuwa, L. B., Chellube, Z. M., Mahmud, M. M. and Abdulrahman, F. I. (2019). Assessment of the levels of herbicide residues in fish samples from Alau Dam, Maiduguri, Borno, State, Nigeria. Environ. Chem., 3(2); 53-58. Anastassiades, M., Lehotay, S. J., Štajnbaher, D. and Schenck, F. J. (2003). Fast and easy multiresidue method employing acetonitrile extraction/partitioning and “dispersive solid-phase extraction” for the determination of pesticide residues in produce. J. AOAC Int., 86(2); 412-431. Anzai, Y., Kim, H., Park, J. Y., Wakabayashi, H. and Oyaizu, H. (2000). Phylogenetic affiliation of the pseudomonads based on 16S rRNA sequence. Int. J. Syst. Evol. Microbiol., 50(4); 1563-1589. Armanpour, S. and Bing, L. (2015). Adsorption of herbicide butachlor in cultivated soils of Golestan Province, Iran. J. Geosci. Environ. Prot., 3(3); 15-24. Ateeq, B., Farah, M. A. and Ahmad, W. (2006). Evidence of apoptotic effects of 2, 4-D and butachlor on walking catfish, Clarias batrachus, by transmission electron microscopy and DNA degradation studies. Life Sci., 78(9); 977-986. Berns, A. E., Philipp, H., Narres, H. D., Burauel, P., Vereecken, H. and Tappe, W. (2008). Effect of gamma‐sterilization and autoclaving on soil organic matter structure as studied by solid state NMR, UV and fluorescence spectroscopy. Eur. J. Soil Sci., 59(3); 540-550. Crouzet, O., Batisson, I., Besse-Hoggan, P., Bonnemoy, F., Bardot, C., Poly, F., Bohatier, J. and Mallet, C. (2010). Response of soil microbial communities to the herbicide mesotrione: a dose-effect microcosm approach. Soil Biol. Biochem., 42(2); 193-202. Cycoń, M. and Piotrowska-Seget, Z. (2009). Changes in bacterial diversity and community structure following pesticides addition to soil estimated by cultivation technique. Ecotoxicol., 18(5); 632-642. Cycoń, M., Wójcik, M. and Piotrowska-Seget, Z. (2009). Biodegradation of the organophosphorus insecticide diazinon by Serratia sp. and Pseudomonas sp. and their use in bioremediation of contaminated soil. Chemosphere, 76(4); 494-501. Dungan, R. S., Ibekwe, A. M. and Yates, S. R. (2003). Effect of propargyl bromide and 1, 3-dichloropropene on microbial communities in an organically amended soil. FEMS Microbiol. Ecol., 43(1); 75-87. Dwivedi, S., Saquib, Q., Al-Khedhairy, A. A. and Musarrat, J. (2012). Butachlor induced dissipation of mitochondrial membrane potential, oxidative DNA damage and necrosis in human peripheral blood mononuclear cells. Toxicol., 302(1); 77-87. Dwivedi, S., Singh, B. R., Al‐Khedhairy, A. A., Alarifi, S. and Musarrat, J. (2010). Isolation and characterization of butachlor‐catabolizing bacterial strain Stenotrophomonas acidaminiphila JS‐1 from soil and assessment of its biodegradation potential. Lett. Appl. Microbiol., 51(1); 54-60. Egea, T. C., da Silva, R,, Boscolo, M., Rigonato, J., Monteiro, D. A., Grünig, D., da Silva, H., van der Wielen, F., Helmus, R., Parsons, J. R. and Gomes, E. (2017). Diuron degradation by bacteria from soil of sugarcane crops. Heliyon, 3(12); e00471. El-Fantroussi, S. (2000). Enrichment and molecular characterization of a bacterial culture that degrades methoxy-methyl urea herbicides and their aniline derivatives. Appl. Environ. Microbiol., 66(12); 5110-5115. European Commission. (2006). Quality control procedures for pesticide residues analysis. Document No. SANCO/10232/2006, SANCO: Brussels, Belgium. Filimon, M. N., Vlad, D. C., Verdes, D., Dumitrascu, V. and Popescu, R. (2015). Enzymatic and biological assessment of sulfonylurea herbicide impact on soil bacterial communities. Afr. J. Agric. Res., 10(14); 1702-1708.
Froment, A. (1972). Soil respiration in a mixed oak forest. Oikos, 23; 273-277. Geng, B. R., Yao, D. and Xue, Q. Q. (2005). Genotoxicity of pesticide dichlorvos and herbicide butachlor in Rhacophorus megacephalus tadpoles. Acta Zool. Sin., 51(3); 447-454. Geng, B., Lin, L., Zhang, Q. and Zhung, B. (2010). Genotoxicity of the pesticide dichlorvos and herbicide butachlor on Rana zhenhaiensis tadpoles. Asian Herpatol. Res., 1(2); 118-122.
Pourbabaei, A. A., et al.
634
Gomez, E., Ferreras, L., Lovotti, L. and Fernandez, E. (2009). Impact of glyphosate application on microbial biomass and metabolic activity in a Vertic Argiudoll from Argentina. Eur. J. Soil Biol., 45(2); 163-167. Heinonen-Tanski, H., Mettälä, A. and Silvo, R. (1984). Measuring methods for soil microbial activity and biomass. Agric. Food Sci., 56(3); 199-203. Iwafune, T., Inao, K., Horio, T., Iwasaki, N., Yokoyama, A. and Nagai, T. (2010). Behavior of paddy pesticides and major metabolites in the Sakura River, Ibaraki, Japan. J. Pestic. Sci., 35(2); 114–123. Kim, N. H., Kim, D. U., Kim, I. and Ka, J. O. (2013). Syntrophic biodegradation of butachlor by Mycobacterium sp. J7A and Sphingobium sp. J7B isolated from rice paddy soil. FEMS Microbiol. Lett., 344(2); 114-120. Krishna, K. R. and Philip, L. (2011). Bioremediation of single and mixture of pesticide-contaminated soils by mixed pesticide-enriched cultures. Appl. Biochem. Biotechnol., 164(8); 1257-1277. Li-feng, G., Jian-dong, J., Xiao-hui, L., Ali, S. W. and Shun-Peng, L. (2007). Biodegradation of ethametsulfuron-methyl by Pseudomonas sp. SW4 isolated from contaminated soil. Curr. Microbiol., 55(5); 420-426. Lin, Y. J., Lin, C., Yeh, K. J. and Lee, A. (2000). Photodegradation of the herbicides butachlor and ronstar using natural sunlight and diethylamine. Bull. Environ. Contam. Toxicol., 64(6); 780-785.
Liu, H. M., Cao, L., Lu, P., Ni, H., Li, Y. X., Yan, X., Hong, Q. and Li, S. P. (2012). Biodegradation of butachlor by Rhodococcus sp. strain B1 and purification of its hydrolase (ChlH) responsible for N-dealkylation of chloroacetamide herbicides. J. Agric. Food Chem., 60(50); 12238-12244. Ma, J. P., Wang, Z., Lu, P., Wang, H. J., Waseem Ali, S., Li, S. P. and Huang, X. (2009). Biodegradation of the sulfonylurea herbicide chlorimuron-ethyl by the strain Pseudomonas sp. LW3. FEMS Microbiol. Lett., 296(2); 203-209. Min, H., Ye, Y. F., Chen, Z. Y., Wu, W. X. and Yufeng, D. (2001). Effects of butachlor on microbial populations and enzyme activities in paddy soil. J. Environ. Sci. Heal. B., 36(5); 581-595. Mohanty, S. S. and Jena, H. M. (2019). Degradation kinetics and mechanistic study on herbicide bioremediation using hyper butachlor-tolerant Pseudomonas putida G3. Process. Saf. Environ., 125; 172-181. O’Mahony, M. M., Dobson, A. D., Barnes, J. D. and Singleton, I. (2006). The use of ozone in the remediation of polycyclic aromatic hydrocarbon contaminated soil. Chemosphere, 63(2); 307-314. Pal, R., Das, P., Chakrabarti, K., Chakraborty, A. and Chowdhury, A. (2006). Butachlor degradation in tropical soils: Effect of application rate, biotic-abiotic interactions and soil conditions. J. Environ. Sci. Heal. B., 41(7); 1103-1113. Pourbabaee, A., Soleymani, A., Torabi, E. and Alizadeh, H. (2018). Degradation and detoxification of nicosulfuron by a Pseudomonas strain isolated from a contaminated cornfield soil. Soil Sediment Contam., 27(8); 756-772. Radivojević, L., Gašić, S., Šantrić, L., Gajić-Umiljendić, J. and Marisavljević, D. (2012). Short-time effects of the herbicide nicosulfuron on the biochemical activity of Chernozem soil. J. Serb. Chem. Soc., 77(6); 845-855. Ramu, S. and Seetharaman, B. (2014). Biodegradation of acephate and methamidophos by a soil bacterium Pseudomonas aeruginosa strain Is-6. J. Environ. Sci. Heal. B., 49(1); 23-34. Rousseaux, S., Hartmann, A., Lagacherie, B., Piutti, S., Andreux, F. and Soulas, G. (2003). Inoculation of an atrazine-degrading strain, Chelatobacter heintzii Cit1, in four different soils: effects of different inoculum densities. Chemosphere, 51(7); 569-576. Šantrić, L., Radivojević, L., Gajić-Umiljendić, J., Sarić-Krsmanović, M. and Đurović-Pejčev, R. (2016). Effects of herbicides on growth and number of actinomycetes in soil and in vitro. Pesticidi i fitomedicina, 31(3-4); 121-128. Singh, B. K., Walker, A. and Wright, D. J. (2006). Bioremedial potential of fenamiphos and chlorpyrifos degrading isolates: influence of different environmental conditions. Soil Biol. Biochem., 38(9); 2682-2693.
Singh, V. and Singh, K. (2016). Effect of herbicide Butachlor on the earthworm Eutyphoeus waltoni Michaelsen. Int. J. Pure App. Biosci., 4(1); 216-225. Sutherland, T. D., Horne, I., Lacey, M. J., Harcourt, R. L., Russell, R. J. and Oakeshott, J. G. (2000). Enrichment of an endosulfan-degrading mixed bacterial culture. Appl. Environ. Microbiol., 66(7); 2822-2828. Thabit, T. M. and El-Naggar, M. A. (2013). Malathion degradation by soil isolated bacteria and
Pollution, 6(3): 627-635, Summer 2020
Pollution is licensed under a "Creative Commons Attribution 4.0 International (CC-BY 4.0)"
635
detection of degradation products by GC-MS. Int. J. Environ. Sci., 3(5); 1467-1476. Torabi, E., Talebi, K., Pourbabaei, A. and Ahmadzadeh, M. (2017). Diazinon dissipation in pesticide-contaminated paddy soil: kinetic modeling and isolation of a degrading mixed bacterial culture. Environ. Sci. Pollut. Res., 24(4); 4117-4133.
Vajargah, M. F. and Hedayati, A. (2017). Acute toxicity of butachlor to Rutilus rutilus caspicus and Sander lucioperca in vivo condition. Transylv. Rev. Syst. Ecol. Res., 19(3); 85-92.
Vandana, L. J., Rao, P. C. and Padmaja, G. (2012). Effect of herbicides and nutrient management on soil enzyme activity. J. Rice Res., 5(1); 50–58. Wang, F., Yao, J., Chen, H., Chen, K., Trebše, P. and Zaray, G. (2010). Comparative toxicity of chlorpyrifos and its oxon derivatives to soil microbial activity by combined methods. Chemosphere, 78(3); 319-326. Wang, Y., Cang, T., Yu, R., Wu, S., Liu, X., Chen, C., Wang, Q. and Cai, L. (2016). Joint acute toxicity of the herbicide butachlor and three insecticides to the terrestrial earthworm, Eisenia fetida. Environ. Sci. and Pollut. Res., 23(12); 11766-11776. Watanabe, H., Nguyen, M. H. T., Souphasay, K., Vu, S. H., Phong, T. K., Tournebize, J. and Ishihara, S. (2007). Effect of water management practice on pesticide behavior in paddy water. Agric. Water Manag., 88(1-3); 132-140. Williams, L. J. and Abdi, H. (2010). Fisher’s least significant difference (LSD) test. Encyclopedia of Research Design. 218; 840-853.
Wu, P., Xie, L., Li, J., Yang, W., Han, Z., Wu, X., Mo, W., Wen, C., Gao, Y., Wan, T. and Zhang, Y. (2020). The removal of butachlor from soil by wastewater‐derived Rhodopseudomonas marshes. Soil Use and Manage., 00; 1-4.
Xue, J., Jiang, W., Liu, F., Zhao, H., Wang, S. and Peng, W. (2014). Development and validation of an alternative to conventional pretreatment methods for residue analysis of butachlor in water, soil, and rice. J. AOAC Int., 97(1); 245-251. Zabaloy, M. C., Garland, J. L. and Gomez, M. A. (2008). An integrated approach to evaluate the impacts of the herbicides glyphosate, 2, 4-D and metsulfuron-methyl on soil microbial communities in the Pampas region, Argentina. Appl. Soil Ecol., 40(1); 1-12. Zhang, J., Zheng, J. W., Liang, B., Wang, C. H., Cai, S., Ni, Y. Y., He, J. and Li, S. P. (2011). Biodegradation of chloroacetamide herbicides by Paracoccus sp. FLY-8 in vitro. J. Agric. Food Chem., 59(9); 4614-4621.
Zheng, J., Li, R., Zhu, J., Zhang, J., He, J., Li, S. and Jiang, J. (2012). Degradation of the chloroacetamide herbicide butachlor by Catellibacterium caeni sp. nov DCA-1T. Int. Biodeterior. Biodegradation, 73; 16-22.