Isolation and characterization of chlorpyrifos-degrading bacteria in tea-growing soils

Lam Thanh Nguyen; Tam Bang Kieu Nguyen; Thanh Huu Luong; Huyen Thi Dam; Phuong Minh Nguyen

doi:10.18006/2023.11(3).563.571

Authors

Lam Thanh Nguyen Ministry of Natural Resources and Environment, 10 Ton That Thuyet, Nam Tu Liem district, Hanoi, Vietnam https://orcid.org/0009-0006-0389-8049
Tam Bang Kieu Nguyen Faculty of Environmental Sciences, University of Science, Vietnam National University, Hanoi, 334 Nguyen Trai, Thanh Xuan, Hanoi, Vietnam https://orcid.org/0000-0003-4953-0646
Thanh Huu Luong Department of Environmental Biology, Institute for Agricultural Environment, Hanoi, Vietnam https://orcid.org/0000-0002-3414-9570
Huyen Thi Dam Faculty of Environmental Sciences, University of Science, Vietnam National University, Hanoi, 334 Nguyen Trai, Thanh Xuan, Hanoi, Vietnam https://orcid.org/0009-0000-5584-0371
Phuong Minh Nguyen Faculty of Environmental Sciences, University of Science, Vietnam National University, Hanoi, 334 Nguyen Trai, Thanh Xuan, Hanoi, Vietnam https://orcid.org/0000-0002-7045-9787

DOI:

https://doi.org/10.18006/2023.11(3).563.571

Keywords:

CPF, Degradation, E. adhaerens VNN3, M. populi CNN2, Remediation

Abstract

The excess use of pesticides in the agricultural sector has caused environmental pollution and affected the complete ecosystem. Among the various commonly used pesticides, chlorpyrifos (CPF) is widely used against multiple agrarian pests due to its effectiveness and higher insecticidal activities. However, along with its beneficial usage, CPF has various residual effects on the environment, causing multiple negative impacts on aquatic organisms and human health. Consequently, methods for eliminating CPF in the background are essential. Among the currently available approaches to CPF remediation, biological methods using microorganisms are eco-friendly and cost-effective. Therefore, this study was conducted to isolate and characterize chlorpyrifos-degrading bacteria from the tea-growing soil of Vietnam. For this, soil samples were collected from the 20 tea-growing areas of Vietnam. From the collected samples, three bacterial strains viz., Methylobacterium populi CNN2, Ensifer adhaerens VNN3, and Acinetobacter pittii CNN4 have been isolated by using streak plate method and identified based on 16S rRNA gene analysis. The study results showed that under laboratory conditions, E. adhaerens VNN3 had the highest CPF degradation ability and was followed by the strain M. populi CNN2. In liquid medium, CPF concentration (100 mg/L) was reduced by 95.2% and 81.4% by E.adhaerens VNN3 and M. populi CNN2, respectively, after 72 h. Further, under in-vitro conditions, the concentration of CPF was reduced from 500 mg/kg to 112 ± 1.73 (77.6%) and 197 ± 2.08 mg/kg (60.6%) by E. adhaerens VNN3 and M. populi CNN2, respectively. Based on the obtained results, it can be concluded that E. adhaerens VNN3 and M. populi CNN2 can be used for CPF-contaminated agricultural soil remediation.

Author Biography

Lam Thanh Nguyen, Ministry of Natural Resources and Environment, 10 Ton That Thuyet, Nam Tu Liem district, Hanoi, Vietnam

Faculty of Environmental Sciences, University of Science, Vietnam National University, Hanoi, 334 Nguyen Trai, Thanh Xuan, Hanoi, Vietnam

References

Akbar, S., & Sultan, S. (2016). Soil bacteria showing a potential of chlorpyrifos degradation and plant growth enhancement. Brazilian Journal of Microbiology,47, 563-570. https://doi.org/10.1016/ j.bjm.2016.04.009 DOI: https://doi.org/10.1016/j.bjm.2016.04.009

Asamba, M. N., Mugendi, E. N., Oshule, P. S., Essuman, S., Chimbevo, L. M., & Atego, N. A. (2022). Molecular characterization of chlorpyrifos degrading bacteria isolated from contaminated dairy farm soils in Nakuru County, Kenya. Heliyon, 8, e09176. https://doi.org./10.1016/j.heliyon.2022.e09176 DOI: https://doi.org/10.1016/j.heliyon.2022.e09176

Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., & Struhl, K. (1994). Current Protocols in Molecular Biology. New York: Wiley.

Bhandari, G., Atreya, K., Scheepers, P. T. J., & Geissen, V. (2020). Concentration and distribution of pesticide residues in soil: Non-dietary human health risk assessment. Chemosphere,253, 126594. https://doi.org/10.1016/j.chemosphere.2020.126594 DOI: https://doi.org/10.1016/j.chemosphere.2020.126594

Blanco, J., Guardia-Escote, L., Mulero, M., Basaure, P., Biosca-Brull, J., Cabré, M., Colomina, M. T., Domingo, J. L., & Sánchez, D. J. (2020). Obesogenic effects of chlorpyrifos and its metabolites during the differentiation of 3T3-L1 preadipocytes. Food and Chemical Toxicology, 137, 111171. https://doi.org/10.1016/ j.fct.2020.111171 DOI: https://doi.org/10.1016/j.fct.2020.111171

Bose, S., Kumar, P. S., & Vo, D.V. N. (2021). A review on the microbial degradation of chlorpyrifos and its metabolite TCP. Chemosphere, 283, 131447. https://doi.org/10.1016/ j.chemosphere.2021.131447 DOI: https://doi.org/10.1016/j.chemosphere.2021.131447

Cheng, C., Liu, W., Hou, K., Zhang, J., Du, Z., Li, B., & Zhu, L. (2023). Ecological safety evaluation of chlorpyrifos on agricultural soil: Effects on soil microbes. Applied Soil Ecology, 189, 104954.https://doi.org/10.1016/j.apsoil.2023.104954 DOI: https://doi.org/10.1016/j.apsoil.2023.104954

Elshikh, M. S., Alarjani, K. M., Huessien, D. S., Elnahas, H. A. M., & Esther, A. R. (2022). Enhanced Biodegradation of Chlorpyrifos by Bacillus cereus CP6 and Klebsiella pneumoniae CP19 from municipal waste water. Environmental Research, 205, 112438. https://doi.org/10.1016/j.envres.2021.112438 DOI: https://doi.org/10.1016/j.envres.2021.112438

EPA. (1996). SW-846 Test Method 3540C: Soxhlet Extraction. Part of Test methods for Evaluating Solid Waste. Retrieved from https://www.epa.gov/sites/default/files/2015-12/documents/3540c.pdf.

Hadibarata, T., Kristanti, R. A., Bilal, M., Yilmaz, M. , & Sathishkumar, P. (2023). Biodegradation mechanism of chlorpyrifos by halophilic bacterium Hortaea sp. B15. Chemosphere, 312, 137260. https://doi.org/10.1016/ j.chemosphere.2022.137260 DOI: https://doi.org/10.1016/j.chemosphere.2022.137260

Hazarika, J., Ganguly, M., & Mahanta, R. (2020). A computational insight into the molecular interactions of chlorpyrifos and its degradation products with the human progesterone receptor leading to endocrine disruption. Journal of Applied Toxicology, 40, 434-443.https://doi.org/10.1002/jat.3916 DOI: https://doi.org/10.1002/jat.3916

Hossain, M. S., Chowdhury, M. A. Z., Pramanik, M. K., Rahman, M. A., Fakhruddin, A. N. M., & Alam, M. K. (2015). Determination of selected pesticides in water samples adjacent to agricultural fields and removal of organophosphorus insecticide chlorpyrifos using soil bacterial isolates. Applied Water Science,5, 171-179.https://doi.org/10.1007/s13201-014-0178-6 DOI: https://doi.org/10.1007/s13201-014-0178-6

Huang, X., Cui, H., & Duan, W. (2020). Ecotoxicity of chlorpyrifos to aquatic organisms: A review. Ecotoxicology and Environmental Safety, 200, 110731. https://doi.org/10.1016/ j.ecoenv.2020.110731 DOI: https://doi.org/10.1016/j.ecoenv.2020.110731

Huang, Y., Zhang, W., Pang, S., Chen, J., Bhatt, P., Mishra, S., & Chen, S. (2021). Insights into the microbial degradation and catalytic mechanisms of chlorpyrifos. Environmental Research, 194, 110660. https://doi.org/10.1016/j.envres.2020.110660 DOI: https://doi.org/10.1016/j.envres.2020.110660

Ishag, S. A., Abdelbagi, A. O., Hammad, A. M. A., Elsheikh, E. A. E., Elsaid, O. E., Hur, J. H., & Laing, M. D. (2016). Biodegradation of Chlorpyrifos, Malathion, and Dimethoate by Three Strains of Bacteria Isolated from Pesticide-Polluted Soils in Sudan. Journal of Agricultural and Food Chemistry, 64, 8491-8498. https://doi.org/10.1021/acs.jafc.6b03334 DOI: https://doi.org/10.1021/acs.jafc.6b03334

Jha, S. K., Chishti, Z., Ahmad, Z., & Arshad, K. R. (2022). Enterobacter sp. SWLC2 for biodegradation of chlorpyrifos in the aqueous medium: Modeling of the process using artificial neural network approaches. Computers and Electronics in Agriculture, 193, 106680. https://doi.org/10.1016/j.compag.2021.106680 DOI: https://doi.org/10.1016/j.compag.2021.106680

Jin, Y., Liu, Z., Peng, T., & Fu, Z. (2015). The toxicity of chlorpyrifos on the early life stage of zebrafish: A survey on the endpoints at development, locomotor behavior, oxidative stress and immunotoxicity. Fish & Shellfish Immunology, 43, 405-414. https://doi.org/10.1016/j.cbpc.2018.12.004 DOI: https://doi.org/10.1016/j.fsi.2015.01.010

Khalid, S., Han, J. I., Hashmi, I., Hasnain, G., Ahmed, M. A., Khan, S. J., & Arshad, M. (2018). Strengthening calcium alginate microspheres using polysulfone and its performance evaluation: Preparation, characterization and application for enhanced biodegradation of chlorpyrifos. Science of the Total Environment, 631-632, 1046-1058. https://doi.org/10.1016/j.scitotenv.2018.03.101 DOI: https://doi.org/10.1016/j.scitotenv.2018.03.101

Li, X., Wang, J., Jia, Y., Reheman, A., & Yan, Y. (2020). The Genome Analysis of Methylobacterium populi YC-XJ1 with Diverse Xenobiotics Biodegrading Capacity and Degradation Characteristics of Related Hydrolase. International Journal of Molecular Sciences, 21. https://doi.org/10.3390/ijms21124436 DOI: https://doi.org/10.3390/ijms21124436

McDonald, N. D., Love, C. E., & Gibbons, H. S. (2021). The ChpR transcriptional regulator of Sinorhizobium meliloti senses 3,5,6-trichloropyridinol, a degradation product of the organophosphate pesticide chlorpyrifos. Access Microbiology, 3, 000297-000297. https://doi.org/10.1099/acmi.0.000297 DOI: https://doi.org/10.1099/acmi.0.000297

Moyano, P., García, J., García, J. M., Pelayo, A., Muñoz-Calero, P., Frejo, M. T., Anadon, M. J., Lobo, M., & Del Pino, J. (2020). Chlorpyrifos-induced cell proliferation in human breast cancer cell lines differentially mediated by estrogen and aryl hydrocarbon receptors and KIAA1363 enzyme after 24 h and 14 days exposure. Chemosphere, 251, 126426. https://doi.org/10.1016/ j.chemosphere.2020.126426 DOI: https://doi.org/10.1016/j.chemosphere.2020.126426

Oltramare, C., Weiss, F. T., Staudacher, P., Kibirango, O., Atuhaire, A., & Stamm, C. (2022). Pesticides monitoring in surface water of a subsistence agricultural catchment in Uganda using passive samplers. Environmental Science and Pollution Research, 30, 10312–10328. https://doi.org/10.1007/s11356-022-22717-2 DOI: https://doi.org/10.1007/s11356-022-22717-2

Pailan, S., Sengupta, K., Ganguly, U., & Saha, P. (2016). Evidence of biodegradation of chlorpyrifos by a newly isolated heavy metal-tolerant bacterium Acinetobacter sp. strain MemCl4. Environmental Earth Sciences,75, 1019. https://doi.org/10.1007/s12665-016-5834-8 DOI: https://doi.org/10.1007/s12665-016-5834-8

Sishu, F. K., Tilahun, S. A., Schmitter, P., Assefa, G., & Steenhuis, T. S. (2022). Pesticide Contamination of Surface and Groundwater in an Ethiopian Highlands' Watershed. Water,14, 3446.https://doi.org/10.3390/w14213446 DOI: https://doi.org/10.3390/w14213446

Soltani-Nezhad, F., Saljooqi, A., Mostafavi, A., & Shamspur, T. (2020). Synthesis of Fe(3)O(4)/CdS-ZnS nanostructure and its application for photocatalytic degradation of chlorpyrifos pesticide and brilliant green dye from aqueous solutions. Ecotoxicology and Environmental Safety,189, 109886.https://doi.org/10.1016/ j.ecoenv.2019.109886 DOI: https://doi.org/10.1016/j.ecoenv.2019.109886

Sud, D., Kumar, J. V., Kaur, P., & Bansal, P. (2020). Toxicity, natural and induced degradation of chlorpyrifos. Journal of The Chilean Chemical Society, 65, 4807-4816. http://dx.doi.org/10.4067/S0717-97072020000204807 DOI: https://doi.org/10.4067/S0717-97072020000204807

Takayasu, T., Yamamoto, H., Ishida, Y., Nosaka, M., Kawaguchi, M., Kuninaka, Y., Kimura, A., & Kondo, T. (2017). Postmortem distribution of chlorpyrifos-methyl, fenitrothion, and their metabolites in body fluids and organ tissues of an intoxication case. Legal medicine(Tokyo),29, 44-50.https://doi.org/10.1016/ j.legalmed.2017.10.002 DOI: https://doi.org/10.1016/j.legalmed.2017.10.002

Tan, H., Li, Q., Zhang, H., Wu, C., Zhao, S., Deng, X., & Li, Y. (2020). Pesticide residues in agricultural topsoil from the Hainan tropical riverside basin: Determination, distribution, and relationships with planting patterns and surface water. Science of the Total Environment, 722, 137856.https://doi.org/10.1016/ j.scitotenv.2020.137856 DOI: https://doi.org/10.1016/j.scitotenv.2020.137856

Zhao, L., Wang, F., & Zhao, J. (2014). Identification and functional characteristics of chlorpyrifos-degrading and plant growth promoting bacterium Acinetobacter calcoaceticus. Journal of Basic Microbiology, 54, 457-63. https://doi.org/10.1002/ jobm.201200639 DOI: https://doi.org/10.1002/jobm.201200639