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Microbial detoxification of bifenthrin insecticide by selected fungal strains and optimizing conditions using response surface methodology for agricultural sustainability

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Abstract

Bifenthrin is a type I broad spectrum pyrethroid insecticide widely employed in urban and agricultural settings with little knowledge about its biodegradation. Bifenthrin was subjected to a 35 days incubation period in which it was degraded by five fungal strains named as Aspergillus niger, Aspergillus flavus, Aspergillus fumigatus, Penicillium chrysogenum, and Lasiodiplodia theobromae. Penicillium chrysogenum was found to be extremely effective in degrading bifenthrin up to 85%. Furthermore, response surface methodology (RSM) with Box-Behnken design is applied to optimize the degradation conditions with varying pH, temperature (°C), and incubation time (days). The p value < 0.05 in the response surface design and analysis of variance showed the significance of the reaction parameters. The ideal conditions for Penicillium chrysogenum to break down bifenthrin (10 mgL−1) were found to be 30 °C, pH 7, and a 24 days incubation period. In eutrophic conditions and a glucose-rich media, this fungus co-metabolized bifenthrin. By hydrolytically cleaving the carboxyl ester bond, the Penicillium chrysogenum breaks down bifenthrin, as shown by the chromatogram of four metabolites from GCMS. The biodegradation of bifenthrin by strain Penicillium chrysogenum and its use in agronomic situations are now well understood as per the findings of this study.

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References

  • Ahmad, K. S. (2020). Environmental contaminant 2-chloro-N-(2,6- diethylphenyl) -N-(methoxymethyl) acetamide remediation via Xanthomonas axonopodis and Aspergillus niger. Environmental Research, 182, 109117.

    CAS  Google Scholar 

  • Amin, M., Yousuf, M., Attaullah, M., Ahmad, N., Azra, M. N., Lateef, M., ... & Naeem, M. (2021). Cholinesterase activity as a potential biomarker for neurotoxicity induced by pesticides in vivo exposed Oreochromis niloticus (Nile tilapia): assessment tool for organophosphates and synthetic pyrethroids. Environmental Technology, 44(14), 2148–2156.

  • Anwar, S., Liaquat, F., Khan, Q. M., Khalid, Z. M., & Iqbal, S. (2009). Biodegradation of chlorpyrifos and its hydrolysis product 3, 5, 6-trichloro-2-pyridinol by Bacillus pumilus strain C2A1. Journal of Hazardous Materials, 168(1), 400–405.

    CAS  Google Scholar 

  • Ariyani, M., Pitoi, M. M., Koesmawati, T. A., Maulana, H., Endah, E. S., & Yusiasih, R. (2020). Pyrethroid residues on tropical soil of an Indonesian tea plantation: Analytical method development, monitoring, and risk assessment. Sustainable Environment Research, 30, 1–10.

    Google Scholar 

  • Bhatt, P., Pathak, V. M., Joshi, S., Bisht, T. S., Singh, K., & Chandra, D. (2019a). Major metabolites after degradation of xenobiotics and enzymes involved in these pathways. In Smart bioremediation technologies (pp. 205–215). Academic Press.

  • Bhatt, P., Gangola, S., Chaudhary, P., Khati, P., Kumar, G., Sharma, A., & Srivastava, A. (2019b). Pesticide induced up-regulation of esterase and aldehyde dehydrogenase in indigenous Bacillus spp. Bioremediation Journal, 23, 42–52.

    CAS  Google Scholar 

  • Bhatt, P., Huang, Y., Zhang, W., Sharma, A., & Chen, S. (2020a). Enhanced cypermethrin degradation kinetics and metabolic pathway in Bacillus thuringiensis strain SG4. Microorganisms, 8, 223.

    CAS  Google Scholar 

  • Bhatt, P., Zhang, W., Lin, Z., Pang, S., Huang, Y., & Chen, S. (2020b). Biodegradation of allethrin by a novel fungus Fusarium proliferatum strain CF2, isolated from contaminated soils. Microorganisms, 8, 593.

  • Birolli, W. G., Arai, M. S., Nitschke, M., & Porto, A. L. (2019). The pyrethroid (±)-lambda-cyhalothrin enantioselective biodegradation by a bacterial consortium. Pesticide Biochemistry and Physiology, 156, 129–137.

    CAS  Google Scholar 

  • Chen, S., Dong, Y. H., Chang, C., Deng, Y., Zhang, X. F., Zhong, G., Song, H., Hu, M., & Zhang, L. H. (2013). Characterization of a novel cyfluthrin-degrading bacterial strain Brevibacterium aureum and its biochemical degradation pathway. Bioresource Technology, 132, 16–23.

    CAS  Google Scholar 

  • Chen, S., Geng, P., Xiao, Y., & Hu, M. (2012). Bioremediation of β-cypermethrin and 3-phenoxybenzaldehyde contaminated soils using Streptomyces aureus HP-S-01. Applied Microbiology and Biotechnology, 94, 505–515.

    CAS  Google Scholar 

  • Chen, S., Hu, Q., Hu, M., Luo, J., Weng, Q., & Lai, K. (2011). Isolation and characterization of a fungus able to degrade pyrethroids and 3-phenoxybenzaldehyde. Bioresource Technology, 102, 8110–8116.

    CAS  Google Scholar 

  • Chen, S., Hu, W., Xiao, Y., Deng, Y., Jia, J., & Hu, M. (2012). Degradation of 3-phenoxybenzoic acid by a Bacillus sp. PLoS One, 7, e50456.

    CAS  Google Scholar 

  • Chen, S., Luo, J., Hu, M., Geng, P., & Zhang, Y. (2012). Microbial detoxification of bifenthrin by a novel yeast and its potential for contaminated soils treatment. PloS one, 7, e30862.

    CAS  Google Scholar 

  • Cycoń, M., & Piotrowska-Seget, Z. (2016). Pyrethroid-degrading microorganisms and their potential for the bioremediation of contaminated soils: A review. Frontiers in Microbiology, 7, 1463.

    Google Scholar 

  • Cycoń, M., Wójcik, M., & 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, 494–501.

    Google Scholar 

  • Cycoń, M., Zmijowska, A., & Piotrowska-Seget, Z. (2014). Enhancement of deltamethrin degradation by soil bioaugmentation with two different strains of Serratia marcescens. International journal of Environmental Science and Technology, 11, 1305–1316.

    Google Scholar 

  • Deer, H. M., & Beard, R. (2001). Effect of water pH on the chemical stability of pesticides. AG/Pesticides, 14, 1.

    Google Scholar 

  • Deng, W., Lin, D., Yao, K., Yuan, H., Wang, Z., Li, J., & Liu, S. (2015). Characterization of a novel β-cypermethrin-degrading Aspergillus niger YAT strain and the biochemical degradation pathway of β-cypermethrin. Applied Microbiology and biotechnology, 99, 8187–8198.

    CAS  Google Scholar 

  • Dritsa, V., Rigas, F., Doulia, D., Avramides, E. J., & Hatzianestis, I. (2009). Optimization of culture conditions for the biodegradation of lindane by the polypore fungus Ganoderma australe. Water, air and Soil Pollution, 204, 19–27.

    CAS  Google Scholar 

  • Fareed, R., Ansari, A., Seecharan, D., & Munroe, L. (2017). Investigating the degrading properties of three different strains of fungi on commonly used pesticides in Guyana. Asian Journal of Natural Product Biochemistry, 15, 5–14.

    Google Scholar 

  • Gajendiran, A., & Abraham, J. (2018). An overview of pyrethroid insecticides. Frontiers in Biology, 13, 79–90.

    CAS  Google Scholar 

  • Gangola, S., Joshi, S., Kumar, S., & Pandey, S. (2019). Comparative analysis of fungal and bacterial enzymes in biodegradation of xenobiotic compounds. In Smart Bioremediation Technologies (pp. 169–189). Academic Press. https://doi.org/10.1016/B978-0-12-818307-6.00010-X

    Chapter  Google Scholar 

  • Hamad, M. T. M. H. (2020). Biodegradation of diazinon by fungal strain Aspergillus niger MK640786 using response surface methodology. Environmental Technology Innovations, 18, 100691.

    Google Scholar 

  • Holmes, R. W., Anderson, B. S., Phillips, B. M., Hunt, J. W., Crane, D. B., et al. (2008). Statewide investigation of the role of pyrethroid pesticides in sediment toxicity in California's urban waterways. Environmental Science and Technology, 42, 7003–7009.

    CAS  Google Scholar 

  • Hu, W., Lu, Q., Zhong, G., Hu, M., & Yi, X. (2019). Biodegradation of pyrethroids by a hydrolyzing carboxylesterase EstA from Bacillus cereus BCC01. Applied Sciences, 9, 477.

    CAS  Google Scholar 

  • Kuivila, K. M., Hladik, M. L., Ingersoll, C. G., Kemble, N. E., Moran, P. W., Calhoun, D. L., & Gilliom, R. J. (2012). Occurrence and potential sources of pyrethroid insecticides in stream sediments from seven US metropolitan areas. Environmental Science and Technology, 46, 4297–4303.

    CAS  Google Scholar 

  • Laskowski, D.A. (2002). Physical and chemical properties of pyrethroids. In: Ware, G.W. (eds) Reviews of environmental contamination and toxicology. Reviews of Environmental Contamination and Toxicology, (vol. 174, pp. 49–170). Springer.

  • Liu, K., Wang, L., Jiang, B., An, J., Nian, B., Wang, D., et al. (2021). Effect of inoculation with Penicillium chrysogenum on chemical components and fungal communities in fermentation of Pu-erh tea. Food Research International, 150, 110748.

    CAS  Google Scholar 

  • Meena, P., Shah, P. G., Patel, K. C., Chobhe, K. A., Viraji, C. R., Chopra, I. (2021). Dissipation behaviour of bifenthrin in water at different pH levels under laboratory conditions. Journal of Environmental Analytical Chemistry, 1–9. https://doi.org/10.1080/03067319.2021.1996568

  • Mohafrash, S. M., Hassan, E. E., El-Shaer, N. H., & Mossa, A. T. H. (2021). Detoxification gene expression, genotoxicity, and hepatorenal damage induced by subacute exposure to the new pyrethroid, imiprothrin, in rats. Environmental Science and Pollution Research, 18, 33505–33521.

    Google Scholar 

  • Mohapatra, S., & Ahuja, A. K. (2009). Effect of moisture and soil type on the degradation of bifenthrin in soil. Pesticide Research Journal, 19, 110–112.

    Google Scholar 

  • Mukherjee, I., Das, S. K., Kumar, A., & Shukla, L. (2020). Sludge amendment affect the persistence, carbon mineralization and enzyme activity of atrazine and bifenthrin. Bulletin of Environmental Contamination and Toxicology, 105, 291–298.

    CAS  Google Scholar 

  • Oliveira, M., Pereira, C., Bessa, C., Araujo, R., & Saraiva, L. (2015). Chronological aging in conidia of pathogenic Aspergillus: Comparison between species. Journal of microbial methods, 118, 57–63.

    Google Scholar 

  • Pankaj, Sharma, A., Gangola, S., Khati, P., Kumar, G., & Srivastava, A. (2016). Novel pathway of cypermethrin biodegradation in a Bacillus sp. strain SG2 isolated from cypermethrin-contaminated agriculture field. Biotechnology, 6, 45.

    CAS  Google Scholar 

  • Prodhan, M. D. H., Afroze, M., Begum, A., & Sarker, D. (2021). Determination of organophosphorus and synthetic pyrethroid pesticide residues and their variability in large size fruit crops. Journal of the Science of Food and Agriculture, 101, 4847–4854.

    CAS  Google Scholar 

  • Ramasubramanian, T., & Paramasivam, M. (2021). Bifenthrin in the tropical sugarcane ecosystem: Persistence and environmental risk assessment. Environmental Science and Pollution Research, 28, 3524–3532.

    CAS  Google Scholar 

  • Riaz, G., Tabinda, A. B., Kashif, M., Yasar, A., Mahmood, A., Rasheed, R., et al. (2018). Monitoring and spatiotemporal variations of pyrethroid insecticides in surface water, sediment, and fish of the river Chenab Pakistan. Environmental Science and Pollution Research, 25, 22584–22597.

    CAS  Google Scholar 

  • Saikia, N., & Gopal, M. (2004). Biodegradation of β-cyfluthrin by fungi. Journal of Agricultural and food Chemistry, 52, 1220–1223.

    CAS  Google Scholar 

  • Shah, P. C., Kumar, V. R., Dastager, S. G., & Khire, J. M. (2017). Phytase production by Aspergillus niger NCIM 563 for a novel application to degrade organophosphorus pesticides. AMB Express, 7, 1–11.

    Google Scholar 

  • Singh, B. K., Walker, A., & Wright, D. J. (2006). Bioremedial potential of fenamiphos and chlorpyrifos degrading isolates: Influence of different environmental conditions. Soil Biology and Biochemistry, 38, 2682–2693.

    CAS  Google Scholar 

  • Song, E., Wang, M., & Shen, D. (2014). Isolation, identification and characterization of a novel Ralstonia sp. FD-1, capable of degrading 4-fluoroaniline. Biodegradation, 25, 85–94.

    CAS  Google Scholar 

  • VanDusen, A. E., Richards, S. L., & Balanay, J. A. G. (2016). Evaluation of bifenthrin barrier spray on foliage in a suburban eastern North Carolina neighborhood. Pest Management Science, 72, 1004–1012.

    CAS  Google Scholar 

  • Wang, C., Chen, F., Zhang, Q., & Fang, Z. (2009). Chronic toxicity and cytotoxicity of synthetic pyrethroid insecticide cis-bifenthrin. Journal of Environmental Science, 21, 1710–1715.

    CAS  Google Scholar 

  • Wang, D., Xue, Q., Zhou, X., Tang, X., & Hua, R. (2015). Isolation and characterization of a highly efficient chlorpyrifos degrading strain of Cupriavidus taiwanensis from sludge. Journal of Basic Microbiology, 55, 229–235.

    CAS  Google Scholar 

  • Wang, Q., Shen, J. Y., Zhang, R., Hong, J. W., Li, Z., Ding, Z., & Xu, L. C. (2020). Effects and mechanisms of pyrethroids on male reproductive system. Toxicology, 438, 152460.

    CAS  Google Scholar 

  • Weston, D. P., Asbell, A. M., Hecht, S. A., Scholz, N. L., & Lydy, M. J. (2011). Pyrethroid insecticides in urban salmon streams of the Pacific Northwest. Environmental pollution, 159, 3051–3056.

    CAS  Google Scholar 

  • Weston, D. P., Holmes, R. W., & Lydy, M. J. (2009). Residential runoff as a source of pyrethroid pesticides to urban creeks. Environmental Pollution, 157, 287–294.

    CAS  Google Scholar 

  • World Health Organization. (2020). The WHO recommended classification of pesticides by hazard and guidelines to classification 2019. World Health Organization.

  • Zhan, H., Huang, Y., Lin, Z., Bhatt, P., & Chen, S. (2020). New insights into the microbial degradation and catalytic mechanism of synthetic pyrethroids. Environmental Research, 182, 109138.

    CAS  Google Scholar 

  • Zhang, C., Jia, L., Wang, S., Qu, J., Li, K., Xu, L., & Yan, Y. (2010). Biodegradation of beta-cypermethrin by two Serratia spp. with different cell surface hydrophobicity. Bioresource Technology, 101, 3423–3429.

    CAS  Google Scholar 

  • Zhang, Q., Li, S., Ma, C., Wu, N., Li, C., & Yang, X. (2018). Simultaneous biodegradation of bifenthrin and chlorpyrifos by Pseudomonas sp. CB2. Environmental Science Health B, Part B, 53, 304–312.

    CAS  Google Scholar 

  • Zhao, J., Jia, D., Du, J., Chi, Y., & Yao, K. (2019). Substrate regulation on co-metabolic degradation of β-cypermethrin by Bacillus licheniformis B-1. AMB Express, 9, 1–11.

    Google Scholar 

  • Zheng, Z., Chen, Y., Zhang, S., Wang, L., & Qian, X. (2016). Determination of isopyrazam residues and its degradation products in cucumber by gas chromatography. Journal of Food Safety and Quality, 7, 540–544.

    Google Scholar 

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Acknowledgements

The concept, idea, data, and writing are the intellectual property right of Dr. Khuram Shahzad Ahmad and Lab E-21 of Department of Environmental Sciences, Fatima Jinnah Women University, The Mall, 46000, Rawalpindi, Pakistan. The authors acknowledge the researchers supporting project number (RSP2023R293) King Saud University, Riyadh, Saudi Arabia.

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Authors and Affiliations

  1. Materials and Environmental Chemistry Lab, Lab-E21, Department of Environmental Sciences, Fatima Jinnah Women University, Rawalpindi, Pakistan

    Sara Majid & Khuram Shahzad Ahmad

  2. Department of Food Sciences & Nutrition, College of Food & Agriculture Sciences, King Saud University, Riyadh, 11451, Saudi Arabia

    Wahidah H. Al-Qahtani

  3. Department of Materials, Photon Science Institute and Sir Henry Royce Institute, Alan Turing Building, The University of Manchester, Oxford Road, Manchester, M13 9PL, United Kingdom

    Muhammad Azad Malik

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  1. Sara Majid
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All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Sara Majid and Khuram Shahzad Ahmad. The first draft of the manuscript was written by Sara Majid. All authors read and approved the final manuscript. Individual contribution of each author is mentioned as follows: Sara Majid: conceptualization, methodology and study design, and writing—original draft. Khuram Shahzad Ahmad: supervision, project administration, validation, and writing—reviewing and editing. Wahidah H. Al-Qahtani: resources, data validation, and software. Muhammad Azad Malik: editing and reviewing of manuscript

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Correspondence to Khuram Shahzad Ahmad.

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Majid, S., Ahmad, K.S., Al-Qahtani, W.H. et al. Microbial detoxification of bifenthrin insecticide by selected fungal strains and optimizing conditions using response surface methodology for agricultural sustainability. Environ Monit Assess 195, 1214 (2023). https://doi.org/10.1007/s10661-023-11801-w

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