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Biodegradation Pathway of the Pyrethroid Pesticide Esfenvalerate by Bacteria from Different Biomes

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Abstract

This manuscript reports on a study of new biocatalysts for the biodegradation of pyrethroid pesticides, such as esfenvalerate. Experiments of esfenvalerate biodegradation by bacteria isolated from Brazilian savannah (Curtobacterium sp. CBMAI 1834, Bacillus sp. 2B, Lysinibacillus sp. CBMAI 1837, and Bacillus sp. 4T), sea (Kocuria sp. CBMAI 135, Kocuria sp. CBMAI 136, Kocuria marina CBMAI 141, and Kocuria sp. CBMAI 145), and a tropical peat usually known as “turfa” soil (Bacillus sp. P5CBNB, Kosakonia sp. CBMAI 1836, Bacillus sp. CBMAI 1833, and Kosakonia sp. CBMAI 1835) were performed. A biodegradation pathway was proposed for a better understanding of the environmental fate of the above mentioned insecticide. Esfenvalerate (S,S-fenvalerate) and its metabolites [3-phenoxybenzaldehyde (PBAld), 3-phenoxybenzoic acid (PBAc), 3-phenoxybenzyl alcohol, and 2-(4-chlorophenyl)-3-methylbutyric acid) (CLAc)] were quantitatively analyzed in triplicate experiments by a validated method. Initially, 100 mg L−1 esfenvalerate (Sumidan 150SC) was added for each experiment. The residual esfenvalerate (104.7–41.6 mg L−1) and formation of PBAc (0.1–8.1 mg L−1), ClAc (1.5–11.0 mg L−1), PBAlc (0.9 mg L−1), and PBAld (completely biotransformed) were quantified. The 12 bacterial strains accelerated (with different efficiencies) the esfenvalerate degradation and increased the metabolites concentrations. A new and more complete biodegradation pathway based on HPLC-time of flight (ToF) and gas chromatography-mass spectrometry (GC-MS) analyses (in which thermal instability products were detected) was proposed. The detected metabolites are smaller and more polar compounds that may be carried by water and contaminate the environment.

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References

  • Alvarenga, N., Birolli, W. G., Seleghim, M. H. R., & Porto, A. L. M. (2014). Biodegradation of methyl parathion by whole cells of marine-derived fungi Aspergillus sydowii and Penicillium decaturense. Chemosphere, 117, 47–52.

    Article  CAS  Google Scholar 

  • Arrebola, F. J., Martinez-Vidal, J. L., Fernandez-Gutierrez, A., & Akhtar, M. H. (1999). Monitoring of pyrethroid metabolites in human urine using solid-phase extraction followed by gas chromatography-tandem mass spectrometry. Analytica Chimica Acta, 401(1-2), 45–54.

    Article  CAS  Google Scholar 

  • Birolli, W. G., Alvarenga, N., Seleghim, M. H. R., & Porto, A. L. M. (2016). Biodegradation of the pyrethroid pesticide esfenvalerate by marine-derived fungi. Marine Biotechnology. doi:10.1007/s10126-016-9710-z.

    Google Scholar 

  • Bradberry, S. M., Cage, S. A., Proudfoot, A. T., & Vale, J. A. (2005). Poisoning due to pyrethroids. Toxicological Reviews, 24(2), 93–106.

    Article  CAS  Google Scholar 

  • Chen, S., Chang, C., Deng, Y., An, S., Dong, Y. H., Zhou, J., Hu, M., Zhong, G., & Zhang, L.-H. (2014). Fenpropathrin biodegradation pathway in Bacillus sp DG-02 and its potential for bioremediation of pyrethroid-contaminated soils. Journal of Agricultural and Food Chemistry, 62(10), 2147–2157.

    Article  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.

    Article  CAS  Google Scholar 

  • Chen, S., Hu, Q., Hu, M., Luo, J., Weng, Q., & Lai, K. (2011a). Isolation and characterization of a fungus able to degrade pyrethroids and 3-phenoxybenzaldehyde. Bioresource Technology, 102(17), 8110–8116.

    Article  CAS  Google Scholar 

  • Chen, S., Yang, L., Hu, M., & Liu, J. (2011b). Biodegradation of fenvalerate and 3-phenoxybenzoic acid by a novel Stenotrophomonas sp. strain ZS-S-01 and its use in bioremediation of contaminated soils. Applied Microbiology and Biotechnology, 90(2), 755–767.

    Article  CAS  Google Scholar 

  • Dash, H. R., Mangwani, N., Chakraborty, J., Kumari, S., & Das, S. (2013). Marine bacteria: potential candidates for enhanced bioremediation. Applied Microbiology and Biotechnology, 97(2), 561–571.

    Article  CAS  Google Scholar 

  • de Oliveira, J. R., Seleghim, M. H. R., & Porto, A. L. (2014). Biotransformation of methylphenylacetonitriles by Brazilian marine fungal strain Aspergillus sydowii CBMAI 934: eco-friendly reactions. Marine Biotechnology, 16(2), 156–160.

    Article  Google Scholar 

  • Derelanko, M. J., & Hollinger, M. A. (2002). Handbook of toxicology (p. 1440). New Jersey: Taylor & Francis.

    Google Scholar 

  • Egeghy, P. P., Hubal, E. A. C., Tulve, N. S., Melnyk, L. J., Morgan, M. K., Fortmann, R. C., & Sheldon, L. S. (2011). Review of pesticide urinary biomarker measurements from selected US EPA children’s observational exposure studies. International Journal of Environmental Research and Public Health, 8(5), 1727–1754.

    Article  CAS  Google Scholar 

  • Enayati, A. A., Asgarian, F., Amouei, A., Sharif, M., Mortazavi, H., Boujhmehrani, H., & Hemingway, J. (2010). Pyrethroid insecticide resistance in Rhipicephalus bursa (Acari, Ixodidae). Pesticide Biochemistry and Physiology, 97(3), 243–248.

    Article  CAS  Google Scholar 

  • Farghaly, M. F. M., Zayed, S., & Soliman, S. M. (2013). Deltamethrin degradation and effects on soil microbial activity. Journal of Environmental Science and Health Part B-Pesticides Food Contaminants and Agricultural Wastes, 48(7), 575–581.

    Article  CAS  Google Scholar 

  • Fenner, K., Canonica, S., Wackett, L. P., & Elsner, M. (2013). Evaluating pesticide degradation in the environment: blind spots and emerging opportunities. Science, 341(6147), 752–758.

    Article  CAS  Google Scholar 

  • Franchi, J. G., Sígolo, J. B., & Lima, J. R. B. (2003). Peat as a soil conditioner used in environmental recovery of mined areas—analytical assessment methodology. Brazilian Journal of Geology, 33(3), 255–262.

    Google Scholar 

  • Guo, P., Wang, B., Hang, B., Li, L., Ali, S. W., He, J., & Li, S. (2009). Pyrethroid-degrading Sphingobium sp JZ-2 and the purification and characterization of a novel pyrethroid hydrolase. International Biodeterioration & Biodegradation, 63(8), 1107–1112.

    Article  CAS  Google Scholar 

  • Housset, P., & Dickman, R. (2009). A promise fulfilled—pyrethroid development and the benefits for agriculture and human health. Bayer CropScience Journal, 62, 135–144.

    Google Scholar 

  • Hu, G. P., Zhao, Y., Song, F. Q., Liu, B., Vasseur, L., Douglas, C., & You, M. S. (2014). Isolation, identification and cyfluthrin-degrading potential of a novel Lysinibacillus sphaericus strain, FLQ-11-1. Research in Microbiology, 165(2), 110–118.

    Article  CAS  Google Scholar 

  • Hussain, S., Siddique, T., Arshad, M., & Saleem, M. (2009). Bioremediation and phytoremediation of pesticides: recent advances. Critical Reviews in Environmental Science and Technology, 39(10), 843–907.

    Article  CAS  Google Scholar 

  • Ki Chang, A., Gee, S. J., Kim, H.-J., Aronov, P. A., Vega, H., Krieger, R. I., & Hammock, B. D. (2011). Immunochemical analysis of 3-phenoxybenzoic acid, a biomarker of forestry worker exposure to pyrethroid insecticides. Analytical and Bioanalytical Chemistry, 401(4), 1285–1293.

    Article  Google Scholar 

  • Lucas, S. C. O. (2014) Avaliação da potencialidade da microbiota da turfa na biorremediação de agroquímicos neonicotinoides em água. In: Rede Nordeste de Biotecnologia – RENORBIO. Universidade Federal de Sergipe, São Cristoval, SE, Brazil, p 112

  • Lumjuan, N., Wicheer, J., Leelapat, P., Choochote, W., & Somboon, P. (2014). Identification and characterisation of Aedes aegypti aldehyde dehydrogenases involved in pyrethroid metabolism. Plos One, 9(7), e102746.

    Article  Google Scholar 

  • Mayer, A. M. S., Rodriguez, A. D., Taglialatela-Scafati, O., & Fusetani, N. (2013). Marine Pharmacology in 2009-2011: Marine compounds with antibacterial, antidiabetic, antifungal, anti-inflammatory, antiprotozoal, antituberculosis, and antiviral activities; affecting the immune and nervous systems, and other miscellaneous mechanisms of action. Marine Drugs, 11(7), 2510–2573.

    Article  Google Scholar 

  • Meira, E. B., dos Anjos, C. S., Birolli, W. G., Peret, M. C. M., Fonseca, L. P., Nitschke, M., Sakamoto, I. K., Varesche, M. B. A., & Porto, A. L. M. P. (2016). Isolation of bacteria from a reforested Brazilian savannah for biodegradation of esfenvarelate. In J. Alvarez (Ed.), Biodegradation: Properties, Analysis and Performance. Hauppauge: Nova Science Publishers.

    Google Scholar 

  • Menezes, C. B. A., Bonugli-Santos, R. C., Miqueletto, P. B., Passarini, M. R. Z., Silva, C. H. D., Justo, M. R., Leal, R. R., Fantinatti-Garboggini, F., Oliveira, V. M., Berlinck, R. G. S., & Sette, L. D. (2010). Microbial diversity associated with algae, ascidians and sponges from the north coast of Sao Paulo state, Brazil. Microbiological Research, 165(6), 466–482.

    Article  Google Scholar 

  • Pace, H. C., & Brenner, C. (2001). The nitrilase superfamily: classification, structure and function. Genome Biology, 2(1). reviews0001.1–reviews0001.9.

  • Soderlund, D. M., Clark, J. M., Sheets, L. P., Mullin, L. S., Piccirillo, V. J., Sargent, D., Stevens, J. T., & Weiner, M. L. (2002). Mechanisms of pyrethroid neurotoxicity: implications for cumulative risk assessment. Toxicology, 171(1), 3–59.

    Article  CAS  Google Scholar 

  • Sogorb, M. A., & Vilanova, E. (2002). Enzymes involved in the detoxification of organophosphorus, carbamate and pyrethroid insecticides through hydrolysis. Toxicology Letters, 128(1-3), 215–228.

    Article  CAS  Google Scholar 

  • Souza, R. C., Mendes, I. C., Reis, F. B., Carvalho, F. M., Nogueira, M. A., Vasconcelos, A. T. R., Vicente, V. A., & Hungria, M. (2016). Shifts in taxonomic and functional microbial diversity with agriculture: how fragile is the Brazilian Cerrado? Bmc Microbiology, 16, 42.

    Article  Google Scholar 

  • Tortora, G. J. (2010). Microbiology: an introduction. New York: Pearson Education.

    Google Scholar 

  • Tyler, C. R., Beresford, N., van der Woning, M., Sumpter, J. P., & Thorpe, K. (2000). Metabolism and environmental degradation of pyrethroid insecticides produce compounds with endocrine activities. Environmental Toxicology and Chemistry, 19(4), 801–809.

    Article  CAS  Google Scholar 

  • Vacondio, B., Birolli, W. G., Ferreira, I. M., Seleghim, M. H. R., Sarah, G., Vasconcellos, S. P., & Porto, A. L. M. (2015). Biodegradation of pentachlorophenol by marine-derived fungus Trichoderma harzianum CBMAI 1677 isolated from ascidian Didemnun ligulum. Biocatalysis and Agricultural Biotechnology, 4(2), 266–275.

    Article  Google Scholar 

  • Veum, L., Pereira, S. R. M., van der Waal, J. C., & Hanefeld, U. (2006). Catalytic hydrogenation of cyanohydrin esters as a novel approach to N-acylated beta-aminio alcohols—reaction optimisation by a design of experiment approach. European Journal of Organic Chemistry, 7, 1664–1671.

    Article  Google Scholar 

  • Wang, B. -z., Ma, Y., Zhou, W. -y., Zheng, J. -w., Zhu, J. -c., He, J., & Li, S.-p. (2011). Biodegradation of synthetic pyrethroids by Ochrobactrum tritici strain pyd-1. World Journal of Microbiology & Biotechnology, 27(10), 2315–2324.

    Article  CAS  Google Scholar 

  • Yu, F. B., Shan, S. D., Luo, L. P., Guan, L. B., & Qin, H. (2013). Isolation and characterization of a Sphingomonas sp strain F-7 degrading fenvalerate and its use in bioremediation of contaminated soil. Journal of Environmental Science and Health Part B-Pesticides Food Contaminants and Agricultural Wastes, 48(3), 198–207.

    Article  CAS  Google Scholar 

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Acknowledgments

The authors are grateful to the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, grant no. 558062/2009-1) and Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP, grant no. 2012/19934-0) for the financial support. W. G. Birolli and E. M. Borges acknowledge CNPq and Sistema de Gestão Ambiental (SGA-USP) for their scholarships, respectively. The authors are also indebted to Angela C. Giampedro, who reviewed the English language of this paper, IHARABRAS S.A. for supplying the technical grade esfenvalerate and the commercial insecticide Sumidan 150SC, and the Chromatography Group (Instituto de Química de São Carlos—USP), including Guilherme M. Titato for the LC-MS analysis (Fapesp grant no. 2004/09498-2).

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Authors and Affiliations

  1. Laboratório de Química Orgânica e Biocatálise, Instituto de Química de São Carlos, Universidade de São Paulo, Av. João Dagnone, 1100, Ed. Química Ambiental, Jd. Santa Angelina, 13563-120, São Carlos, SP, Brazil

    Willian G. Birolli, Eloá M. Borges & André L. M. Porto

  2. Laboratório de Biotecnologia Microbiana, Instituto de Química de São Carlos, Universidade de São Paulo, Avenida João Dagnone, 1100, Ed. Química Ambiental, Jd. Santa Angelina, 13563-120, São Carlos, SP, Brazil

    Marcia Nitschke

  3. Laboratório de Química Analítica Ambiental, Centro de Ciências Exatas e Tecnologia, Departamento de Química, Universidade Federal de Sergipe, Avenida Marechal Rondon. Jardim Rosa Elze, 49100-000, Sao Cristovao, SE, Brazil

    Luciane P. C. Romão

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  1. Willian G. Birolli
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  2. Eloá M. Borges
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  5. André L. M. Porto
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Correspondence to André L. M. Porto.

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Birolli, W.G., Borges, E.M., Nitschke, M. et al. Biodegradation Pathway of the Pyrethroid Pesticide Esfenvalerate by Bacteria from Different Biomes. Water Air Soil Pollut 227, 271 (2016). https://doi.org/10.1007/s11270-016-2968-y

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