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Marine Biotechnology

, Volume 18, Issue 4, pp 511–520 | Cite as

Biodegradation of the Pyrethroid Pesticide Esfenvalerate by Marine-Derived Fungi

  • Willian G. Birolli
  • Natália Alvarenga
  • Mirna H. R. Seleghim
  • André L. M. Porto
Original Article

Abstract

Esfenvalerate biodegradation by marine-derived fungi is reported here. Esfenvalerate (S,S-fenvalerate) and its main metabolites [3-phenoxybenzaldehyde (PBAld), 3-phenoxybenzoic acid (PBAc), 3-phenoxybenzyl alcohol (PBAlc), and 2-(4-chlorophenyl)-3-methylbutyric acid (CLAc)] were quantitatively analyzed by a validated method in triplicate experiments. All the strains (Penicillium raistrickii CBMAI 931, Aspergillus sydowii CBMAI 935, Cladosporium sp. CBMAI 1237, Microsphaeropsis sp. CBMAI 1675, Acremonium sp. CBMAI 1676, Westerdykella sp. CBMAI 1679, and Cladosporium sp. CBMAI 1678) were able to degrade esfenvalerate, however, with different efficiencies. Initially, 100 mg L−1 esfenvalerate (Sumidan 150SC) was added to each culture in 3 % malt liquid medium. Residual esfenvalerate (64.8–95.2 mg L−1) and the concentrations of PBAc (0.5–7.4 mg L−1), ClAc (0.1–7.5 mg L−1), and PBAlc (0.2 mg L−1) were determined after 14 days. In experiments after 7, 14, 21, and 28 days of biodegradation with the three most efficient strains, increasing concentrations of the toxic compounds PBAc (2.7–16.6 mg L−1, after 28 days) and CLAc (6.6–13.4 mg L−1, after 28 days) were observed. A biodegradation pathway was proposed, based on HPLC-ToF results. The biodegradation pathway includes PBAld, PBAc, PBAlc, ClAc, 2-hydroxy-2-(3-phenoxyphenyl)acetonitrile, 3-(hydroxyphenoxy)benzoic acid, and methyl 3-phenoxy benzoate. Marine-derived fungi were able to biodegrade esfenvalerate in a commercial formulation and showed their potential for future bioremediation studies in contaminated soils and water bodies.

Keywords

Marine fungi Fenvalerate Biotransformation Insecticide Organic pollutant 

Notes

Acknowledgments

W. G. Birolli and N. Alvarenga thank CNPq and FAPESP for their scholarships, respectively. A. L. M. Porto is 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 financial support. The authors express their gratitude to Roberto G. S. Berlinck (IQSC-USP, São Carlos, SP, Brazil) for providing the marine microorganisms, Timothy Roberts, 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).

Compliance with Ethical Standards

Ethical Statement

I would like to declare on behalf of my co-authors that the work described was an original research that has not been published previously and neither is under consideration for publication elsewhere (partly or in full). No data, text, or theories by others are presented as if they were the author’s own. This article does not contain any studies with human participants or animals performed by any of the authors.

Conflict of Interest

There are no conflict of interest in the submission of this manuscript, and all the authors approved the manuscript publication.

Supplementary material

10126_2016_9710_MOESM1_ESM.docx (736 kb)
ESM 1 (DOCX 736 kb)

References

  1. Adelsbach TL, Tjeerdema RS (2003) Chemistry and fate of fenvalerate and esfenvalerate. Rev Environ Contam Toxicol 176:137–154PubMedGoogle Scholar
  2. Ahn KC, Gee SJ, Kim H-J, Aronov PA, Vega H, Krieger RI, Hammock BD (2011) Immunochemical analysis of 3-phenoxybenzoic acid, a biomarker of forestry worker exposure to pyrethroid insecticides. Anal Bioanal Chem 401:1285–1293PubMedCrossRefGoogle Scholar
  3. Alvarenga N, Birolli WG, Seleghim MHR, Porto ALM (2014) Biodegradation of methyl parathion by whole cells of marine-derived fungi Aspergillus sydowii and Penicillium decaturense. Chemosphere 117:47–52PubMedCrossRefGoogle Scholar
  4. Arrebola FJ, Martinez-Vidal JL, Fernandez-Gutierrez A, Akhtar MH (1999) Monitoring of pyrethroid metabolites in human urine using solid-phase extraction followed by gas chromatography-tandem mass spectrometry. Anal Chim Acta 401:45–54CrossRefGoogle Scholar
  5. Barr DB, Olsson AO, Wong LY, Udunka S, Baker SE, Whitehead RD, Magsumbol MS, Williams BL, Needham LL (2010) Urinary concentrations of metabolites of pyrethroid insecticides in the general US population: national health and nutrition examination survey 1999-2002. Environ Health Perspect 118:742–748PubMedPubMedCentralCrossRefGoogle Scholar
  6. Birolli WG, Alvarenga N, Vacondio B, Seleghim MHR, Porto ALM (2014) Growth assessment of marine-derived fungi in the presence of esfenvalerate and its main metabolites. J Microb Biochem Technol 6:260–267CrossRefGoogle Scholar
  7. Bouldin JL, Milam CD, Farris JL, Moore MT, Smith S, Cooper CM (2004) Evaluating toxicity of Asana XL (R) (esfenvalerate) amendments in agricultural ditch mesocosms. Chemosphere 56:677–683PubMedCrossRefGoogle Scholar
  8. 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. Bioresour Technol 102:8110–8116PubMedCrossRefGoogle Scholar
  9. 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. Appl Microbiol Biotechnol 90:755–767PubMedCrossRefGoogle Scholar
  10. 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:e50456PubMedPubMedCentralCrossRefGoogle Scholar
  11. Colombo R, Yariwake JH, Lanza MRV (2014) Analysis of degradation products of esfenvalerate by SBSE/HPLC-UV/DAD using fractional factorial design. Quim Nova 37:535–539Google Scholar
  12. da Silva NA, Birolli WG, Seleghim MHR, Porto ALM (2013) Biodegradation of the organophosphate pesticide profenofos by marine fungi. In: Patil Y (ed) Applied bioremediation—active and passive approaches. InTech, Morn Hill, pp 149–180Google Scholar
  13. Dash HR, Mangwani N, Chakraborty J, Kumari S, Das S (2013) Marine bacteria: potential candidates for enhanced bioremediation. Appl Microbiol Biotechnol 97:561–571PubMedCrossRefGoogle Scholar
  14. Derelanko MJ, Hollinger MA (2002) Handbook of toxicology. Taylor & Francis, New JerseyGoogle Scholar
  15. Egeghy PP, Cohen Hubal EA, Tulve NS, Melnyk LJ, Morgan MK, Fortmann RC, Sheldon LS (2011) Review of pesticide urinary biomarker measurements from selected US EPA children’s observational exposure studies. Int J Environ Res Public Health 8:1727–1754PubMedPubMedCentralCrossRefGoogle Scholar
  16. EPA (2013) Pesticide ecotoxicity database. http://cfpub.epa.gov/ecotox/. Accessed 29 April 2015
  17. European Commission (2000) Review report for the active substance esfenvalerate. http://ec.europa.eu/food/fs/sfp/ph_ps/pro/eva/existing/list1-15_en.pdf. Accessed 1 Sept 2015
  18. Farghaly MFM, Zayed SMAD, Soliman SM (2013) Deltamethrin degradation and effects on soil microbial activity. J Environ Sci Health B 48:575–581PubMedCrossRefGoogle Scholar
  19. Havens PL (1995) Fate of herbicides in the environment. In: Smith A (ed) Handbook of weed management systems. Wiley, York, pp 245–278Google Scholar
  20. Heinis LJ, Knuth ML (1992) The mixing, distribution and persistence of esfenvalerate within littoral enclosures. Environ Toxicol Chem 11:11–25CrossRefGoogle Scholar
  21. Housset P, Dickman R (2009) A promise fulfilled—pyrethroid development and the benefits for agriculture and human health. Bayer CropScience J 62:135–144Google Scholar
  22. Katagi T (2012) Environmental behavior of synthetic pyrethroids. Top Curr Chem 314:167–202PubMedCrossRefGoogle Scholar
  23. Ki Chang A, Gee SJ, Kim H-J, Aronov PA, Vega H, Krieger RI, Hammock BD (2011) Immunochemical analysis of 3-phenoxybenzoic acid, a biomarker of forestry worker exposure to pyrethroid insecticides. Anal Bioanal Chem 401:1285–1293CrossRefGoogle Scholar
  24. Kjer J, Debbab A, Aly AH, Proksch P (2010) Methods for isolation of marine-derived endophytic fungi and their bioactive secondary products. Nat Protoc 5:479–490PubMedCrossRefGoogle Scholar
  25. Kossuga MH, Romminger S, Xavier C, Milanetto MC, do Valle MZ, Pimenta EF, Morais RP, de Carvalho E, Mizuno CM, Coradello LFC, Barroso VM, Vacondio B, Javaroti DCD, Seleghim MHR, Cavalcanti BC, Pessoa C, Moraes MO, Lima BA, Goncalves R, Bonugli-Santos RC, Sette LD, Berlinck RGS (2012) Evaluating methods for the isolation of marine-derived fungal strains and production of bioactive secondary metabolites. Rev Bras Farmacogn 22:257–267CrossRefGoogle Scholar
  26. Lee PW, Stearns SM, Powell WR (1988) Metabolic-fate of fenvalerate in wheat plants. J Agric Food Chem 36:189–193CrossRefGoogle Scholar
  27. Liang WQ, Wang ZY, Li H, Wu PC, Hu JM, Luo N, Cao LX, Liu YH (2005) Purification and characterization of a novel pyrethroid hydrolase from Aspergillus niger ZD11. J Agric Food Chem 53:7415–7420PubMedCrossRefGoogle Scholar
  28. Liu S-L, Yao K, Jia D-Y, Lai W, Zhao N, Yuan H-Y (2011) Study on pre-treatment method for HPLC analysis of cypermethrin in Aspergillus oryzae degradation system. J Sichuan Univ 43:179–183Google Scholar
  29. Lozano SJ, Brazner JC, Knuth ML, Heinis LJ, Sargent KW, Tanner DK, Anderson LE, O’Halloran SL, Bert SL (1989) Effects, persistence and distribution of esfenvalerate in littoral enclosures. Environmental Protection Agency. Rep.No.DU E104/PPA 06/7592AGoogle Scholar
  30. Materna EJ, Rabeni CF, Lapoint TW (1995) Effects of the synthetic pyrethroid insecticide, esfenvalerate, on larval leopard frogs (Rana spp). Environ Toxicol Chem 14:613–622Google Scholar
  31. Meyer BN, Lam C, Moore S, Jones RL (2013) Laboratory degradation rates of 11 pyrethroids under aerobic and anaerobic conditions. J Agric Food Chem 61:4702–4708PubMedCrossRefGoogle Scholar
  32. Mukherjee I, Mittal A (2007) Dissipation of β-cyfluthrin by two fungi Aspergillus nidulans var. dentatus and Sepedonium maheswarium. Toxicol Environ Chem 89:319–326CrossRefGoogle Scholar
  33. Ng CM (2012) The transport of chemicals and biota into coastal rivers and marine ecosystems. Dissertation. University of CaliforniaGoogle Scholar
  34. Nowell LH, Capel PD, Dileanis PD (1999) Pesticides in stream sediment and aquatic biota: distribution, trends, and governing factors. CRC Press LLC, Boca RatonCrossRefGoogle Scholar
  35. Ohkawa H, Nambu K, Inui H, Miyamoto J (1978) Metabolic-fate of fenvalerate (SUMICIDIN) in soil and by soil-microorganisms. J Pestic Sci 3:129–141CrossRefGoogle Scholar
  36. Ortega SN, Nitschke M, Mouad AM, Landgraf MD, Rezende MOO, Seleghim MHR, Sette LD, Porto ALM (2011) Isolation of Brazilian marine fungi capable of growing on DDD pesticide. Biodegradation 22:43–50PubMedCrossRefGoogle Scholar
  37. Pan DY, Liang XM (1993) Safety study of pesticides on bog frog, a predatory natural enemy of pest in paddy field. J Hunan Agric Coll 19:47–54Google Scholar
  38. Passarini MRZ, Rodrigues MVN, da Silva M, Sette LD (2011) Marine-derived filamentous fungi and their potential application for polycyclic aromatic hydrocarbon bioremediation. Mar Pollut Bull 62:364–370PubMedCrossRefGoogle Scholar
  39. Radosetich SR, Holt J, Ghersa C (1997) Weed ecology. Wiley, New YorkGoogle Scholar
  40. Saikia N, Gopal M (2004) Biodegradation of beta-cyfluthrin by fungi. J Agric Food Chem 52:1220–1223PubMedCrossRefGoogle Scholar
  41. Schnoor JL (1992) Fate of pesticides and chemicals in the environment. In: Wolfe NL (ed) Fate of pesticides and chemicals in the environment. Wiley, New York, pp 93–104Google Scholar
  42. Sogorb MA, Vilanova E (2002) Enzymes involved in the detoxification of organophosphorus, carbamate and pyrethroid insecticides through hydrolysis. Toxicol Lett 128:215–228PubMedCrossRefGoogle Scholar
  43. Tortora GJ (2010) Microbiology: an introduction, 10th edn. Pearson Education, Upper Saddle RiverGoogle Scholar
  44. Tyler CR, Beresford N, Van der Woning M, Sumpter JP, Thorpe K (2000) Metabolism and environmental degradation of pyrethroid insecticides produce compounds with endocrine activities. Environ Toxicol Chem 19:801–809CrossRefGoogle Scholar
  45. Ueyama J, Kimata A, Kamijima M, Hamajima N, Ito Y, Suzuki K, Inoue T, Yamamoto K, Takagi K, Saito I, Miyamoto K-I, Hasegawa T, Kondo T (2009) Urinary excretion of 3-phenoxybenzoic acid in middle-aged and elderly general population of Japan. Environ Res 109:175–180PubMedCrossRefGoogle Scholar
  46. Vadhana D, Carloni M, Fedeli D, Nasuti C, Gabbianelli R (2011) Perturbation of rat heart plasma membrane fluidity due to metabolites of permethrin insecticide. Cardiovasc Toxicol 11:226–234PubMedCrossRefGoogle Scholar
  47. Verma AK, Raghukumar C, Naik CG (2011) A novel hybrid technology for remediation of molasses-based raw effluents. Bioresour Technol 102:2411–2418PubMedCrossRefGoogle Scholar
  48. Verma AK, Raghukumar C, Parvatkar RR, Naik CG (2012) A rapid two-step bioremediation of the anthraquinone dye, reactive blue 4 by a marine-derived fungus. Water Air Soil Pollut 223:3499–3509CrossRefGoogle Scholar
  49. Viant MR, Pincetich CA, Tjeerderna RS (2006) Metabolic effects of dinoseb, diazinon and esfenvalerate in eyed eggs and alevins of Chinook salmon (Oncorhynchus tshawytscha) determined by H-1 NMR metabolomics. Aquat Toxicol 77:359–371PubMedCrossRefGoogle Scholar
  50. Wang BZ, Ma Y, Zhou W, Zheng J, Zhu J, He J, Li S (2011) Biodegradation of synthetic pyrethroids by Ochrobactrum tritici strain pyd-1. World J Microbiol Biotechnol 27:2315–2324CrossRefGoogle Scholar
  51. Yu FB, Shan SD, Luo LP, Guan LB, Qin H (2013) Isolation and characterization of a Sphingomonas sp. strain F-7 degrading fenvalerate and its use in bioremediation of contaminated soil. J Environ Sci Health B 48:198–207PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Willian G. Birolli
    • 1
  • Natália Alvarenga
    • 1
  • Mirna H. R. Seleghim
    • 2
  • André L. M. Porto
    • 1
  1. 1.Laboratório de Química Orgânica e Biocatálise, Instituto de Química de São CarlosUniversidade de São PauloSão CarlosBrazil
  2. 2.Departamento de Ecologia e Biologia EvolutivaUniversidade Federal de São CarlosSão CarlosBrazil

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