Metabolism of an insecticide fipronil by soil fungus Cunninghamella elegans ATCC36112.
Bioremediation
Cunninghamella elegans
Fipronil
Fungal metabolism
Inhibitor
Journal
Archives of microbiology
ISSN: 1432-072X
Titre abrégé: Arch Microbiol
Pays: Germany
ID NLM: 0410427
Informations de publication
Date de publication:
14 Jun 2023
14 Jun 2023
Historique:
received:
22
03
2023
accepted:
21
05
2023
revised:
25
04
2023
medline:
16
6
2023
pubmed:
15
6
2023
entrez:
14
6
2023
Statut:
epublish
Résumé
In this study, the metabolic pathway of the phenylpyrazole insecticide fipronil in Cunninghamella elegans (C. elegans) was investigated. Approximately 92% of fipronil was removed within 5 days, and seven metabolites were accumulated simultaneously. The structures of the metabolites were completely or tentatively identified by GC-MS and
Identifiants
pubmed: 37316622
doi: 10.1007/s00203-023-03594-w
pii: 10.1007/s00203-023-03594-w
doi:
Substances chimiques
fipronil
QGH063955F
Insecticides
0
Pyrazoles
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
264Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Abdel-Daim MM, Dessouki AA, Abdel-Rahman HG, Eltaysh R, Alkahtani S (2019) Hepatorenal protective effects of taurine and N-acetylcysteine against fipronil induced injuries: the antioxidant status and apoptotic markers expression in rats. Sci Total Environ 650:2063–2073. https://doi.org/10.1016/j.scitotenv.2018.09.313
doi: 10.1016/j.scitotenv.2018.09.313
pubmed: 30290348
Abraham J, Gajendiran A (2019) Biodegradation of fipronil and its metabolite fipronil sulfone by Streptomyces rochei strain AJAG7 and its use in bioremediation of contaminated soil. Pestic Biochem Physiol 155:90–100. https://doi.org/10.1016/j.pestbp.2019.01.011
doi: 10.1016/j.pestbp.2019.01.011
pubmed: 30857632
Al-Badran AA, Fujiwara M, Mora MA, Gatlin DM (2021) The adverse effects of the phenylpyrazole, fipronil, on juvenile white shrimp Litopenaeus setiferus. Environ Sci Pollut Res 28(41):58688–58700. https://doi.org/10.1007/s11356-021-14651-6
doi: 10.1007/s11356-021-14651-6
Ardeshir RA, Zolgharnein H, Movahedinia A, Salamat N, Zabihi E (2018) CYP1A gene expression as a basic factor for fipronil toxicity in Caspian kutum fish. Toxicol Rep 5:113–124. https://doi.org/10.1016/j.toxrep.2017.12.014
doi: 10.1016/j.toxrep.2017.12.014
pubmed: 29854583
Asha S, Vidyavathi M (2009) Cunninghamella—a microbial model for drug metabolism studies: a review. Biotechnol Adv 27:16–29. https://doi.org/10.1016/j.biotechadv.2008.07.005
doi: 10.1016/j.biotechadv.2008.07.005
pubmed: 18775773
Beeler AB, Schlenk DK, Rimoldi JM (2001) Synthesis of fipronil sulfide, an active metabolite, from the parent insecticide fipronil. Tetrahedron Lett 42(32):5371–5372. https://doi.org/10.1016/S0040-4039(01)01043-7
doi: 10.1016/S0040-4039(01)01043-7
Bhatti S, Satyanarayana GNV, Patel DK, Satish A (2019) Bioaccumulation, biotransformation and toxic effect of fipronil in Escherichia coli. Chemosphere 231:207–215. https://doi.org/10.1016/j.chemosphere.2019.05.124
doi: 10.1016/j.chemosphere.2019.05.124
pubmed: 31129401
Chang YN, Tsai TH (2020) Preclinical transplacental transfer and pharmacokinetics of fipronil in rats. Drug Metab Dispos 48(10):886–893. https://doi.org/10.1124/dmd.120.000088
doi: 10.1124/dmd.120.000088
pubmed: 32723848
Chen D, Li J, Zhao Y, Wu Y (2021) Human exposure of fipronil insecticide and the associated health risk. J Agric Food Chem 70(1):63–71. https://doi.org/10.1021/acs.jafc.1c05694
doi: 10.1021/acs.jafc.1c05694
pubmed: 34971309
Chen TT, Hu JJ, Chen YY, Liu Y, Li Y, Xu H (2022) Tracking the environmental fate of fipronil and three of its metabolites in garlic based on sampling rate-corrected in vivo solid phase microextraction combined with gas chromatography-mass spectrometry. Anal Chim Acta 1190:339263. https://doi.org/10.1016/j.aca.2021.339263
doi: 10.1016/j.aca.2021.339263
pubmed: 34857131
Cravedi JP, Delous G, Zalko D, Viguie C, Debrauwer L (2013) Disposition of fipronil in rats. Chemosphere 93(10):2276–2283. https://doi.org/10.1016/j.chemosphere.2013.07.083
doi: 10.1016/j.chemosphere.2013.07.083
pubmed: 24016625
Dube AK, Kumar MS (2017) Biotransformation of bromhexine by Cunninghamella elegans, C. echinulata and C. blakesleeana. Braz J Microbiol 48(2):259–267. https://doi.org/10.1016/j.bjm.2016.11.003
doi: 10.1016/j.bjm.2016.11.003
pubmed: 27988088
El-Murr A, Ali HA, Elgaml SA, Hashish EA (2016) The β-1,3-glucan alleviated the hepatotoxicity induced by combination of fipronil and lead in common carp (Cyprinus carpio). Comp Clin Pathol 25:689–697. https://doi.org/10.1007/s00580-016-2249-6
doi: 10.1007/s00580-016-2249-6
Fu Z, Wang Y, Chen J, Wang Z, Wang X (2016) How pbdes are transformed into dihydroxylated and dioxin metabolites catalyzed by the active center of cytochrome p450s: a dft study. Environ Sci Technol 50(15):8155–8163. https://doi.org/10.1021/acs.est.6b00524
doi: 10.1021/acs.est.6b00524
pubmed: 27363260
Gajendiran A, Abraham J (2017) Biomineralisation of fipronil and its major metabolite, fipronil sulfone, by Aspergillus glaucus strain AJAG1 with enzymes studies and bioformulation. 3 Biotech 7:212. https://doi.org/10.1007/s13205-017-0820-8
doi: 10.1007/s13205-017-0820-8
pubmed: 28667652
pmcid: 5493570
Gan J, Bondarenko S, Oki L, Haver D, Li JX (2012) Occurrence of fipronil and its biologically active derivatives in urban residential runoff. Environ Sci Technol 46(3):1489–1495. https://doi.org/10.1021/es202904x
doi: 10.1021/es202904x
pubmed: 22242791
Gibbons D, Morrissey C, Mineau P (2015) A review of the direct and indirect effects of neonicotinoids and fipronil on vertebrate wildlife. Environ Sci Pollut Res 22(1):103–118. https://doi.org/10.1007/s11356-014-3180-5
doi: 10.1007/s11356-014-3180-5
Guo Q, Zhao S, Zhang J, Qi K, Du Z, Shao B (2018) Determination of fipronil and its metabolites in chicken egg, muscle and cake by a modified QuEChERS method coupled with LC-MS/MS. Food Addit Contam 35:1543–1552. https://doi.org/10.1080/19440049.2018.1472395
doi: 10.1080/19440049.2018.1472395
Kanetis L, Forster H, Jones CA, Borkovich KA, Adaskaveg JE (2008) Characterization of genetic and biochemical mechanisms of fludioxonil and pyrimethanil resistance in field isolates of Penicillium digitatum. Phytopathology 98:205–214. https://doi.org/10.1094/PHYTO-98-2-0205
doi: 10.1094/PHYTO-98-2-0205
pubmed: 18943197
Katsumata H, Okada T, Kaneco S, Suzuki T, Ohta K (2010) Degradation of fenitrothion by ultrasound/ferrioxalate/UV system. Ultrason Sonochem 17:200–206. https://doi.org/10.1016/j.ultsonch.2009.06.011
doi: 10.1016/j.ultsonch.2009.06.011
pubmed: 19592289
Khan S, Jan MH, Kumar D, Telang AG (2015) Firpronil induced spermotoxicity is associated with oxidative stress, DNA damage and apoptosis in male rats. Pestic Biochem Physiol 124:8–14. https://doi.org/10.1016/j.pestbp.2015.03.010
Khan MF, Murphy CD (2023) Fluorotelomer alcohols are efficiently biotransformed by Cunninghamella elegans. Environ Sci Pollut Res 30:23613–23623. https://doi.org/10.1007/s11356-022-23901-0
doi: 10.1007/s11356-022-23901-0
Kim YH, Lee CJ, Go HY, Konishi KY, Lee KS, Peter CKL, Yu MH (2010) Decolorization of malachite green by cytochrome c in the mitochondria of the fungus Cunninghamella elegans. Arch Biochem Biophys 494(2):159–165. https://doi.org/10.1016/j.abb.2009.11.027
doi: 10.1016/j.abb.2009.11.027
pubmed: 19944668
Kumar R, Singh B, Gupta VK (2012) Biodegradation of fipronil by Paracoccus sp. in different types of soil. Bull Environ Contam Toxicol 88(5):781–787. https://doi.org/10.1007/s00128-012-0578-y
doi: 10.1007/s00128-012-0578-y
pubmed: 22371192
Lawrie RD, Mitchelll RD, Dhammi A, Wallace A, Hodgson E, Roe RM (2020) Role of long non-coding RNAin DEET- and fipronil-mediated alteration of transcripts associated with phase I and phase II xenobiotic metabolism in human primary hepatocytes. Pestic Biochem Phys 167:104607. https://doi.org/10.1016/j.pestbp.2020.104607
doi: 10.1016/j.pestbp.2020.104607
Lee H, Kim E, Shin Y, Lee JH, Hur HG, Kim JH (2016) Identification and formation pattern of metabolites of cyazofamid by soil fungus Cunninghamella elegans. J Korean Soc Appl Biol Chem 59:9–14. https://doi.org/10.1007/s13765-015-0127-6
doi: 10.1007/s13765-015-0127-6
Li M, Li P, Wang L, Feng M, Han L (2015) Determination and dissipation of fipronil and its metabolites in peanut and soil. J Agric Food Chem 63:4435–4443. https://doi.org/10.1021/jf5054589
doi: 10.1021/jf5054589
pubmed: 25664639
Lu M, Du J, Zhou P, Chen H, Lu C, Zhang Q (2015) Endocrine disrupting potential of fipronil and its metabolite in reporter gene assays. Chemosphere 120:246–251. https://doi.org/10.1016/j.chemosphere.2014.07.015
doi: 10.1016/j.chemosphere.2014.07.015
pubmed: 25112704
Mandal K, Singh B, Jariyal M, Gupta VK (2013) Microbial degradation of fipronil by bacillus thuringiensis. Ecotox Environ Safe 93:87–92. https://doi.org/10.1016/j.ecoenv.2013.04.001
doi: 10.1016/j.ecoenv.2013.04.001
McMahen RL, Strynar MJ, Dagnino S, Herr DW, Moser VC, Garantziotis S, Andersen EM, Freeborn DL, McMillan L, Lindstrom AB (2015) Identification of fipronil metabolites by time-of-flight mass spectrometry for application in a human exposure study. Environ Int 78:16–23. https://doi.org/10.1016/j.envint.2015.01.016
doi: 10.1016/j.envint.2015.01.016
pubmed: 25687022
pmcid: 5247556
Miller JL, Schmidt TS, Metre P, Mahler BJ, Moran PW (2020) Common insecticide disrupts aquatic communities: a mesocosm-to-field ecological risk assessment of fipronil and its degradates in US streams. Sci Adv 6(43):eabc1299. https://doi.org/10.1126/sciadv.abc1299
doi: 10.1126/sciadv.abc1299
pubmed: 33097542
pmcid: 7608825
Moody JD, Freeman JP, Fu PP, Cerniglia CE (2002) Biotransformation of Mirtazapine by Cunninghamella elegans. Drug Metab Dispos 30(11):1274–1279. https://doi.org/10.1124/dmd.30.11.1274
doi: 10.1124/dmd.30.11.1274
pubmed: 12386135
Nace CG, Genter MB, Sayre LM, Crofton KM (1997) Effect of methimazole, an FMO substrate and competitive inhibitor, on the neurotoxicity of 3,3′-iminodipropionitrile in male rats. Toxicol Sci 37:131–140. https://doi.org/10.1006/faat.1997.2307
doi: 10.1006/faat.1997.2307
Ngim KK, Crosby DG (2001) Abiotic processes influencing fipronil and desthiofipronil dissipation in California, USA, rice fields. Environ Toxicol Chem 20(5):972–977. https://doi.org/10.1002/etc.5620200506
doi: 10.1002/etc.5620200506
pubmed: 11337886
Ngim KK, Mabury SA, Crosby DG (2000) Elucidation of fipronil photodegradation pathways. J Agric Food Chem 48(10):4661–4665. https://doi.org/10.1021/jf9913007
doi: 10.1021/jf9913007
pubmed: 11052715
Palmer-Brown W, de Melo Souza PL, Murphy CD (2019) Cyhalothrin biodegradation in Cunninghamella elegans. Environ Sci Pollut Res 26(2):1414–1421. https://doi.org/10.1007/s11356-018-3689-0
doi: 10.1007/s11356-018-3689-0
Qian Y, Wang C, Wang J, Zhang X, Zhou Z, Zhao M, Lu C (2017) Fipronil-induced enantioselective developmental toxicity to zebrafish embryo-larvae involves changes in DNA methylation. Sci Rep 7:1–11. https://doi.org/10.1038/s41598-017-02255-5
doi: 10.1038/s41598-017-02255-5
Ramasubramanian T, Paramasivam M (2017) Determination and dissipation of fipronil and its metabolites in/on sugarcane crop. Int J Environ Anal Chem 97(11):1037–1052. https://doi.org/10.1080/03067319.2017.1377519
doi: 10.1080/03067319.2017.1377519
Schocken MJ, Mao J, Schabacker DJ (1997) Microbial transformations of the fungicide cyprodinil (CGA-219417). J Agric Food Chem 45:3647–3651. https://doi.org/10.1021/jf970298l
doi: 10.1021/jf970298l
Singh BK, Walker A (2006) Microbial degradation of organophosphorus compounds. FEMS Microbiol Rev 30(3):428–471. https://doi.org/10.1111/j.1574-6976.2006.00018.x
doi: 10.1111/j.1574-6976.2006.00018.x
pubmed: 16594965
Singh NS, Sharma R, Singh SK, Singh DK (2021) A comprehensive review of environmental fate and degradation of fipronil and its toxic metabolites. Environ Res 199(5):111316. https://doi.org/10.1016/j.envres.2021.111316
doi: 10.1016/j.envres.2021.111316
pubmed: 33989624
Slotkin TA, Skavicus S, Card J, Levin ED, Seidler FJ (2016) Diverse neurotoxicants target the differentiation of embryonic neural stem cells into neuronal and glial phenotypes. Toxicology 372:42–51. https://doi.org/10.1016/j.tox.2016.10.015
doi: 10.1016/j.tox.2016.10.015
pubmed: 27816694
Song X, Wang XL, Liao GQ, Pan YC, Qian YZ, Qiu J (2021) Toxic effects of fipronil and its metabolites on PC12 cell metabolism. Ecotoxicol Environ Saf 224:112677. https://doi.org/10.1016/j.ecoenv.2021.112677
doi: 10.1016/j.ecoenv.2021.112677
pubmed: 34450423
Sorrentino JM, Sponchiado RM, Santos N, Oliveira SS (2019) Biotransformation of metronidazole by cunninghamella elegans ATCC 9245. Drug Anal Res 3(1):36–41. https://doi.org/10.22456/2527-2616.94032
doi: 10.22456/2527-2616.94032
Sponchiado R, Sorrentino J, Cordenonsi LM, Fuentefria AM, Garcia CV (2020) Rifampicin: biotransformation study using the fungus Cunninghamella elegans and monitoring through UHPLC-MS. Drug Anal Res 4(1):44–48. https://doi.org/10.22456/2527-2616.101989
doi: 10.22456/2527-2616.101989
Stockdale DP, Beutler JA, Wiemer DF (2017) Synthesis of amide isosteres of schweinfurthin-based stilbenes. Bioorgan Med Chem 25(20):5483–5489. https://doi.org/10.1016/j.bmc.2017.08.016
doi: 10.1016/j.bmc.2017.08.016
Tang J, Usmani KA, Hodgson E, Rose RL (2004) In vitro metabolism of fipronil by human and rat cytochrome P450 and its interactions with testosterone and diazepam. Chem Biol Interact 147:319–329. https://doi.org/10.1016/j.cbi.2004.03.002
doi: 10.1016/j.cbi.2004.03.002
pubmed: 15135087
Uniyal S, Paliwal R, Sharma RK, Rai JPN (2016) Degradation of fipronil by Stenotrophomonas acidaminiphila isolated from rhizospheric soil of Zea mays. 3 Biotech 6:48. https://doi.org/10.1007/s13205-015-0354-x
doi: 10.1007/s13205-015-0354-x
pubmed: 28330119
pmcid: 4746198
Vasylieva N, Ahn KC, Barnych B, Gee SJ, Hammock BD (2015) Development of an immunoassay for the detection of the phenylpyrazole insecticide fipronil. Environ Sci Technol 49:10038–10047. https://doi.org/10.1021/acs.est.5b01005
doi: 10.1021/acs.est.5b01005
pubmed: 26196357
pmcid: 4605820
Vasylieva N, Barnych B, Wan D, El-Sheikh ESA, Nguyen HM, Wulff H, McMahen R, Strynar M, Gee SJ, Hammock BD (2017) Hydroxy-fipronil is a new urinary biomarker of exposure to fipronil. Environ Int 103:91–98. https://doi.org/10.1016/j.envint.2017.03.012
doi: 10.1016/j.envint.2017.03.012
pubmed: 28343720
pmcid: 5432128
Wan K, Jiang XY, Tang XM, Xiao L, Chen Y, Huang CL, Zhu FW, Wang FH, Xu HH (2022) Study on absorption, distribution, metabolism, and excretion properties of novel insecticidal GABA receptor antagonist, pyraquinil, in diamondback moth combining maldi mass spectrometry imaging and high-resolution mass spectrometry. J Agric Food Chem 70(20):6072–6083. https://doi.org/10.1021/acs.jafc.2c00468
doi: 10.1021/acs.jafc.2c00468
pubmed: 35576451
Wang X, Martínez MA, Wu Q, Ares I, Martínez-Larranaga MR, Anadon A, Yuan Z (2016) Fipronil insecticide toxicology: oxidative stress and metabolism. Crit Rev Toxicol 46(10):876–899. https://doi.org/10.1080/10408444.2016.1223014
doi: 10.1080/10408444.2016.1223014
pubmed: 27643517
Wolfand JM, LeFevre GH, Luthy RG (2016) Metabolization and degradation kinetics of the urban-use pesticide fipronil by white rot fungus Trametes versicolor. Environ Sci 18:1256–1265. https://doi.org/10.1039/C6EM00344C
doi: 10.1039/C6EM00344C
Zawadzka K, Bernat P, Felczak A, Lisowska K (2015) Carbazole hydroxylation by the filamentous fungi of the Cunninghamella species. Environ Sci Pollut Res 22(24):19658–19666. https://doi.org/10.1007/s11356-015-5146-7
doi: 10.1007/s11356-015-5146-7
Zhao MA, Gu H, Zhang CJ, Jeong IH, Kim JH, Zhu YZ (2020) Metabolism of insecticide diazinon by Cunninghamella elegans ATCC36112. RSC Adv 10:19659–19668. https://doi.org/10.1039/D0RA02253E
doi: 10.1039/D0RA02253E
pubmed: 35515422
pmcid: 9054078
Zhu YZ, Keum YS, Yang L, Lee H, Park H, Kim JH (2010) Metabolism of a fungicide mepanipyrim by soil fungus Cunninghamella elegans ATCC36112. J Agric Food Chem 58:12379–12384. https://doi.org/10.1021/jf102980y
doi: 10.1021/jf102980y
pubmed: 21047134
Zhu YZ, Fu M, Jeong IH, Kim JH, Zhang CJ (2017) Metabolism of an Insecticide Fenitrothion by Cunninghamella elegans ATCC36112. J Agric Food Chem 65(49):10711–10718. https://doi.org/10.1021/acs.jafc.7b04273
doi: 10.1021/acs.jafc.7b04273
pubmed: 29144738