Volume 42 Issue 3
May  2021
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Article Contents
Huan Wang, Tian-Xiu Qiu, Jian-Fei Lu, Han-Wei Liu, Ling Hu, Lei Liu, Jiong Chen. Potential aquatic environmental risks of trifloxystrobin: Enhancement of virus susceptibility in zebrafish through initiation of autophagy. Zoological Research, 2021, 42(3): 339-349. doi: 10.24272/j.issn.2095-8137.2021.056
Citation: Huan Wang, Tian-Xiu Qiu, Jian-Fei Lu, Han-Wei Liu, Ling Hu, Lei Liu, Jiong Chen. Potential aquatic environmental risks of trifloxystrobin: Enhancement of virus susceptibility in zebrafish through initiation of autophagy. Zoological Research, 2021, 42(3): 339-349. doi: 10.24272/j.issn.2095-8137.2021.056

Potential aquatic environmental risks of trifloxystrobin: Enhancement of virus susceptibility in zebrafish through initiation of autophagy

doi: 10.24272/j.issn.2095-8137.2021.056
Funds:  This work was supported by the National Natural Science Foundation of China (31902410), Program of State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products (KF20200106), Natural Science Foundation of Zhejiang Province (LY21C190002), and Foundation of Ningbo City of China (202003N4120)
More Information
  • Corresponding author: E-mail: liulei2@nbu.edu.cnjchen1975@163.com
  • Received Date: 2021-02-20
  • Accepted Date: 2021-04-06
  • Published Online: 2021-05-08
  • Publish Date: 2021-05-18
  • Chronic pollution in aquatic ecosystems can lead to many adverse effects, including a greater susceptibility to pathogens among resident biota. Trifloxystrobin (TFS) is a strobilurin fungicide widely used in Asia to control soybean rust. However, it has the potential to enter aquatic ecosystems, where it may impair fish resistance to viral infections. To explore the potential environmental risks of TFS, we characterized the antiviral capacities of fish chronically exposed to TFS and subsequently infected with spring viraemia of carp virus (SVCV). Although TFS exhibited no significant cytotoxicity at the tested environmental concentrations during viral challenge, SVCV replication increased significantly in a time-dependent manner within epithelioma papulosum cyprini (EPC) cells and zebrafish exposed to 25 μg/L TFS. Results showed that the highest viral load was more than 100-fold that of the controls. Intracellular biochemical assays indicated that autophagy was induced by TFS, and associated changes included an increase in autophagosomes, conversion of LC3-II, accumulation of Beclin-1, and degradation of P62 in EPC cells and zebrafish. In addition, TFS markedly decreased the expression and phosphorylation of mTOR, indicating that activation of TFS may be associated with the mTOR-mediated autophagy pathway. This study provides new insights into the mechanism of the immunosuppressive effects of TFS on non-target aquatic hosts and suggests that the existence of TFS in aquatic environments may contribute to outbreaks of viral diseases.
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  • [1]
    Ahne W, Bjorklund HV, Essbauer S, Fijan N, Kurath G, Winton JR. 2002. Spring viremia of carp (SVC). Diseases of Aquatic Organisms, 52(3): 261−272.
    [2]
    Balmer BF, Powers RL, Zhang TH, Lee J, Vigant F, Lee B, et al. 2017. Inhibition of an aquatic rhabdovirus demonstrates promise of a broad-spectrum antiviral for use in aquaculture. Journal of Virology, 91(4): e02181−16.
    [3]
    Bartlett DW, Clough JM, Godwin JR, Hall AA, Hamer M, Parr-Dobrzanski B. 2002. The strobilurin fungicides. Pest Management Science, 58(7): 649−662. doi: 10.1002/ps.520
    [4]
    Bello-Perez M, Pereiro P, Coll J, Novoa B, Perez L, Falco A. 2020. Zebrafish C-reactive protein isoforms inhibit SVCV replication by blocking autophagy through interactions with cell membrane cholesterol. Scientific Reports, 10(1): 566. doi: 10.1038/s41598-020-57501-0
    [5]
    Cao MC, Li SY, Wang QS, Wei P, Liu YN, Zhu GN, et al. 2015. Track of fate and primary metabolism of trifloxystrobin in rice paddy ecosystem. Science of the Total Environment, 518–519: 417−423.
    [6]
    Chen ZY, Liu H, Li ZQ, Wang M, Zhang QY. 2006. Detection of viral pathogen from diseased common carp (Cyprinus carpio) by infectious tests. Journal of Fishery Sciences of China, 13(4): 617−623. (in Chinese)
    [7]
    Cheng P, Ni Z, Dai X, Wang B, Ding W, Smith AR, et al. 2013. The novel BH-3 mimetic apogossypolone induces Beclin-1- and ROS-mediated autophagy in human hepatocellular carcinoma cells. Cell Death & Disease, 4(2): e489.
    [8]
    Cheng Y, Azad MB, Gibson SB. 2009. Superoxide is the major reactive oxygen species regulating autophagy. Cell Death & Differentiation, 16(7): 1040−1052.
    [9]
    Collotta M, Bertazzi PA, Bollati V. 2013. Epigenetics and pesticides. Toxicology, 307: 35−41. doi: 10.1016/j.tox.2013.01.017
    [10]
    Cui F, Chai TT, Liu XX, Wang CJ. 2017. Toxicity of three strobilurins (Kresoxim-methyl, pyraclostrobin, and trifloxystrobin) on Daphnia magna. Environmental Toxicology and Chemistry, 36(1): 182−189. doi: 10.1002/etc.3520
    [11]
    Deb D, Engel BA, Harbor J, Hahn L, Lim KJ, Zhai T. 2010. Investigating potential water quality impacts of fungicides used to combat soybean rust in Indiana. Water, Air, and Soil Pollution, 207(1–4): 273−288.
    [12]
    Dietrich JP, Van Gaest AL, Strickland SA, Arkoosh MR. 2014. The impact of temperature stress and pesticide exposure on mortality and disease susceptibility of endangered Pacific salmon. Chemosphere, 108: 353−359. doi: 10.1016/j.chemosphere.2014.01.079
    [13]
    Dikic I, Elazar Z. 2018. Mechanism and medical implications of mammalian autophagy. Nature Reviews Molecular Cell Biology, 19(6): 349−364. doi: 10.1038/s41580-018-0003-4
    [14]
    Dikkeboom AL, Radi C, Toohey-Kurth K, Marcquenski S, Engel M, Goodwin AE, et al. 2004. First report of spring viremia of carp virus (SVCV) in wild common carp in North America. Journal of Aquatic Animal Health, 16(4): 169−178. doi: 10.1577/H03-064.1
    [15]
    Dupuy C, Cabon J, Louboutin L, Le Floch S, Morin T, Danion M. 2019. Cellular, humoral and molecular responses in rainbow trout (Oncorhynchus mykiss) exposed to a herbicide and subsequently infected with infectious hematopoietic necrosis virus. Aquatic Toxicology, 215: 105282. doi: 10.1016/j.aquatox.2019.105282
    [16]
    European Food Safety Authority (EFSA), Arena M, Auteri D, Barmaz S, Bellisai G, Brancato A, et al. 2017. Peer review of the pesticide risk assessment of the active substance trifloxystrobin. FESA Journal, 15(10): e04989.
    [17]
    Feng YM, Huang YH, Zhan H, Bhatt P, Chen SH. 2020. An overview of strobilurin fungicide degradation: current status and future perspective. Frontier in Microbiology, 11: 389. doi: 10.3389/fmicb.2020.00389
    [18]
    Garver KA, Dwilow AG, Richard J, Booth TF, Beniac DR, Souter BW. 2007. First detection and confirmation of spring viraemia of carp virus in common carp, Cyprinus carpio L., From Hamilton Harbour, Lake Ontario, Canada. Journal of Fish Diseases, 30(11): 665−671. doi: 10.1111/j.1365-2761.2007.00851.x
    [19]
    Gotesman M, Soliman H, Besch R, El-Matbouli M. 2015. Inhibition of spring viraemia of carp virus replication in an Epithelioma papulosum cyprini cell line by RNAi. Journal of Fish Diseases, 38(2): 197−207. doi: 10.1111/jfd.12227
    [20]
    He BN, Wang X, Yang CL, Zhu JB, Jin YX, Fu ZW. 2020. The regulation of autophagy in the pesticide-induced toxicity: Angel or demon?. Chemosphere, 242: 125138. doi: 10.1016/j.chemosphere.2019.125138
    [21]
    He CC, Klionsky DJ. 2009. Regulation mechanisms and signaling pathways of autophagy. Annual Review of Genetics, 43: 67−93. doi: 10.1146/annurev-genet-102808-114910
    [22]
    Jang Y, Kim JE, Jeong SH, Paik MK, Kim JS, Cho MH. 2016. Trifloxystrobin-induced mitophagy through mitochondrial damage in human skin keratinocytes. The Journal of Toxicological Sciences, 41(6): 731−737. doi: 10.2131/jts.41.731
    [23]
    Junges CM, Peltzer PM, Lajmanovich RC, Attademo AM, Cabagna Zenklusen MC, Basso A. 2012. Toxicity of the fungicide trifloxystrobin on tadpoles and its effect on fish-tadpole interaction. Chemosphere, 87: 1348−1354. doi: 10.1016/j.chemosphere.2012.02.026
    [24]
    Komárek M, Čadková E, Chrastný V, Bordas F, Bollinger JC. 2010. Contamination of vineyard soils with fungicides: a review of environmental and toxicological aspects. Environment International, 36(1): 138−151. doi: 10.1016/j.envint.2009.10.005
    [25]
    Koutná M, Veselý T, Psikal I, Hůlová J. 2003. Identification of spring viraemia of carp virus (SVCV) by combined RT-PCR and nested PCR. Diseases of Aquatic Organisms, 55(3): 229−235.
    [26]
    Levine B, Deretic V. 2007. Unveiling the roles of autophagy in innate and adaptive immunity. Nature Reviews Immunology, 7(10): 767−777. doi: 10.1038/nri2161
    [27]
    Li H, Cao FJ, Zhao F, Yang Y, Teng MM, Wang CJ, et al. 2018. Developmental toxicity, oxidative stress and immunotoxicity induced by three strobilurins (pyraclostrobin, trifloxystrobin and picoxystrobin) in zebrafish embryos. Chemosphere, 207: 781−790. doi: 10.1016/j.chemosphere.2018.05.146
    [28]
    Liu L, Hu Y, Shen YF, Wang GX. 2017. Evaluation on antiviral activity of coumarin derivatives against spring viraemia of carp virus in epithelioma papulosum cyprini cells. Antiviral Research, 144: 173−185. doi: 10.1016/j.antiviral.2017.06.007
    [29]
    Liu L, Jiang C, Wu ZQ, Gong YX, Wang GX. 2013. Toxic effects of three strobilurins (trifloxystrobin, azoxystrobin and kresoxim-methyl) on mRNA expression and antioxidant enzymes in grass carp (Ctenopharyngodon idella) juveniles. Ecotoxicology and Environmental Safety, 98: 297−302. doi: 10.1016/j.ecoenv.2013.10.011
    [30]
    Liu L, Song DW, Liu GL, Shan LP, Qiu TX, Chen J. 2020a. Hydroxycoumarin efficiently inhibits spring viraemia of carp virus infection in vitro and in vivo. Zoological Research, 41(4): 395−409. doi: 10.24272/j.issn.2095-8137.2020.037
    [31]
    Liu LY, Zhu BB, Wu SS, Lin L, Liu GX, Zhou Y, et al. 2015. Spring viraemia of carp virus induces autophagy for necessary viral replication. Cellular Microbiology, 17(4): 595−605. doi: 10.1111/cmi.12387
    [32]
    Liu T, Liu YL, Fang K, Zhang XL, Wang XG. 2020b. Transcriptome, bioaccumulation and toxicity analyses of earthworms (Eisenia fetida) affected by trifloxystrobin and trifloxystrobin acid. Environmental Pollution, 265: 115100. doi: 10.1016/j.envpol.2020.115100
    [33]
    Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods, 25(4): 402−408. doi: 10.1006/meth.2001.1262
    [34]
    Luo XS, Qin XX, Liu ZY, Chen D, Yu WW, Zhang KK, et al. 2020. Determination, residue and risk assessment of trifloxystrobin, trifloxystrobin acid and tebuconazole in Chinese rice consumption. Biomedical Chromatography, 34(1): e4694.
    [35]
    Ma JG, Zhu JY, Wang WY, Ruan PP, Rajeshkumar S, Li XY. 2019. Biochemical and molecular impacts of glyphosate-based herbicide on the gills of common carp. Environmental Pollution, 252: 1288−1300. doi: 10.1016/j.envpol.2019.06.040
    [36]
    Morley NJ. 2010. Interactive effects of infectious diseases and pollution in aquatic molluscs. Aquatic Toxicology, 96(1): 27−36. doi: 10.1016/j.aquatox.2009.09.017
    [37]
    Orvedahl A, Alexander D, Tallóczy Z, Sun QH, Wei YJ, Zhang W, et al. 2007. HSV-1 ICP34.5 confers neurovirulence by targeting the Beclin 1 autophagy protein. Cell Host & Microbe, 1(1): 23−35.
    [38]
    Pesonen M, Vähäkangas K. 2019. Autophagy in exposure to environmental chemicals. Toxicology Letters, 305: 1−9. doi: 10.1016/j.toxlet.2019.01.007
    [39]
    Pizzi M. 1950. Sampling variation of the fifty percent end-point, determined by the Reed-Muench (Behrens) method. Human Biology, 22(3): 151−190.
    [40]
    Qin L, Wang Z, Tao LY, Wang Y. 2010. Er stress negatively regulates AKT/TSC/mTOR pathway to enhance autophagy. Autophagy, 6(2): 239−247. doi: 10.4161/auto.6.2.11062
    [41]
    Schmid D, Dengjel J, Schoor O, Stevanovic S, Münz C. 2006. Autophagy in innate and adaptive immunity against intracellular pathogens. Journal of Molecular Medicine, 84(3): 194−202. doi: 10.1007/s00109-005-0014-4
    [42]
    Shoji-Kawata S, Levine B. 2009. Autophagy, antiviral immunity, and viral countermeasures. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research, 1793(9): 1478−1484. doi: 10.1016/j.bbamcr.2009.02.008
    [43]
    Song JY, Nakayama K, Murakami Y, Kitamura SI. 2011. Heavy oil exposure induces high moralities in virus carrier Japanese flounder Paralichthys olivaceus. Marine Pollution Bulletin, 63(5–12): 362−365.
    [44]
    Taylor NGH, Peeler EJ, Denham KL, Crane CN, Thrush MA, Dixon PF, et al. 2013. Spring viraemia of carp (SVC) in the UK: the road to freedom. Preventive Veterinary Medicine, 111(1–2): 156−164.
    [45]
    Varela M, Romero A, Dios S, Van der Vaart M, Figueras A, Meijer AH, et al. 2014. Cellular visualization of macrophage pyroptosis and interleukin-1β release in a viral hemorrhagic infection in zebrafish larvae. Journal of Virology, 88(20): 12026−12040. doi: 10.1128/JVI.02056-14
    [46]
    Wan G, Xie WD, Liu ZY, Xu W, Lao YZ, Huang N, et al. 2014. Hypoxia-induced MIR155 is a potent autophagy inducer by targeting multiple players in the MTOR pathway. Autophagy, 10(1): 70−79. doi: 10.4161/auto.26534
    [47]
    Wang C, Wu JX, Zhang Y, Wang K, Zhang HY. 2015. Field dissipation of trifloxystrobin and its metabolite trifloxystrobin acid in soil and apples. Environmental Monitoring and Assessment, 187(1): 4100. doi: 10.1007/s10661-014-4100-3
    [48]
    Wang K, Sun ZH, Yang LD, He L, Li XH, Wang G. 2020. Respiratory toxicity of azoxystrobin, pyraclostrobin and coumoxystrobin on Chlorella vulgaris. Bulletin of Environmental Contamination and Toxicology, 104(6): 799−803. doi: 10.1007/s00128-020-02869-y
    [49]
    Wightwick AM, Bui AD, Zhang P, Rose G, Allinson M, Myers JH, et al. 2012. Environmental fate of fungicides in surface waters of a horticultural-production catchment in southeastern Australia. Archives of Environmental Contamination and Toxicology, 62(3): 380−390. doi: 10.1007/s00244-011-9710-y
    [50]
    Xing HJ, Liu T, Zhang ZW, Wang XL, Xu SW. 2015. Acute and subchronic toxic effects of atrazine and chlorpyrifos on common carp (Cyprinus carpio L.): immunotoxicity assessments. Fish & Shellfish Immunology, 45(2): 327−333.
    [51]
    Xiong JB, Nie L, Chen J. 2019. Current understanding on the roles of gut microbiota in fish disease and immunity. Zoological Research, 40(2): 70−76. doi: 10.24272/j.issn.2095-8137.2018.069
    [52]
    Yoon SY, Ha YE, Choi JE, Ahn J, Lee H, Kweon HS, et al. 2008. Coxsackievirus B4 uses autophagy for replication after calpain activation in rat primary neurons. Journal of Virology, 82(23): 11976−11978. doi: 10.1128/JVI.01028-08
    [53]
    Yuan JF, Yang Y, Nie HH, Li LJ, Gu WG, Lin L, et al. 2014. Transcriptome analysis of epithelioma papulosum cyprini cells after SVCV infection. BMC Genomics, 15: 935. doi: 10.1186/1471-2164-15-935
    [54]
    Zhang YN, Li ZC, Ge XN, Guo X, Yang HC. 2011. Autophagy promotes the replication of encephalomyocarditis virus in host cells. Autophagy, 7(6): 613−628. doi: 10.4161/auto.7.6.15267
    [55]
    Zhu B, Liu GL, Liu L, Ling F, Wang GX. 2015a. Assessment of trifloxystrobin uptake kinetics, developmental toxicity and mRNA expression in rare minnow embryos. Chemosphere, 120: 447−455. doi: 10.1016/j.chemosphere.2014.07.100
    [56]
    Zhu LF, Wang HL, Liu HJ, Li W. 2015b. Effect of trifloxystrobin on hatching, survival, and gene expression of endocrine biomarkers in early life stages of medaka (Oryzias latipes). Environmental Toxicology, 30(6): 648−655. doi: 10.1002/tox.21942
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