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Toxicological effects benzotriazole to the marine scallop Chlamys nobilis: a 2-month exposure study

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Abstract

Benzotriazole and its associated derivatives (BTs) are widely used as ultraviolet stabilizers and corrosion inhibitors. They have been extensively found in marine environments and are bioaccumulative through the food chain. However, the toxicities of BTs to marine organisms are seldom identified and no assessment has been conducted for filter-feeding bivalves. In this study, a marine scallop Chlamys nobilis was exposed to 0, 0.01, 0.1, and 1.0 mg/L of BT for 60 days. Effects of BT on endocrine system, cytochrome P450 activity, antioxidant activity, and neural activity of C. nobilis were examined. The results showed that BT exerted significant estrogenic effects on both male and female scallops and inhibited EROD activities of C. nobilis even at 0.01 mg/L level. BT at ≥ 0.01 mg/L levels also caused significant oxidative stress on C. nobilis. Moreover, most of the adverse effects of BT to C. nobilis were found from day 35 and 0.01 mg/L was the lowest concentration with observed effects, showing the long-term toxic effects of BT to C. nobilis. Thus, the adverse effects of BT and its derivatives to marine benthic communities deserve more attention in future research.

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References

  • Aebi H (1984) [13] Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  Google Scholar 

  • Bhat HK, Calaf G, Hei TK, Loya T, Vadgama JV (2003) Critical role of oxidative stress in estrogen-induced carcinogenesis. Proc Natl Acad Sci 100:3913–3918

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Breedveld GD, Roseth R, Hem L, Sparrevik M (2002) Triazoles in the terrestrial environment. 20001103-1 final report. Norwegian geotechnical institute, Oslo

    Google Scholar 

  • Cancilla DA, Martinez J, Van Aggelen GC (1998) Detection of aircraft deicing/antiicing fluid additives in a perched water monitoring well at an international airport. Environ Sci Technol 32:3834–3835

    Article  CAS  Google Scholar 

  • Coburn C, Hudgens R, Mullen M (1999) Environmental effects of engine coolant additives. SAE technical paper 1999-01-0137. https://doi.org/10.4271/1999-01-0137

  • Cohen G, Kim M, Ogwu V (1996) A modified catalase assay suitable for a plate reader and for the analysis of brain cell cultures. J Neurosci Methods 67:53–56

    Article  CAS  Google Scholar 

  • Cooke J, Hinton D (1999) Promotion by 17β-estradiol and β-hexachlorocyclohexane of hepatocellular tumors in medaka, Oryzias latipes. Aquat Toxicol 45:127–145

    Article  CAS  Google Scholar 

  • De Montellano PO, Mathews JM (1981) Autocatalytic alkylation of the cytochrome P-450 prosthetic haem group by 1-aminobenzotriazole. Isolation of an NN-bridged benzyne-protoporphyrin IX adduct. Biochem J 195:761–764

    Article  Google Scholar 

  • Draper H, Hadley M (1990) [43] malondialdehyde determination as index of lipid peroxidation. Methods Enzymol 186:421–431

    Article  CAS  Google Scholar 

  • Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–90

    Article  CAS  Google Scholar 

  • Esterbauer H, Cheeseman KH (1990) Determination of aldehydic lipid-peroxidation products - malonaldehyde and 4-hydroxynonenal. Methods Enzymol 186:407–421

    Article  CAS  Google Scholar 

  • Fent K, Woodin BR, Stegeman JJ (1998) Effects of triphenyltin and other organotins on hepatic monooxygenase system in fish. Comp Biochem Physiol Part C Toxicol Pharmacol 121:277–288

    CAS  Google Scholar 

  • Fent K, Chew G, Li J, Gomez E (2014) Benzotriazole UV-stabilizers and benzotriazole: antiandrogenic activity in vitro and activation of aryl hydrocarbon receptor pathway in zebrafish eleuthero-embryos. Sci Total Environ 482:125–136

    Article  CAS  Google Scholar 

  • Gagné F, Blaise C, Salazar M, Salazar S, Hansen PD (2001) Evaluation of estrogenic effects of municipal effluents to the freshwater mussel Elliptio complanata. Comp Biochem Physiol Part C Toxicol Pharmacol 128:213–225

    Article  Google Scholar 

  • Giger W, Schaffner C, Kohler HPE (2006) Benzotriazole and tolyltriazole as aquatic contaminants. 1. Input and occurrence in rivers and lakes. Environ Sci Technol 40:7186–7192

    Article  CAS  Google Scholar 

  • Harris CA, Routledge EJ, Schaffner C, Brian JV, Giger W, Sumpter JP (2007) Benzotriazole is antiestrogenic in vitro but not in vivo. Environ Toxicol Chem 26:2367–2372

    Article  CAS  Google Scholar 

  • Hart D, Davis L, Erickson L, Callender T (2004) Sorption and partitioning parameters of benzotriazole compounds. Microchem J 77:9–17

    Article  CAS  Google Scholar 

  • Hartwell SI, Jordahl DM, Evans JE, May EB (1995) Toxicity of aircraft de-icer and anti-icer solutions to aquatic organisms. Environ Toxicol Chem 14:1375–1386

    Article  CAS  Google Scholar 

  • He TT, Liang B, Liu WH, Shin PKS, Wu RSS (2012) Estrogenic potential of benzotriazole on marine medaka (Oryzias melastigma). Ecotoxicol Environ Saf 80:327–332

    Article  CAS  Google Scholar 

  • Health Council of The Netherlands (2000) Dutch expert committee on occupational standards (DECOS): 1,2,3-Benzotriazole. Health Council of the Netherlands, the Hague (publication no. 2000/14OSH)

  • Jeong HG, Kim JY, Choi CY, You HJ, Hahm KS (2001) Suppression of CYP1A1 expression by 4-nonylphenol in murine Hepa-1c1c7 cells. Cancer Lett 165:95–101

    Article  CAS  Google Scholar 

  • Kadar E, Dashfield S, Hutchinson TH (2010) Developmental toxicity of benzotriazole in the protochordate Ciona intestinalis (Chordata, Ascidiae). Anal Bioanal Chem 396:641–647

    Article  CAS  Google Scholar 

  • Kiss A, Fries E (2009) Occurrence of benzotriazoles in the rivers Main, Hengstbach, and Hegbach (Germany). Environ Sci Pollut Res 16:702–710

    Article  CAS  Google Scholar 

  • Konuma S, Ogawa A, Masunaga S, Nakamura Y (2009) UV filters in seawater and sediment: partitioning and horizontal distributions on the coastal shoreline in and around the Tokyo Bay. In: 18th Symposium on Environmental Chemistry, pp 448–449

  • Krüner G, Westernhagen HV (1999) Sources of measurement error in assays of EROD activity of fish for biological effects monitoring. Helgol Mar Res 53:250–256

    Article  Google Scholar 

  • Kucuksezgin F, Pazi I, Yucel-Gier G, Akcali B, Galgani F (2013) Monitoring of heavy metal and organic compound levels along the eastern Aegean coast with transplanted mussels. Chemosphere 93:1511–1518

    Article  CAS  Google Scholar 

  • Liang XF, Wang M, Chen X, Zha JM, Chen HH, Zhu LF, Wang ZJ (2014) Endocrine disrupting effects of benzotriazole in rare minnow (Gobiocypris rarus) in a sex-dependent manner. Chemosphere 112:154–162

    Article  CAS  Google Scholar 

  • Liang XF, Martyniuk CJ, Zha JM, Wang ZJ (2016) Brain quantitative proteomic responses reveal new insight of benzotriazole neurotoxicity in female Chinese rare minnow (Gobiocypris rarus). Aquat Toxicol 181:67–75

    Article  CAS  Google Scholar 

  • Liang XF, Zha JM, Martyniuk CJ, Wang ZJ, Zhao J (2017) Histopathological and proteomic responses in male Chinese rare minnow (Gobiocypris rarus) indicate hepatotoxicity following benzotriazole exposure. Environ Pollut 229:459–469

    Article  CAS  Google Scholar 

  • Liu YS, Ying GG, Shareef A, Kookana RS (2012) Occurrence and removal of benzotriazoles and ultraviolet filters in a municipal wastewater treatment plant. Environ Pollut 165:225–232

    Article  CAS  Google Scholar 

  • Loos R, Gawlik BM, Locoro G, Rimaviciute E, Contini S, Bidoglio G (2009) EU-wide survey of polar organic persistent pollutants in European river waters. Environ Pollut 157:561–568

    Article  CAS  Google Scholar 

  • Montesdeoca-Esponda S, Sosa-Ferrera Z, Santana-Rodríguez JJ (2012) On-line solid-phase extraction coupled to ultra-performance liquid chromatography with tandem mass spectrometry detection for the determination of benzotriazole UV stabilizers in coastal marine and wastewater samples. Anal Bioanal Chem 403:867–876

    Article  CAS  Google Scholar 

  • Nakata H, Murata S, Filatreau J (2009) Occurrence and concentrations of benzotriazole UV stabilizers in marine organisms and sediments from the Ariake Sea, Japan. Environ Sci Technol 43:6920–6926

    Article  CAS  Google Scholar 

  • Nakata H, Shinohara R, Murata S, Watanabe M (2010) Detection of benzotriazole UV stabilizers in the blubber of marine mammals by gas chromatography-high resolution mass spectrometry (GC-HRMS). J Environ Monit 12:2088–2092

    Article  CAS  Google Scholar 

  • Nakata H, Shinohara RI, Nakazawa Y, Isobe T, Sudaryanto A, Subramanian A, Tanabe S, Zakaria MP, Zheng GJ, Lam PKS, Kim EY, Min BY, We SU, Viet PH, Tana TS, Prudente M, Frank D, Lauenstein G, Kannan K (2012) Asia-Pacific mussel watch for emerging pollutants: distribution of synthetic musks and benzotriazole UV stabilizers in Asian and US coastal waters. Mar Pollut Bull 64:2211–2218

    Article  CAS  Google Scholar 

  • Navas JM, Segner H (2001) Estrogen-mediated suppression of cytochrome P4501A (CYP1A) expression in rainbow trout hepatocytes: role of estrogen receptor. Chem Biol Interact 138:285–298

    Article  CAS  Google Scholar 

  • Parks N (2009) UV-stabilizing chemicals contaminating Japan’s marine environment. Environ Sci Technol 43:6896–6897

    Article  CAS  Google Scholar 

  • Ricci MS, Toscano DG, Mattingly CJ, Toscano WA (1999) Estrogen receptor reduces CYP1A1 induction in cultured human endometrial cells. J Biol Chem 274:3430–3438

    Article  CAS  Google Scholar 

  • Rollinson G, Callely AG (1986) No evidence for the biodegradation of benzotriazole by elective culture or continuous enrichment. Biotechnol Lett 8:303–304

    Article  CAS  Google Scholar 

  • Song S, Ruan T, Wang T, Liu R, Jiang G (2014) Occurrence and removal of benzotriazole ultraviolet stabilizers in a wastewater treatment plant in China. Environ Sci: Process Impacts 16:1076–1082

    CAS  Google Scholar 

  • Stanton MG (1968) Colorimetric determination of inorganic phosphate in the presence of biological material and adenosine triphosphate. Anal Biochem 22:27–34

    Article  CAS  Google Scholar 

  • Vaccaro E, Meucci V, Intorre L, Soldani G, Di Bello D, Longo V, Gervasi PG, Pretti C (2005) Effects of 17 beta-estradiol, 4-nonylphenol and PCB 126 on the estrogenic activity and phase 1 and 2 biotransformation enzymes in male sea bass (Dicentrarchus labrax). Aquat Toxicol 75:293–305

    Article  CAS  Google Scholar 

  • Voutsa D, Hartmann P, Schaffner C, Giger W (2006) Benzotriazoles, alkylphenols and bisphenol a in municipal wastewaters and in the Glatt River, Switzerland. Environ Sci Pollut Res 13:333–341

    Article  CAS  Google Scholar 

  • Weiss S, Reemtsma T (2005) Determination of benzotriazole corrosion inhibitors from aqueous environmental samples by liquid chromatography-electrospray ionization-tandem mass spectrometry. Anal Chem 77:7415–7420

    Article  CAS  Google Scholar 

  • Whyte JJ, Jung RE, Schmitt CJ, Tillitt DE (2000) Ethoxyresorufin-O-deethylase (EROD) activity in fish as a biomarker of chemical exposure. Crit Rev Toxicol 30:347–570

    Article  CAS  Google Scholar 

  • Wolschke H, Xie ZY, Moller A, Sturm R, Ebinghaus R (2011) Occurrence, distribution and fluxes of benzotriazoles along the German large river basins into the North Sea. Water Res 45:6259–6266

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The help of Yuelin Li in scallop collection and laboratory work are greatly appreciated. Dr. Ping Li, Cui Guo, Diwen Wang, Huibin Cao, Huihui Liu, and Tong Chen from Shantou University also provided invaluable assistance and guidance to this study.

Funding

This work was supported by grants from the Marine Public Welfare Project of China (no. 201005012) and 211 Project of Guangdong Province (no. 20091686).

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Correspondence to Wen-hua Liu.

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Responsible editor: Cinta Porte

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He, Tt., Zhang, T., Liu, Sb. et al. Toxicological effects benzotriazole to the marine scallop Chlamys nobilis: a 2-month exposure study. Environ Sci Pollut Res 26, 10306–10318 (2019). https://doi.org/10.1007/s11356-019-04201-6

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