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The toxicity of sediments from Taihu Lake evaluated by several in vitro bioassays

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Abstract

In vitro bioassays are useful techniques for the determination of biological effects in sediment samples containing complex mixtures of contaminants. In this study, 28 surface sediment samples from Taihu Lake, East China, were collected for toxicity assessment using a battery of in vitro bioassays. The battery included a two-hybrid yeast bioassay for estrogenic and thyroidal effects, the H4IIE rat hepatoma cell bioassay for aryl hydrocarbon (Ah) receptor (Ah-agonists)-mediated effects as measured by ethoxyresorufin-O-deethylase (EROD) activity, and the SOS/umu bioassay for genotoxic effects. Toxicities were expressed as 17β-estradiol equivalents (EEQs), T3 (3,5,3′-triiodothyronine) equivalents (T3-EQs), 2,3,7,8-tetrachlorodibenzo-p-dioxin equivalents (TEQs), and induction ratios (IRs) of β-galactosidase activity. The results showed that total estrogenic effects in sediment samples ranged from 0.0011 to 12.4 pg EEQ/g sediment [dry weight (d.w.)], the thyroidal effects ranged from 0.35 to 24.8 pg T3-EQ/g sediment (d.w.), the Ah-agonist effects varied from 2.70 to 37.8 pg TEQ/g sediment (d.w.), and the weight of soil required for the extracts to lead to a positive result (IR 2.0) in the SOS/umu bioassay was between 1.98 and 15.3 mg (d.w.) per well. Significantly positive correlations were only found between lgT3-EQs and lgEEQs, which indicated similar spatial distributions of estrogenic and thyroidal effects in Taihu Lake. These results suggested that the applied battery of in vitro bioassays represented an efficient (fast and cost-effective) screening system for the identification of emerging contaminants in Taihu Lake and provided meaningful information for further analysis and risk evaluation.

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References

  • Arcaro KF, O’Keefe PW, Yang Y (1999) Antiestrogenicity of environmental polycyclic aromatic hydrocarbons in human breast cancer cells. Toxicology 133:115–127

    Article  CAS  Google Scholar 

  • Bihari N, Fafandel M, Hamer B, Kralj-Bilen B (2006) PAH content, toxicity and genotoxicity of coastal marine sediments from the Rovinj area, Northern Adriatic, Croatia. Sci Total Environ 366:602–611

    Article  CAS  Google Scholar 

  • Boas M, Feldt-Rasmussen U, Main KM (2012) Thyroid effects of endocrine disrupting chemicals. Mol Cell Endocrinol 355:240–248

    Article  CAS  Google Scholar 

  • Brack W (2003) Effect-directed analysis: a promising tool for the identification of organic toxicants in complex mixtures? Anal Bioanal Chem 2003(377):397–407

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Brown SB, Adams BA, Cyr DG, Eales JG (2004) Contaminant effects on the teleost fish thyroid. Environ Toxicol Chem 23:1680–1701

    Article  CAS  Google Scholar 

  • Cachot J, Geffard O, Augagneur S, Lacroix S, Le Menach K, Peluhet L, Couteau J, Denier X, Devier MH, Pottier D, Budzinski H (2006) Evidence of genotoxicity related to high PAH content of sediments in the upper part of the Seine estuary (Normandy, France). Aquat Toxicol 79:257–267

    Article  CAS  Google Scholar 

  • Cao SX, Zeng XY, Song H, Li HR, Yu ZQ, Sheng GY, Fu JM (2012) Levels and distributions of organophosphate flame retardants and plasticizers in sediment from Taihu Lake. China Environ Toxicol Chem 31:1478–1484

    Article  CAS  Google Scholar 

  • Creusot N, Budzinski H, Balaguer P, Kinani S, Porcher JM, Ait-Aissa S (2013) Effect-directed analysis of endocrine-disrupting compounds in multi-contaminated sediment: identification of novel ligands of estrogen and pregnane X receptors. Anal Bioanal Chem 405:2553–2566

    Article  CAS  Google Scholar 

  • Duong CN, Schlenk D, Chang NI, Kim SD (2009) The effect of particle size on the bioavailability of estrogenic chemicals from sediments. Chemosphere 76:395–401

    Article  CAS  Google Scholar 

  • Fetter E, Krauss M, Brion F, Kah O, Scholz S, Brach W (2014) Effect-directed analysis for estrogenic compounds in a fluvial sediment sample using transgenic cyp19a1b-GFP zebrafish embryos. Aquat Toxicol 154:221–229

    Article  CAS  Google Scholar 

  • Fu MZ, Li ZY, Gao HW (2007) Distribution characteristics of nonylphenol in Jiaozhou Bay of Qingdao and its adjacent rivers. Chemosphere 69:1009–1016

    Article  CAS  Google Scholar 

  • Gale RW, Long ER, Schwartz TR, Tillitt DE (2000) Evaluation of planar halogenated and polycyclic aromatic hydrocarbons in estuarine sediments using ethoxyresorufin-O-deethylase induction of H4IIE cells. Environ Toxicol Chem 19:1348–1359

    Article  CAS  Google Scholar 

  • Ghisari M, Bonefeld-Jorgensen ECB (2009) Effects of plasticizers and their mixtures on estrogen receptor and thyroid hormone functions. Toxicol Lett 189:67–77

    Article  CAS  Google Scholar 

  • Giesy JP, Hilscherova K, Jones PD, Kannan K, Machala M (2002) Cell bioassays for detection of aryl hydrocarbon (AhR) and estrogen receptor (ER) mediated activity in environmental samples. Mar Pollut Bull 14:3–16

    Article  Google Scholar 

  • Gutleb AC, Meerts IATM, Bergsma JH, Shriks M, Murk AJ (2005) T-Screen as a tool to identify thyroid hormone receptor active compounds. Environ Toxicol Pharmacol 19:231–238

    Article  CAS  Google Scholar 

  • Gutleb AC, Schriks M, Mossink L, Van den Berg JHJ, Murk AJ (2007) A synchronized amphibian metamorphosis assay as an improved tool to detect thyroid hormone disturbance by endocrine disruptors and apolar sediment extracts. Chemosphere 70:93–100

    Article  CAS  Google Scholar 

  • Hamer B, Bihari N, Reifferscheid G, Zahn RF, Müller WEG, Betet R (2000) Evaluation of the SOS/umu-test post-treatment assay for the detection of genotoxic activities of pure compounds and complex environmental mixtures. Mutat Res 466:161–171

    Article  CAS  Google Scholar 

  • Hecker M, Hollert H (2009) Effect-directed analysis (EDA) in aquatic ecotoxicology: state of the art and future challenges. Environ Sci Pollut Res 16:607–613

    Article  Google Scholar 

  • Hu WP, Zhai SJ, Zhu Z, Han HJ (2008) Impacts of the Yangtze River water transfer on the restoration of Lake Taihu. Ecol Eng 34:30–49

    Article  CAS  Google Scholar 

  • Jiang WW, Yan Y, Ma M, Wang DH, Luo Q, Wang ZJ, Satyanarayanan SK (2012) Assessment of source water contamination by estrogenic disrupting compounds in China. J Environ Sci 24:320–328

    Article  CAS  Google Scholar 

  • Jin XL, Jiang GB, Huang GL, Liu JF, Zhou QF (2004) Determination of 4-tert-octylphenol, 4-nonylphenol and bisphenol A in surface waters from the Haihe River in Tianjin by gas chromatography–mass spectrometry with selected ion monitoring. Chemosphere 56:1113–1119

    Article  CAS  Google Scholar 

  • Jugan ML, Oziol L, Bimbot M, Huteau V, Tamisier-karolak S, Blondeau JP, Lévi Y (2009) In vitro assessment of thyroid and estrogenic endocrine disruptors in wastewater treatment plants, rivers and drinking water supplies in the greater Paris area (France). Sci Total Environ 407:3579–3587

    Article  CAS  Google Scholar 

  • Koh CH, Khim JS (2005) Instrumental and bioanalytical measures of dioxin-like and estrogenic compounds and activities associated with sediment from the Korean coast. Ecotox Environ Safe 61:366–379

    Article  CAS  Google Scholar 

  • Kosmehl T, Krebs F, Manz W, Erdinger L, Braunbeck T, Hollert H (2004) Comparative genotoxicity testing of Rhine river sediment extracts using the permanent cell lines RTG-2 and RTW-W1 in the comet assay and Ames assay. J Soils Sediments 4:84–94

    Article  CAS  Google Scholar 

  • Legler J, Dennekamp M, Vethaak AD, Brouwer A, Koeman JH, van der Burg B, Murk AJ (2002) Detection of estrogenic activity in sediment-associated compounds using in vitro reporter gene assays. Sci Total Environ 293:69–83

    Article  CAS  Google Scholar 

  • Lei BL, Kang J, Wang XT, Yu YX, Zhang XL, Wen Y, Wang YP (2014) The levels of PAHs and aryl hydrocarbon receptor effects in sediments of Taihu Lake, China. Environ Sci Pollut Res 21:6547–6557

    Article  CAS  Google Scholar 

  • Li J, Li N, Ma M, Giesy JP, Wang ZJ (2008a) In vitro profiling of the endocrine disrupting potency of organochlorine pesticides. Toxicol Lett 183:65–71

    CAS  Google Scholar 

  • Li J, Ma M, Wang ZJ (2008b) A two-hybrid yeast assay to quantify the effects of xenobiotics on thyroid hormone-mediated gene expression. Environ Toxicol Chem 27:159–167

    Article  CAS  Google Scholar 

  • Li J, Ma M, Wang ZJ (2010a) In vitro profiling of endocrine disrupting effects of phenols. Toxicol in Vitro 24:201–207

    Article  CAS  Google Scholar 

  • Li N, Wang DH, Zhou YQ, Ma M, Li J, Wang ZJ (2010b) Dibutyl phthalate contributes to the thyroid receptor antagonistic activity in drinking water processes. Environ Sci Technol 44:6863–6868

    Article  CAS  Google Scholar 

  • Li N, Ma M, Rao KF, Wang ZJ (2011) In vitro thyroid disrupting effects of organic extracts from WWTPs in Beijing. J Environ Sci 23:671–675

    Article  CAS  Google Scholar 

  • Liu GQ, Zhang G, Jin ZD, Li J (2009) Sedimentary record of hydrophobic organic compounds in relation to regional economic development: a study of Taihu Lake, East China. Environ Pollut 157:2994–3000

    Article  CAS  Google Scholar 

  • Louiz I, Kinani S, Gouze ME, Ben-Attia M, Menif D, Bouchonnet S, Porcher JM, Ben-Hassine OK (2008) Monitoring of dioxin-like, estrogenic and anti-androgenic activities in sediments of the Bizerta lagoon (Tunisia) by means of in vitro cell-based bioassays: contribution of low concentrations of polynuclear aromatic hydrocarbons (PAHs). Sci Total Environ 402:318–329

    Article  CAS  Google Scholar 

  • Lu GH, Yan ZH, Wang YH, Chen W (2011) Assessment of estrogenic contamination and biological effects in Lake Taihu. Ecotoxicology 20:974–981

    Article  CAS  Google Scholar 

  • Luo JP, Ma M, Zha JM, Wang ZJ (2009) Characterization of aryl hydrocarbon receptor agonists in sediments of Wenyu River, Beijing. China Water Res 43:2441–2448

    Article  CAS  Google Scholar 

  • Luo JP, Lei BL, Ma M, Zha JM, Wang ZJ (2011) Identification of estrogen receptor agonists in sediments from Wenyu River, Beijing. China Water Res 45:3908–3914

    Article  CAS  Google Scholar 

  • Madikizela B, Ndhlala AR, Finnie JF, Van Staden J (2014) Antimycobacterial, anti-inflammatory and genotoxicity evaluation of plants used for the treatment of tuberculosis and related symptoms in South Africa. J Ethnopharmacol 153:286–391

    Google Scholar 

  • Maletz S, Floehr T, Beier S, Klümper C, Brouwer A, Behnisch P, Higley E, Giesy JP, Hecker M, Gebhardt W, Linnemann V, Pinnekamp J, Hollert H (2013) In vitro characterization of the effectiveness of enhanced sewage treatment processes to eliminate endocrine activity of hospital effluents. Water Res 47:1545–1557

    Article  CAS  Google Scholar 

  • Mamindy-Pajany Y, Hamer B, Roméo M, Géret F, Galgani F, Durmiši E, Hurel C, Marmier N (2011) The toxicity of composted sediments from Mediterranean ports evaluated by several bioassays. Chemosphere 82:362–369

    Article  CAS  Google Scholar 

  • Mehler WT, Li HZ, Pang JX, Sun BQ, Lydy MJ, You J (2011) Bioavailability of hydrophobic organic contaminants in sediment with different particle-size distributions. Arch Environ Contam Toxicol 61:74–82

    Article  CAS  Google Scholar 

  • Murata T, Yamauchi K (2008) 3,3′,5-Triodo-L-thyronine-like activity in effluents from domestic sewage treatment plants detected by in vitro and in vivo bioassays. Toxicol Appl Pharmacol 226:309–317

    Article  CAS  Google Scholar 

  • Nash JP, Kime DE, Van der Ven LT, Wester PW, Brion F, Maack G, Stahlschmidt-Allner P, Tyler CR (2004) Long-term exposure to environmental concentrations of the pharmaceutical ethynylestradiol causes reproductive failure in fish. Environ Health Perspect 112:1725–1733

    Article  CAS  Google Scholar 

  • Power DM, Llewellyn L, Faustino M, Nowell MA, Björnsson BT, Einarsdottir IE, Canario AVM, Sweeney GE (2001) Thyroid hormones in growth and development of fish. Comp Bichem Physiol Part C 130:447–459

    CAS  Google Scholar 

  • Qiao M, Chen YY, Zhang QH, Huang SB, Ma M, Wang CX, Wang ZJ (2006) Identification of Ah receptor agonists in sediment of Meiliang Bay, Taihu Lake. China Environ Sci Technol 40:1415–1419

    Article  CAS  Google Scholar 

  • Rajoria S, Suriano R, George AL, Shanmugam A, Jussim C, Shin EJ, Moscatello A, Geliebter J, Carpi A, Tiwari RK (2012) Estrogen activity as a preventive and therapeutic target in thyroid cancer. Biomed Pharmacother 66:151–158

    Article  CAS  Google Scholar 

  • Roach PS, Luvizotto GL, Kosmehl T, Böttcher M, Storch V, Braunbeck T, Hollert H (2009) Sediment genotoxicity in the Tietê River (Sǎo Paulo, Brazil): in vitro comet assay versus in situ micronucleus assay studies. Ecotoxicol Environ Saf 72:1842–1848

    Article  Google Scholar 

  • Rocha PS, Azab E, Schmidt B, Storch V, Hollert H, Braunbeck T (2010) Changes in toxicity and dioxin-like activity of sediments from the Tietê River (Sǎo Paulo, Brazil). Ecotoxicol Environ Saf 73:550–558

    Article  Google Scholar 

  • Schmitt S, Reifferschedi G, Claus E, Schlüsener M (2012) Effect directed analysis and mixture effects of estrogenic compounds in a sediment of the river Elbe. Environ Sci Pollut Res 19:3350–3361

    Article  CAS  Google Scholar 

  • Shen C, Huang S, Wang Z, Qiao M, Tang X, Yu C, Shi D, Zhu Y, Shi J, Chen X, Setty K, Chen Y (2008) Identification of Ah receptor agonists in soil of e-waste recycling sites from Taizhou area in China. Environ Sci Technol 42:49–55

    Article  CAS  Google Scholar 

  • Shi W, Wang XY, Hu GJ, Hao YQ, Zhang XW, Liu HL, Wei S, Wang XR, Yu HX (2011) Bioanalytical and instrumental analysis of thyroid hormone disrupting compounds in water sources along the Yangtze River. Environ Pollut 159:441–448

    Article  CAS  Google Scholar 

  • Song M, Jiang Q, Xu Y, Liu H, Lam PKS, O’Toole D, Zhang Q, Giesy J, Jiang G (2006a) AhR-active compounds in sediments of the Haihe and Dagu Rivers, China. Chemosphere 63:1222–1230

    Article  CAS  Google Scholar 

  • Song M, Xu Y, Jiang Q, Lam PKS, O’Toole DK, Giesy JP, Jiang GB (2006b) Measurement of estrogenic activity in sediments from Haihe and Dagu River China. Environ Int 32:676–681

    Article  Google Scholar 

  • Sota AM, Justicia H, Wary JW (1991) P-nonyl-phenol: an estrogenic xenobiotic released from “modified” polystyrene. Environ Health Perspect 92:167–173

    Article  Google Scholar 

  • Spink DC, Eugster HP, Lincoln DW (1992) 17β-Estradiol hydroxylation catalyzed by human cytochrome P4501A1: a comparison of the activities induced by 2,3,7,8-tetrachlorodibenze-p-dioxin in MCF-7 cells with those from heterologous expression of the cDNA. Arch Biochem Biophys 293:248–342

    Article  Google Scholar 

  • Terasaki M, Kosaka K, Kunikane S, Makino M, Shiraishi F (2011) Assessment of thyroid hormone activity of halogenated bisphenol A using a yeast two-hybrid assay. Chemosphere 84:1527–1530

    Article  CAS  Google Scholar 

  • Ternes T, Stumpf M, Mueller J, Haberer K, Wiken R, Servos M (1999) Behavior and occurrence of estrogens in municipal sewage treatment plants I. Investig Sci Total Environ 225:81–90

    Article  CAS  Google Scholar 

  • Tillitt DE, Giesy J (1991) Characterization of the H4IIE rat hepatoma cell bioassay as a tool for assessing toxic potency of planar halogenated hydrocarbons in environmental samples. Environ Sci Technol 25:87–92

    Article  CAS  Google Scholar 

  • Van Lipzig MMH, Vermeulen NPE, Gusinu R, Legler J, Frank H, Seidel A, Meerman JHN (2005) Formation of estrogenic metabolites of benzo[a]pyrene and chrysene by cytochrome P450 activity and their combined and supra-maximal estrogenic activity. Environ Toxicol Pharmacol 19:41–45

    Article  Google Scholar 

  • Wang ZQ, Zhang YZ, Zhang Y, Wang SR, Wu P, Huang JF (2012) Spatial distribution and risk assessment of typical EDCs in Yili River of Taihu Basin. Res Environ Sci (In Chinese) 25:1351–1358

    CAS  Google Scholar 

  • Xiao RY, Wang ZJ, Wang CX, Yu G (2006) Soil screening for identifying ecological risk stressors using a battery of in vitro cell bioassays. Chemosphere 64:71–78

    Article  CAS  Google Scholar 

  • Xu J, Zhang Y, Guo CS, He Y, Li L, Meng W (2013) Levels and distribution of tetrabromobisphenol A and hexabromocyclododecane in Taihu Lake China. Environ Toxicol Chem 32:2249–2255

    Article  CAS  Google Scholar 

  • Yoo H, Khim J, Giesy J (2006) Receptor-mediated in vitro bioassay for characterization of Ah-R-active compounds and activities in sediment from Korea. Chemosphere 62:1261–1271

    Article  CAS  Google Scholar 

  • Zha J, Sun L, Zhou Y, Spear P, Ma M, Wang Z (2008) Assessment of 17a-ethinylestradiol effects and underlying mechanisms in a continuous, multigeneration exposure of the Chinese rare minnow (Gobiocypris rarus). Toxicol Appl Pharm 226:298–308

    Article  CAS  Google Scholar 

  • Zhang HJ, Hu WP, Gu K, Li QQ, Zheng DL, Zhai SH (2013) An improved ecological model and software for short-term algal bloom forecasting. Environ Modell Softw 48:152–162

    Article  Google Scholar 

  • Zhao ZH, Zhang L, Wu JL, Fan CX (2013) Residual levels, tissue distribution and risk assessment of organochlorine pesticides (OCPs) in edible fishes from Taihu Lake China. Environ Monit Assess 185:9265–9277

    Article  CAS  Google Scholar 

  • Zhou L, Li HR, Yu ZQ, Ren M, Zeng XY, Peng PA, Sheng GY, Fu JM (2012) Chlorinated and brominated dibenzo-p-dioxins and dibenzofurans in surface sediment from Taihu Lake China. J Environ Monit 14:1935–1942

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by the National Key Basic Research Development Program (Grant No. 2008CB418205), Program for Changjiang Scholars and Innovative Research Team in University (Grant No. IRT13078), and the Outstanding Young Teacher Research and Special Projects (Grant No. shu10040). We thank Professor Wang Zijian from the State Key Laboratory of Environmental Aquatic Chemistry, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, for his technical assistance during the experiments.

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  1. Institute of Environmental Pollution and Health, College of Environmental and Chemical Engineering, Shanghai University, Shanghai, 200444, China

    Bingli Lei, Jia Kang, Xuetong Wang, Qian Liu & Jiamo Fu

  2. State Key Laboratory of Organic Geochemistry, Guangdong Key Laboratory of Environment and Resources, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou, 510640, China

    Zhiqiang Yu, Xiangying Zeng & Jiamo Fu

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  1. Bingli Lei
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  2. Jia Kang
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Correspondence to Zhiqiang Yu.

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Lei, B., Kang, J., Wang, X. et al. The toxicity of sediments from Taihu Lake evaluated by several in vitro bioassays. Environ Sci Pollut Res 22, 3419–3430 (2015). https://doi.org/10.1007/s11356-014-3640-y

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