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Toxicity evaluation of 4,4′-di-CDPS and 4,4′-di-CDE on green algae Scenedesmus obliquus: growth inhibition, change in pigment content, and oxidative stress

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Abstract

Polychlorinated diphenyl sulfides and polychlorinated diphenyl ethers are two types of dioxin-like pollutants, which are prevalent in aquatic environments. However, to date, limited information is available regarding their toxicity to green algae. In this study, growth inhibition, effect on pigment content, and oxidative stress potentials of 4,4′-di-CDPS and 4,4′-di-CDE on green algae Scenedesmus obliquus were investigated. The results indicate that the EC50 values of 4,4′-di-CDPS after 24, 48, 72, and 96 h of exposure were 1.736, 1.172, 0.994, and 0.820 mg/L, while the corresponding values for 4,4′-di-CDE were 0.697, 1.087, 0.833, and 0.327 mg/L. As compared to the control group, most of the measured pigment content in algal cells significantly decreased after 96-h exposure to these two chemicals, suggesting their suppressive capability on the photosynthesis process in algal cells. Additionally, oxidative stress occurred as demonstrated by the significantly inhibited activities of the antioxidant enzymes (total superoxide dismutase (T-SOD), catalase (CAT), and glutathione peroxidase (GPx)), and high increases in malondialdehyde (MDA) content in all 4,4′-di-CDE-treated groups and some moderate-dose and high-dose treatments with 4,4′-di-CDPS. Acute toxicity tests and biochemical analysis showed that 4,4′-di-CDE was more toxic than 4,4′-di-CDPS on S. obliquus.

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References

  • Almeida AC, Gomes T, Langford K, Thomas KV, Tollefsen KE (2017) Oxidative stress in the algae Chlamydomonas reinhardtii exposed to biocides. Aquat Toxicol 189:50–59

    Article  CAS  Google Scholar 

  • Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynthetica 51:163–190

    Article  CAS  Google Scholar 

  • Ballesteros ML, Wunderlin DA, Bistoni MA (2009) Oxidative stress responses in different organs of Jenynsia multidentata exposed to endosulfan. Ecotoxicol Environ Saf 72:199–205

    Article  CAS  Google Scholar 

  • Banudevi S, Krishnamoorthy G, Venkataraman P, Vignesh C, Aruldhas MM, Arunakaran J (2006) Role of α-tocopherol on antioxidant status in liver, lung and kidney of PCB exposed male albino rats. Food Chem Toxicol 44:2040–2046

    Article  CAS  Google Scholar 

  • Becker M, Phillips T, Safe S (1991) Polychlorinated diphenyl ethers: a review. Toxicol Environ Chem 33:189–200

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Cao DJ, Shi XD, Li H, Xie PP, Zhang HM, Deng JW, Liang YG (2015) Effects of lead on tolerance, bioaccumulation, and antioxidative defense system of green algae, Cladophora. Ecotoxicol Environ Saf 112:231–237

    Article  CAS  Google Scholar 

  • Calabrese EJ, Blain RB (2009) Hormesis and plant biology. Environ Pollut 157:42–48

    Article  CAS  Google Scholar 

  • Chen H, Zou YQ, Zhang LJ, Wen YZ, Liu WP (2014) Enantioselective toxicities of chiral ionic liquids 1-alkyl-3-methylimidazolium lactate to aquatic algae. Aquat Toxicol 154:114–120

    Article  CAS  Google Scholar 

  • Chen HL, Hsu CH, Hung DZ, Hu ML (2006) Lipid peroxidation and antioxidant status in workers exposed to PCDD/Fs of metal recovery plants. Sci Total Environ 372:12–19

    Article  CAS  Google Scholar 

  • Cheng C, Huang LD, Ma R, Zhou ZQ, Diao JL (2015) Enantioselective toxicity of lactofen and its metabolites in Scenedesmus obliquus. Algal Res 10:72–79

    Article  Google Scholar 

  • De NE, Meriç S, Gallo M, Iaccarino M, Della CR, Lofrano G, Russo T, Pagano G (2007) Vegetable and synthetic tannins induce hormesis/toxicity in sea urchin early development and in algal growth. Environ Pollu 146:46–54

    Article  CAS  Google Scholar 

  • Domingo JL (2006) Polychlorinated diphenyl ethers (PCDEs): environmental levels, toxicity and human exposure. Environ Inter 32:121–127

    Article  CAS  Google Scholar 

  • Domingo JL, Bocio A, Falcoa G, Llobet JM (2006) Exposure to PBDEs and PCDEs associated with the consumption of edible marine species. Environ Sci Technol 40:4394–4399

    Article  CAS  Google Scholar 

  • Feng MB, Qu RJ, Wang C, Wang LS, Wang ZY (2013) Comparative antioxidant status in freshwater fish Carassius auratus exposed to six current-use brominated flame retardants: a combined experimental and theoretical study. Aquat Toxicol 140–141:314–323

    Article  CAS  Google Scholar 

  • Geoffroy L, Dewez D, Vernet G, Popovic R (2003) Oxyfluorfen toxic effect on S. obliquus evaluated by different photosynthetic and enzymatic biomarkers. Arch Environ Contam Toxicol 45:445–452

    Article  CAS  Google Scholar 

  • Hermes-Lima M (2004) Oxygen in biology and biochemistry: role of free radicals. John Wiley & Sons, Inc

  • Huang LD, Lu DH, Diao JL, Zhou ZQ (2012a) Enantioselective toxic effects and biodegradation of benalaxyl in Scenedesmus obliquus. Chemosphere 87:7–11

    Article  CAS  Google Scholar 

  • Huang LD, Lu DH, Zhang P, Diao JL, Zhou ZQ (2012b) Enantioselective toxic effects of hexaconazole enantiomers against in Scenedesmus obliquus. Chirality 24:610–614

    Article  CAS  Google Scholar 

  • Iverson F, Newsome H, Hierlihy L (1987) Induction of rat hepatic monooxygenase activity by polychlorinated diphenyl ethers. Food Chem Toxicol 25:305–307

    Article  CAS  Google Scholar 

  • Ivo PN, Lyaquatali AD (2002) HPLC analysis of 4-chlorophenyl methyl sulphide and diphenyl sulphide and their corresponding sulphoxides and sulphones in rat liver microsomes. J Pharm Biomed Anal 27:315–325

    Article  Google Scholar 

  • Jarafi M (2007) Dose- and time-dependent effects of sulfur mustard on antioxidant system in liver and brain of rat. Toxicology 231:30–39

    Article  CAS  Google Scholar 

  • Kirkman MN, Gaetani GF (1984) Catalase: a tetrameric enzyme with four tightly bound molecules of NADPH. Proc Natl Acad Sci U S A 81:4343–4347

    Article  CAS  Google Scholar 

  • Klaunig JE, Wang ZM, Pu XZ, Zhou SY (2011) Oxidative stress and oxidative damage in chemical carcinogenesis. Toxicol Appl Pharmacol 254:86–99

    Article  CAS  Google Scholar 

  • Kováčik J, Bořivoj K, Babula P (2014) Oxidative stress, uptake and bioconversion of 5-fluorouracil in algae. Chemosphere 100:116–123

    Article  CAS  Google Scholar 

  • Kruz J, Ballschmiter K (1995) Isomer specific determination of 79 polychlorinated diphenyl ethers (PCDE) in cod liver oil, chlorophenols and a fly ash. Fresenius J Anal Chem 351:98–109

    Article  Google Scholar 

  • Kurz J, Ballschmiter K (1999) Vapour pressures, aqueous solubilities, Henry’s law constants, partition coefficients between gas/water (K gw), n-octanol/water (K ow) and gas/n-octanol (K go) of 106 polychlorinated diphenyl ethers (PCDE). Chemosphere 38:573–586

    Article  CAS  Google Scholar 

  • Li CG, Qin L, Qu RJ, Sun P, Wang ZY (2016) Responses of antioxidant defense system to polyfluorinated dibenzo-p-dioxins (PFDDs) exposure in liver of freshwater fish Carassius auratus. Ecotox Environ Saf 126:170–176

    Article  CAS  Google Scholar 

  • Li X, Ping X, Xiumei S, Zhenbin W, Liqiang X (2005) Toxicity of cypermethrin on growth, pigments, and superoxide dismutase of Scenedesmus obliquus. Ecotox Environ Saf 60:188–192

    Article  CAS  Google Scholar 

  • Li Y, Li M, Shi JQ, Wang ZY (2012) Hepatic antioxidative responses to PCDPSs and estimated short-term biotoxicity in freshwater fish. Aquat Toxicol 120–121:90–98

    Article  CAS  Google Scholar 

  • Liu H, Zhang X, Dong Y, Chen C, Zhu S, Ma X (2015a) Enantioselective toxicities of chiral ionic liquids 1-alkyl-3-methyl imidazolium tartrate on Scenedesmus obliquus. Aquat Toxicol 169:179–187

    Article  CAS  Google Scholar 

  • Liu HJ, Xia YL, Cai WD, Zhang YN, Zhang XQ, Du ST (2017a) Enantioselective oxidative stress and oxidative damage caused by Rac- and S-metolachlor to Scenedesmus obliquus. Chemosphere 173:22–30

    Article  CAS  Google Scholar 

  • Liu HJ, Xiong MY (2009) Comparative toxicity of racemic metolachlor and Smetolachlor to Chlorella pyrenoidosa. Aquat Toxicol 93:100–106

    Article  CAS  Google Scholar 

  • Liu HJ, Zhang XQ, Chen CD, Du ST, Dong Y (2015b) Effects of imidazolium chloride ionic liquids and their toxicity to Scenedesmus obliquus. Ecotoxicol Environ Saf 122:83–90

    Article  CAS  Google Scholar 

  • Liu W, Li J, Gao L, Zhang Z, Zhao J, He X, Zhang X (2017b) Bioaccumulation and effects of novel chlorinated polyfluorinated ether sulfonate in freshwater alga Scenedesmus obliquus. Environ Pollut 233:8–15

    Article  CAS  Google Scholar 

  • Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30

    Article  CAS  Google Scholar 

  • Mandal S, Mallick N (2012) Biodiesel production by the green microalga Scenedesmus obliquus in a recirculatory aquaculture system. Appl Environ Microbiol 78:5929–5934

    Article  CAS  Google Scholar 

  • Mofeed J, Mosleh YY (2013) Toxic responses and antioxidative enzymes activity of Scenedesmus obliquus exposed to fenhexamid and atrazine, alone and in mixture. Ecotox Environ Safe 95:234–240

    Article  CAS  Google Scholar 

  • Naito Y, Akaboshi F, Goto T, Sugyama N, Ono S, Fukaya T, Kuwabara E, Kajii M, Nishimura H, Sugiura M (1995) Diphenyl sulfides, sulfoxides, and sulfones for prevention and treatment of eosinophil-related diseases. 21 JP 07048251 A

  • Nilsson CA, Renburg L (1974) Further studies on impurities in chlorophenols. J Chromatograph A 89:325–333

    Article  CAS  Google Scholar 

  • OECD (2011) Organization for Economic Cooperation and Development guidelines for testing of chemicals: freshwater alga and cyanobacteria. Growth Inhibition Tests, Paris

    Google Scholar 

  • Pandey S, Parvez S, Sayeed I, Haque R, Bin-Hafeez B, Raisuddin S (2003) Biomarkers of oxidative stress: a comparative study of river Yamuna fish Wallago attu (Bl & Schn). Sci Total Environ 309:105–115

    Article  CAS  Google Scholar 

  • Qin L, Liu F, Liu H, Wei ZB, Sun P, Wang ZY (2014) Evaluation of HODE-15, FDE-15, CDE-15, and BDE-15 toxicity on adult and embryonic zebrafish (Danio rerio). Environ Sci Pollut Res 21:14047–14057

    Article  CAS  Google Scholar 

  • Qin L, Feng MB, Zhang XS, Wang LS, Wang ZY (2015) Occurrence of polychlorinated diphenyl ethers in Nanjing section of the Yangtze River: level and distribution pattern. Environ Sci Pollut Res 22:9924–9232

    Google Scholar 

  • Ritchie RJ (2008) Universal chlorophyll equations for estimating chlorophylls a, b, c, and d and total chlorophylls in natural assemblages of photosynthetic organisms using acetone, methanol, or ethanol solvents. Photosynthetica 46:115–126

    Article  CAS  Google Scholar 

  • Rosiaka KL, Seo BW, Chu I, Francis BM (1997) Effects of maternal exposure to chlorinated diphenyl ethers on thyroid hormone concentrations in maternal and juvenile rats. J Environ Sci Health Part B 32:377–393

    Article  Google Scholar 

  • Schwarzbauer J, Littke R, Weigelt V (2000) Identification of specific organic contaminants for estimating the contribution of the Elbe River to the pollution of the German Bight. Org Geochem 31:1713–1731

    Article  CAS  Google Scholar 

  • Shi JQ, Feng MB, Zhang XS, Wei ZB, Wang ZY (2013) Acute oral toxicity and liver oxidant/antioxidant stress of halogenated benzene, phenol, and diphenyl ether in mice: a comparative and mechanism exploration. Environ Sci Pollut Res 20:6138–6149

    Article  CAS  Google Scholar 

  • Shi JQ, Zhang XS, Qu RQ, Xu Y, Wang ZY (2012) Synthesis and QSPR study on environment-related properties of polychlorinated diphenyl sulfides (PCDPSs). Chemosphere 88:844–854

    Article  CAS  Google Scholar 

  • Sinkkonen S (1993) Environmental analysis of chlorinated aromatic thioethers, sulphoxides and sulphones. J Chromatogr A 642:47–52

    Article  CAS  Google Scholar 

  • Sinkkonen S, Vattulainen A, Aittola JP, Paasivirta J, Lahtiperä M (1993) Polychlorinated dibenzothiophenes, thianthrenes and diphenylsulfides formed in metal reclamation. Organohalogen Compd 11:195–198

    CAS  Google Scholar 

  • Tripathi BN, Mehta SK, Amar A, Gaur JP (2006) Oxidative stress in Scenedesmus sp. during short- and long-term exposure to Cu2+ and Zn2+. Chemosphere 62:538–544

    Article  CAS  Google Scholar 

  • Uner N, Oruc E, Sevgiler Y (2005) Oxidative stress-related and ATPase effects of etoxazole in different tissues of Oreochromisniloticus. Environ Toxicol Pharmacol 20:99–106

    Article  CAS  Google Scholar 

  • Xiong L, Xie P, Sheng XM, Wu ZB, Xie LQ (2005) Toxicity of cypermethrin on growth, pigments, and superoxide dismutase of Scenedesmus obliquus. Ecotox Environ Safe 60:188–192

    Article  CAS  Google Scholar 

  • Yang F, Qu RJ, Wang M, Tang YQ, Feng MB, Wang ZY (2013) Experimental and QSPR study of sorption properties of polychlorinated diphenyl sulfides (PCDPSs) in Yangtze River plain soil. Geoderma 193-194:140–148

    Article  CAS  Google Scholar 

  • Zeng XL, Wang ZY, Ge ZG, Liu HX (2007) Quantitative structure-property relationships for predicting subcooled liquid vapor pressure (P L) of 209 polychlorinated diphenyl ethers (PCDEs) by DFT and the position of cl substitution (PCS) methods. Atmos Environ 41:3590–3603

    Article  CAS  Google Scholar 

  • Zeng XL, Zhang XS, Qin L, Wang ZY (2015) Tissue distribution, excretion, and metabolism of 2,2′,4,4′,5-penta-chlorinated diphenylsulfide (CDPS-99) in ICR mice. J Chromatogr B 1001:90–97

    Article  CAS  Google Scholar 

  • Zhang XS, Liu F, Chen BY, Li Y, Wang ZY (2012) Acute and subacute oral toxicity of polychlorinated diphenyl sulfides in mice: determining LD50 and assessing the status of hepatic oxidative stress. Environ Toxicol Chem 31:1485−1493

    Google Scholar 

  • Zhang XS, Liu F, Wei ZB, Wang ZY (2013) Synthesis of diaryl ethers by CuI-catalyed C-O bond formation via Ullman coupling: assessing the reactivity of aryl halides. Lett Org Chem 10:31–36

    CAS  Google Scholar 

  • Zhang XS, Qin L, Qu RJ, Feng MB, Wei ZB, Wang LS, Wang ZY (2014a) Occurrence of polychlorinated diphenyl sulfides (PCDPSs) in surface sediments and surface water from the Nanjing section of the Yangtze River. Environ Sci Technol 48:11429–11436

    Article  CAS  Google Scholar 

  • Zhang XS, Feng MB, Liu F, Qin L, Qu RJ, Li DL, Wang ZY (2014b) Subacute oral toxicity of BDE-15, CDE-15, and HODE-15 in ICR male mice: assessing effects on hepatic oxidative stress and metals status and ascertaining the protective role of vitamin E. Environ Sci Pollut Res 21:1924–1935

    Article  CAS  Google Scholar 

  • Zhang R, Zhang XW, Zhang JJ, Qu RJ, Zhang JM, Liu X, Chen J, Wang ZY, Yu HX (2014c) Interaction with AHR1 receptor and avian inter-species sensitivity variation by polychlorinated diphenylsulfides. Environ Sci Technol 48:10948–10956

    Article  CAS  Google Scholar 

  • Zhang XS, Qin L, Li DL, Wei ZB, Wang ZY (2014d) Hepatic oxidative status and metal homeostasis disturbance of 2-hydroxylated dioxin in ICR mice. Environ Toxicol Phar 38:881–890

    Article  CAS  Google Scholar 

  • Zhao FF, Xiang QQ, Zhou Y, Xu X, Qiu XY, Yu Y, Ahmad F (2017a) Evaluation of the toxicity of herbicide topramezone to Chlorella vulgaris: oxidative stress, cell morphology and photosynthetic activity. Ecotoxicol Environ Safe 143:129–135

    Article  CAS  Google Scholar 

  • Zhao Y, Wang Y, Li Y, Santschi PH, Quigg A (2017b) Response of photosynthesis and the antioxidant defense system of two microalgal species (Alexandrium minutum and Dunaliella salina) to the toxicity of BDE-47. Mar Pollut Bull 124:459–469

    Article  CAS  Google Scholar 

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Acknowledgments

This research was financially supported by the National Natural Science Foundation of China (No. 21607001), the Anhui Provincial Natural Science Foundation (No. 1608085QB45), and the Science Research Project of Anhui Education Department (No. KJ2015A090).

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Correspondence to Xuesheng Zhang.

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Responsible editor: Cinta Porte

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Fang, B., Shi, J., Qin, L. et al. Toxicity evaluation of 4,4′-di-CDPS and 4,4′-di-CDE on green algae Scenedesmus obliquus: growth inhibition, change in pigment content, and oxidative stress. Environ Sci Pollut Res 25, 15630–15640 (2018). https://doi.org/10.1007/s11356-018-1749-0

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