Skip to main content

Advertisement

SpringerLink
Log in

Multi-biomarker responses in green mussels exposed to PFCs: effects at molecular, cellular, and physiological levels

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Perfluorinated chemicals (PFCs) are extremely persistent and have been found extensively in the environment and wildlife. Oceans are the final sink for many persistent organic pollutants (POPs) including PFCs. However, to date, there has been a lack of studies that investigated the environmental consequences of PFCs on marine organisms. To fill in this gap, environmental toxicity of two dominant PFCs, perfluorooctane sulfonate (PFOS) and perfluorooctanoate (PFOA), was examined in a sentinel species, green mussel Perna viridis, using a series of biomarkers corresponding to different biological levels (molecular, cellular, and physiological). Correlations among these biomarkers were also investigated. The results showed that the tested compounds can induce a series adverse effect at different biological levels, including oxidative stress, DNA damage, membrane instability, suppressed filtration rate, and reduced body weight. Correlation analysis revealed that excess production of reactive oxygen species could be the major toxic pathway. An indirect mode of toxic action was also explored where adverse impacts could be secondary effects of PFC exposure. The joint analysis of biomarkers from multiple biological levels resulted in a comprehensive understanding of how PFC exposure can influence the health of organisms. The correlations of these biomarkers also provided a new perspective of the ecological consequences of PFCs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Al-Subiai SN, Moody AJ, Mustafa SA, Jha AN (2011) A multiple biomarker approach to investigate the effects of copper on the marine bivalve mollusc, Mytilus edulis. Ecotoxicol Environ Saf 74:1913–1920

    Article  CAS  Google Scholar 

  • Arukwe A, Mortensen AS (2011) Lipid peroxidation and oxidative stress responses of salmon fed a diet containing perfluorooctane sulfonic- or perfluorooctane carboxylic acids. Comp Biochem Physiol C Toxicol Pharmacol 154:288–295

    Article  CAS  Google Scholar 

  • Austin ME, Kasturi BS, Barber M, Kannan K, MohanKumar PS, MohanKumar SMJ (2003) Neuroendocrine effects of perflurooactane sulfonate in rats. Environ Health Perspect 111:1485–1489

    Article  CAS  Google Scholar 

  • Berthiaume J, Wallace KB (2002) Perfluorooctanoate, perflourooctanesulfonate, and N-ethyl perfluorooctanesulfonamido ethanol; peroxisome proliferation and mitochondrial biogenesis. Toxicol Lett 129:23–32

    Article  CAS  Google Scholar 

  • Binelli A, Parolini M, Cogni D, Pedriali A, Provini A (2009) A multi-biomarker assessment of the impact of the antibacterial trimethoprim on the non-target organism Zebra mussel (Dreissena polymorpha). Comp Biochem Physiol C Toxicol Pharmacol 150:329–336

    Article  CAS  Google Scholar 

  • Bradbury A (2005) Length-weight models for intertidal clams in Puget Sound: (Bivalve Regions 1, 5, 6, 7, and 8). Washington, Dept. of Fish and Wildlife, Fish Program, Fish Management Division

  • Brooks S, Lyons B, Goodsir F, Bignell J, Thain J (2009) Biomarker responses in mussels, an integrated approach to biological effects measurements. J Toxicol Environ Health Part A Curr Issues 72:196–208

    Article  CAS  Google Scholar 

  • Cai M, Zhao Z, Yin Z, Ahrens L, Huang P, Yang H, He J, Sturm R, Ebinghaus R, Xie Z (2012) Occurrence of perfluoroalkyl compounds in surface waters from the North Pacific to the Arctic Ocean. Environ Sci Technol 46:661–668

    Article  CAS  Google Scholar 

  • Canty MN, Hutchinson TH, Brown RJ, Jones MB, Jha AN (2009) Linking genotoxic responses with cytotoxic and behavioural or physiological consequences: differential sensitivity of echinoderms (Asterias rubens) and marine molluscs (Mytilus edulis). Aquat Toxicol 94:68–76

    Article  CAS  Google Scholar 

  • Corsini E, Sangiovanni E, Avogadro A, Galbiati V, Viviani B, Marinovich M, Galli CL, Dell'Agli M, Germolec DR (2012) In vitro characterization of the immunotoxic potential of several perfluorinated compounds (PFCs). Toxicol Appl Pharmacol 258:248–255

    Article  CAS  Google Scholar 

  • D'Hollander W, De Voogt P, De Coen W, Bervoets L (2010) Perfluorinated substances in human food and other sources of human exposure. Rev Environ Contam Toxicol 208:179–215

    Google Scholar 

  • Dorts J, Kestemont P, Marchand PA, D'Hollander W, Thezenas ML, Raes M, Silvestre F (2011) Ecotoxicoproteomics in gills of the sentinel fish species, Cottus gobio, exposed to perfluorooctane sulfonate (PFOS). Aquat Toxicol 103:1–8

    Article  CAS  Google Scholar 

  • Fang JKH, Wu RSS, Yip CKM, Shin PKS (2009) Power analysis for biomarkers in mussels for use in coastal pollution monitoring. Mar Pollut Bull 58:1152–1158

    Article  CAS  Google Scholar 

  • Faria M, Carrasco L, Diez S, Riva MC, Bayona JM, Barata C (2009) Multi-biomarker responses in the freshwater mussel Dreissena polymorpha exposed to polychlorobiphenyls and metals. Comp Biochem Physiol C Toxicol Pharmacol 149:281–288

    Article  Google Scholar 

  • Giesy JP, Naile JE, Khim JS, Jones PD, Newsted JL (2010) Aquatic toxicology of perfluorinated chemicals. Rev Environ Contam Toxicol 202:1–52

    CAS  Google Scholar 

  • Guruge KS, Hikono H, Shimada N, Murakami K, Hasegawa J, Yeung LWY, Yamanaka N, Yamashita N (2009) Effect of perfluorooctane sulfonate (PFOS) on influenza A virus-induced mortality in female B6C3F1 mice. J Toxicol Sci 34:687–691

    Article  CAS  Google Scholar 

  • Hagenaars A, Knapen D, Meyer IJ, van der Ven K, Hoff P, De Coen W (2008) Toxicity evaluation of perfluorooctane sulfonate (PFOS) in the liver of common carp (Cyprinus carpio). Aquat Toxicol 88:155–163

    Article  CAS  Google Scholar 

  • Hagenaars A, Vergauwen L, De Coen W, Knapen D (2011) Structure-activity relationship assessment of four perfluorinated chemicals using a prolonged zebrafish early life stage test. Chemosphere 82:764–772

    Article  CAS  Google Scholar 

  • Houde M, De Silva AO, Muir DCG, Letcher RJ (2011) Monitoring of perfluorinated compounds in aquatic biota: an updated review PFCs in aquatic biota. Environ Sci Technol 45:7962–7973

    Article  CAS  Google Scholar 

  • Hu J, Yu J, Tanaka S, Fujii S (2011) Perfluorooctane sulfonate (PFOS) and perfluorooctanoic acid (PFOA) in water environment of Singapore. Water Air Soil Pollut 216:179–191

    Article  CAS  Google Scholar 

  • Hu WY, Jones PD, DeCoen W, King L, Fraker P, Newsted J, Giesy JP (2003) Alterations in cell membrane properties caused by perfluorinated compounds. Comp Biochem Physiol C Toxicol Pharmacol 135:77–88

    Article  Google Scholar 

  • Jönsson EM, Brandt I, Brunström B (2002) Gill filament-based EROD assay for monitoring waterborne dioxin-like pollutants in fish. Environ Sci Technol 36:3340–3344

    Article  Google Scholar 

  • Kennedy GL, Butenhoff JL, Olsen GW, O'Connor JC, Seacat AM, Perkins RG, Biegel LB, Murphy SR, Farrar DG (2004) The toxicology of perfluorooctanoate. Crit Rev Toxicol 34:351–384

    Article  CAS  Google Scholar 

  • Kim WK, Lee SK, Jung J (2010) Integrated assessment of biomarker responses in common carp (Cyprinus carpio) exposed to perfluorinated organic compounds. J Hazard Mater 180:395–400

    Article  CAS  Google Scholar 

  • Kleszczynski K, Skladanowski AC (2009) Mechanism of cytotoxic action of perfluorinated acids. I. Alteration in plasma membrane potential and intracellular pH level. Toxicol Appl Pharmacol 234:300–305

    Article  CAS  Google Scholar 

  • Kleszczynski K, Skladanowski AC (2011) Mechanism of cytotoxic action of perfluorinated acids. III. Disturbance in Ca(2+) homeostasis. Toxicol Appl Pharmacol 251:163–168

    Article  CAS  Google Scholar 

  • Latala A, Nedzi M, Stepnowski P (2009) Acute toxicity assessment of perfluorinated carboxylic acids towards the Baltic microalgae. Environ Toxicol Pharmacol 28:167–171

    Article  CAS  Google Scholar 

  • Lema SC, Schultz IR, ScholzN L, Incardona JP, Swanson P (2007) Neural defects and cardiac arrhythmia in fish larvae following embryonic exposure to 2,2',4,4'-tetrabromodiphenyl ether (PBDE 47). Aquat Toxicol 82:296–307

    Google Scholar 

  • Lindstrom AB, Strynar MJ, Libelo EL (2011) Polyfluorinated compounds: past, present, and future. Environ Sci Technol 45:7954–7961

    Article  CAS  Google Scholar 

  • Liu CH, Gin KYH, Chang VWC, Goh BPL, Reinhard M (2011) Novel perspectives on the bioaccumulation of PFCs—the concentration dependency. Environ Sci Technol 45:9758–9764

    Article  CAS  Google Scholar 

  • Liu CS, Yu K, Shi XJ, Wang JX, Lam PKS, Wu RSS, Zhou BS (2007) Induction of oxidative stress and apoptosis by PFOS and PFOA in primary cultured hepatocytes of freshwater tilapia (Oreochromis niloticus). Aquat Toxicol 82:135–143

    Article  CAS  Google Scholar 

  • Liu L, Liu W, Song JL, Yu HY, Jin YH, Oami K, Sato I, Saito N, Tsuda S (2009) A comparative study on oxidative damage and distributions of perfluorooctane sulfonate (PFOS) in mice at different postnatal developmental stages. J Toxicol Sci 34:245–254

    Article  CAS  Google Scholar 

  • Mulkiewicz E, Jastorff B, Skladanowski AC, Kleszczynski K, Stepnowski P (2007) Evaluation of the acute toxicity of perfluorinated carboxylic acids using eukaryotic cell lines, bacteria and enzymatic assays. Environ Toxicol Pharmacol 23:279–285

    Article  CAS  Google Scholar 

  • Newman MC (2009) Fundamentals of ecotoxicology. CRC Press, Florida

    Google Scholar 

  • Nobels I, Dardenne F, De Coen W, Blust R (2010) Application of a multiple endpoint bacterial reporter assay to evaluate toxicological relevant endpoints of perfluorinated compounds with different functional groups and varying chain length. Toxicol In Vitro 24:1768–1774

    Article  CAS  Google Scholar 

  • Oakes KD, Sibley PK, Martin JW, MacLean DD, Solomon KR, Mabury SA, Van Der Kraak GJ (2005) Short-term exposures of fish to perfluorooctane sulfonate: acute effects on fatty acyl-CoA oxidase activity, oxidative stress, and circulating sex steroids. Environ Toxicol Chem 24:1172–1181

    Article  CAS  Google Scholar 

  • Okay OS, Karacik B (2008) Bioconcentration and phototoxicity of selected PAHs to marine mussel Mytilus galloprovincialis. J Environ Sci Health Part A Toxic Hazard Subst Environ Eng 43:1234–1242

    Article  CAS  Google Scholar 

  • Parolini M, Binelli A, Cogni D, Provini A (2010) Multi-biomarker approach for the evaluation of the cyto-genotoxicity of paracetamol on the zebra mussel (Dreissena polymorpha). Chemosphere 79:489–498

    Article  CAS  Google Scholar 

  • Ramos R, Garcia E (2007) Induction of mixed-function oxygenase system and antioxidant enzymes in the coral Montastraea faveolata on acute exposure to benzo(a)pyrene. Comp Biochem Physiol C Toxicol Pharmacol 144:348–355

    Article  CAS  Google Scholar 

  • Sarkar A, Ray D, Shrivastava AN, Sarker S (2006) Molecular biomarkers: their significance and application in marine pollution monitoring. Ecotoxicology 15:333–340

    Article  CAS  Google Scholar 

  • Shipley JM, Hurst CH, Tanaka SS, DeRoos FL, Butenhoff JL, Seacat AM, Waxman DJ (2004) Trans-activation of PPARα and induction of PPARα target genes by perfluorooctane-based chemicals. Toxicol Sci 80:151–160

    Article  CAS  Google Scholar 

  • Stahl T, Mattern D, Brunn H (2011) Toxicology of perfluorinated compounds. Environ Sci Europe 23:38

    Article  Google Scholar 

  • Stevenson CN, MacManus-Spencer LA, Luckenbach T, Luthy RG, Epel D (2006) New perspectives on perfluorochemical ecotoxicology: inhibition and induction of an efflux transporter in the marine mussel, Mytilus californianus. Environ Sci Technol 40:5580–5585

    Article  CAS  Google Scholar 

  • Theobald N, Caliebe C, Gerwinski W, Hühnerfuss H, Lepom P (2011) Occurrence of perfluorinated organic acids in the North and Baltic seas. Part 1: distribution in sea water. Environ Sci Pollut Res 18:1057–1069

    Article  CAS  Google Scholar 

  • Villeneuve DL, Garcia-Reyero N (2011) Vision & strategy: predictive ecotoxicology in the 21st century. Environ Toxicol Chem SETAC 30:1–8

    Article  CAS  Google Scholar 

  • Wang T, Khim JS, Chen C, Naile JE, Lu Y, Kannan K, Park J, Luo W, Jiao W, Hu W, Giesy JP (2012) Perfluorinated compounds in surface waters from Northern China: comparison to level of industrialization. Environ Int 42:37–46

    Article  CAS  Google Scholar 

  • Watanabe MX, Jones SP, Iwata H, Kim EY, Kennedy SW (2009) Effects of co-exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin and perfluorooctane sulfonate or perfluorooctanoic acid on expression of cytochrome P450 isoforms in chicken (Gallus gallus) embryo hepatocyte cultures. Comp Biochem Physiol C Pharmacol Toxicol 149:605–612

    Google Scholar 

  • Wei YH, Shi XJ, Zhang HX, Wang JS, Zhou BS, Dai JY (2009) Combined effects of polyfluorinated and perfluorinated compounds on primary cultured hepatocytes from rare minnow (Gobiocypris rarus) using toxicogenomic analysis. Aquat Toxicol 95:27–36

    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 

  • Yang JH (2010) Perfluorooctanoic acid induces peroxisomal fatty acid oxidation and cytokine expression in the liver of male Japanese medaka (Oryzias latipes). Chemosphere 81:548–552

    Article  CAS  Google Scholar 

  • Zareitalabad P, Siemens J, Hamer M, Amelung W (2013) Perfluorooctanoic acid (PFOA) and perfluorooctanesulfonic acid (PFOS) in surface waters, sediments, soils and wastewater—a review on concentrations and distribution coefficients. Chemosphere 91:725–732

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. School of Civil & Environmental Engineering, Nanyang Technological University, 50 Nanyang Avenue, Singapore, 639798, Singapore

    Changhui Liu & Victor W. C. Chang

  2. Department of Civil & Environmental Engineering, National University of Singapore, 1 Engineering Drive, Singapore, 117576, Singapore

    Karina Y. H. Gin

Authors
  1. Changhui Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karina Y. H. Gin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Victor W. C. Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Victor W. C. Chang.

Additional information

Responsible editor: Markus Hecker

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 29 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, C., Gin, K.Y.H. & Chang, V.W.C. Multi-biomarker responses in green mussels exposed to PFCs: effects at molecular, cellular, and physiological levels. Environ Sci Pollut Res 21, 2785–2794 (2014). https://doi.org/10.1007/s11356-013-2216-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-013-2216-6

Keywords

Search

Navigation