Abstract
Mussels, Mytilus galloprovincialis, showed a high bioaccumulation ability when exposed to waterborne tetrabromodiphenyl ether (BDE-47), with a bioconcentration factor of 10,900 L Kg−1 wet weight, and slow depuration rates in clean seawater. Kinetic and concentration–response experiments were performed measuring in the exposed mussel the activities of three molecular biomarkers: glutathione S-transferase (GST), glutathione peroxidase (GPx) and acetylcholinesterase (AChE). The long term (30 days) exposure of mussels to all concentrations (2–15 µg L−1) of BDE-47 significantly inhibited the AChE and GST activities, a result that supports the suitability of these biomarkers in marine pollution monitoring programs. However, GPx activity showed a less consistent pattern of response depending on the concentration and the duration of exposure.
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Aarab N, Lemaire-Gony S, Unruh E, Hansen PD, Larsen BK, Andersen OK, Narbonne JF (2006) Preliminary study of responses in mussel (Mytilus edulis) exposed to bisphenol A, diallyl phthalate and tetrabromodiphenyl ether. Aquat Toxicol 78S:S86–S92
Akcha F, Izuel C, Venier P, Budzinski H, Burgeot T, Narbornne J-F (2000) Enzymatic biomarker measurement and study of DNA adduct formation in benzo[a]pyrene-contaminated mussels, Mytilus galloprovincialis. Aquat Toxicol 49:269–287
Alaee M, Wenning RJ (2002) The significance of brominated flame retardants in the environment: current understanding. Issues and challenges. Chemosphere. 46:579–582
Barsiene J, Syvokiene J, Bjornstad A (2006) Induction of micronuclei and other nuclear abnormalities in mussels exposed to bisphenol A, diallyl phthalate and tetrabromodiphenyl ether-47. Aquat Toxicol 78S:S105–S108
Bellas J, Albentosa M, Vidal-Liñán L, Besada V, Franco MA, Fumega J, González-Quijano A, Viñas L, Beiras R (2013) Combined use of chemical, biochemical and physiological variables in mussels for the assessment of marine pollution along the N-NW Spanish coast. Mar Environ Res. doi:10.1016/j.marenvres.2013.09.015
Bocquené G, Galgani F (1990) Characterization and assay conditions for use of AChE activity from several marine species in pollution monitoring. Mar Environ Res 30:75–89
Bocquené G, Galgani F (1998) Biological effects of contaminants: cholinesterases inhibition by organophosphate and carbamate compounds. ICES Tech Mar Environ Sci 22:1–13
Browne EP, Stapleton HM, Kelly SM, Tilton SC, Gallagher EP (2009) In vitro hepatic metabolism of 2,2′,4,4′,5-pentabromodiphenyl ether (BDE 99) in Chinook Salmon (Onchorhynchus tshawytscha). Aquat Toxicol 92:281–287
Chen L, Yu K, Huang C, Yu L, Zhu B, Lam PKS, Lam JCW, Zhou B (2012) Prenatal transfer of polybrominated diphenyl ethers (PBDEs) results in developmental neurotoxicity in zebrafish larvae. Environ Sci Technol 46:9727–9734
Christensen JH, Platz J (2001) Screening of polybrominated diphenyl ethers in blue mussels, marine and freshwater sediments in Denmark. J Environ Monit 3:543–547
Covaci A, Gheorghe A, Voorspoels S, Maervoet J, Steen Redeker E, Blust R et al. (2003) Determination of brominated flame retardants, with emphasis on polybrominated diphenyl ethers (PBDEs) in environmental and human samples—a review. Environ Int 29:735–756
De Wit CY (2002) An overview of brominated flame retardants in the environment. Chemosphere 46:583–624
De Wit CA, Alaee M, Muir DCG (2006) Levels and trends of brominated flame retardants in the Arctic. Chemosphere 64:209–233
EC (2008) Regulation (EC) No 1272/2008 of the European Parliament and of the Council of 16 December 2008 on classification, labelling and packaging of substances and mixtures, amending and repealing Directives 67/548/EEC and 1999/45/EC, and amending Regulation (EC) No 1907/2006 (Text with EEA relevance). Off J Eur Union L353:1355
Escartin E, Porte C (1997) The use of cholinesterase and carboxylesterase activities from Mytilus galloprovincialis in pollution monitoring. Environ Toxicol Chem 16:2090–2095
Fitzpatrick PJ, O´Halloran J, Sheehan D, Walsh AR (1997) Assessment of a glutathione S-tranferase and related proteins in the gill and digestive gland of Mytilus edulis (L.), as potential organic pollution biomarkers. Biomarkers 2:51–56
Funes V, Alhama J, Navas JI, López-Barea J, Peinado J (2006) Ecotoxicological effects of metal pollution in two mollusc species from the Spanish South Atlantic litoral. Environ Pollut 139:214–223
Galgani F, Bocquené G (1989) A method for routine detection of organophosphates and carbamates in sea water. Environ Technol Lett 10:311–322
Gama AC, Sanatcumar P, Viana P, Barceló D, Bordado JC (2006) The occurrence of polybrominated diphenyl ethers in river and coastal biota from Portugal. Chemosphere 64:306–310
Grintzalis k, Georgiou CD, Dailianis S (2012) Total thiol redox status as a potent biomarker of PAH-mediated effects on mussels. Mar Environ Res 81:26–34
Guilhermino L, Barros P, Silva MC, Soares AMVM (1998) Should the use of inhibition of cholinesterases as a specific biomarker for organophosphate and carbamate pesticides be questioned? Biomarkers 3(2):157–163
Gustafsson K, Björk M, Burreau S, Gilek M (1999) Bioaccumulation kinetics of brominated flame retardants (polybrominated diphenyl ethers) in blue mussels (Mytilus edulis). Environ Toxicol Chem 16:1218–1224
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-tranferase. The first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139
Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine. Oxford University Press, Oxford
Ji C, Wu H, Wei L, Zhao J, Yu J (2013) Proteomic and metabolomic analysis reveal gender-specific responses of mussel Mytilus galloprovincialis to 2, 2′, 4, 4′-tetrabromodiphenyl ether (BDE 47). Aquat Toxicol 140–141:449–457
Johansson I, Héas-Moisan K, Guiot N, Munschy C, Tronczynski J (2006) Polybrominated diphenyl ethers (PBDEs) in mussels from selected French coastal sites: 1981–2003. Chemosphere 64:296–305
Key PB, Hoguet J, Chung KW, Venturella JJ, Pennington PL, Fulton MH (2009) Lethal and sublethal effects of simvastatin, irgarol, and PBDE-47 on the estuarine fish, Fundulus heteroclitus. J Environ Sci Health B 44(4):379–382
Landrum PF, Lee H II, Lydy MJ (1992) Toxicokinetics in aquatic systems: model comparisons and use in hazard assessment. Environ Toxicol Chem 11:1709–1725
Lema SC, Schultz I, Scholz N, Incardona J, 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
Livingstone DR (1990) Cytochrome P-450 and Oxidative-metabolism in invertebrates. Biochem Soc Trans 18:15–19
Livingstone DR (1991) Organic xenobiotic metabolism in marine invertebrates. Adv Comput Environ Phys 7:45–185
Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:266–275
McHenery JG, Linley-Adams GE, Moore DC, Rodger GK, Davies IM (1997) Experimental and field studies of effects of dichlorvos exposure on acetylcholinesterase activity in the gills of the mussel, Mytilus edulis L. Aquat Toxicol 38:125–143
Mhadhbi L (2012) Etude écotoxicologique des composés polybromés (PBDEs) et perfluorés (PFCs) chez les larves et juveniles du turbot (Psetta máxima). PhD. These, Université de Carthage, Tunize
Minier C, Forget-Leray J, Bjϕrnstad A, Camus L (2008) Multixenobiotic resistance, acetyl-choline esterase activity and total oxyradical scavenging capacity of the Arctic spider crab, Hyas araneus, following exposure to bisphenol A, tetra bromo diphenyl ether and diallyl phthalate. Mar Pollut Bull 56:1410–1415
Oliveira M, Ribeira A, Hylland K, Guilhermino L (2013) Single and combined effects of microplastics and pyrene on juveniles (0 + group) of the common goby Pomatoschistus microps (Teleostei, Gobiidae). Ecol Indic 34:641–647
Orbea A, Cajaraville MP (2006) Peroxisome proliferation and antioxidant enzymes in transplanted mussels of four Basque estuaries with different levels of polycyclic aromatic hydrocarbon and polychlorinated biphenyl pollution. Environ Toxicol Chem 25:1616–1626
OSPAR Commission (2014) http://www.ospar.org Last visit: 27/02/2014
Parolini M, Binelli A (2012) Cyto-genotoxic effects induced by three brominated diphenyl ether congeners on the fresh water mussel Dreissena polymorpha. Ecotoxicol Environ Saf 79:247–255
Parolini M, Pedriali A, Binelli A (2012) Variation of antioxidant activity in Dreissena polymorpha specimens exposed to 2,2′,4,4′,5,6′-hexa BDE (BDE-154). Water Air Soil Pollut 223:3067–3076
Prevedouros K, Jones KC, Sweetman AJ (2004) Estimation of the production, consumption, and atmospheric emissions of pentabrominated diphenyl ether in Europe between 1970 and 2000. Environ Sci Technol 38:3224–3231
Prohaska JR (1980) The glutathione peroxidase activity of glutathione S-transferase. Biochim Biophys Acta 611:87–98
QUASIMEME (2004) QUASIMEME Laboratory Performance Studies. SOAFD. Marine Laboratory. P.O. Box 101, Victoria Road, Aberdeen
Regoli F, Principato G (1995) Glutathione, glutathione-dependent and antioxidant enzymes in mussel, Mytilus galloprovincialis, exposed to metals under field and laboratory conditions: implications for the use of biochemical biomarkers. Aquat Toxicol 31:143–164
Roberts SC, Noyes PD, Gallagher EP, Stapleton HM (2011) Species-specific differences and structure-activity relationships in the debromination of PBDE congeners in three fish species. Environ Sci Technol 45:1999–2005
Santos MA, Pacheco M, Ahmad I (2004) Anguilla anguilla L. antioxidants responses to in situ bleached kraft pulp mill effluent outlet exposure. Environ Int 30:301–308
Sheehan D, Meade G, Foley VM, Dowd CA (2001) Structure, function and evolution of glutathione transferase for classification of non-mammalian members of an ancient superfamily. Biochem J 360:1–16
Stockholm Convention (2014) http://chm.pops.int Last visit: 27/02/2014
Tsangaris C, Kormas K, Strogyloudi E, Hatzianestis I, Neofitou C, Andral B, Galgani F (2010) Multiple biomarkers of pollution effects in caged mussels on the Greek coastline. Comp Biochem Phys C 151:369–378
Van der Oost R, Beyer J, Vermeulen NEP (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharm 13:57–149
Vidal-Liñán L, Bellas J (2013) Practical procedures for selected biomarkers in mussels, Mytilus galloprovincialis—implications for marine pollution monitoring. Sci Total Environ 461–462:56–64
Vidal-Liñán L, Bellas J, Campillo JA, Beiras R (2010) Integrated use of antioxidant enzymes in mussels, Mytilus galloprovincialis, for monitoring pollution in highly productive coastal areas of Galicia (NW Spain). Chemosphere 78:265–272
Wells D, Cofino W (1997) The assessment of the QUASIMEME laboratory performance studies data: techniques and approach. Mar Pollut Bull 35:18–27
Wolkers H, Van Bavel B, Derocher AE, Wiig O, Kovacs KM, Lydersen C, Lindstrom G (2004) Congener-specific accumulation and food chain transfer of polybrominated diphenyl ethers in two Artic food chains. Environ Sci Technol 38:1667–1674
Zhao A, Liu H, Zhang A, Wang Z, Zhang H, Wang H (2011) Effect of BDE-209 on glutathione system in Carassius auratus. Environ Toxicol Chem 32:35–38
Acknowledgments
Authors are grateful to Marta Miñambres, Tania Tato, Cristina García-Arboleya and Diego Rial for their technical assistance and personnel at ECIMAT. This work was financed by the Spanish Ministry of Science and Innovation through the Research Project (CTM2009-10908). The first author was granted with a FPU fellowship from the Spanish Government.
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Vidal-Liñán, L., Bellas, J., Fumega, J. et al. Bioaccumulation of BDE-47 and effects on molecular biomarkers acetylcholinesterase, glutathione-S-transferase and glutathione peroxidase in Mytilus galloprovincialis mussels. Ecotoxicology 24, 292–300 (2015). https://doi.org/10.1007/s10646-014-1377-5
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DOI: https://doi.org/10.1007/s10646-014-1377-5