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Anthropogenic pollution stimulates oxidative stress in soft tissues of mussel Crenomytilus grayanus (Dunker1853)

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Abstract

The digestive gland and gills of the mussel Crenomytilus grayanus extracted from three locations — (i) sampled from a clean and (ii) polluted site and (iii) transplanted from the nonpolluted to polluted site - were analysed for antioxidant enzymes (superoxide dismutase, catalase, glutathione reductase), total oxyradical scavenging capacity and levels of lipid peroxidation products (malondialdehyde, conjugated dienes and lipofuscin). Perturbation of redox status was found in both digestive gland and gill tissues of mussels living in the polluted area. As the activities of superoxide dismutase and catalase were 1.2–3 times higher, the total oxyradical scavenging capacity was lower by 20–35% and the levels of lipid peroxidation products were 2–7 times higher compared to mussels from the reference site. In transplanted mussels, the lipid peroxidation process in both tissues was significantly stimulated (the level of conjugated dienes was increased 1.7–2.5-fold; malondialdehyde and lipofuscin contents were increased 3.5–5-fold) and the total oxyradical scavenging capacity fell by 50–70%. In addition, the transplantation generally resulted in transient and variable responses of antioxidant enzymes for both tissues. Complex response-behaviour of the antioxidant enzymes strongly points to the necessity of employing a combined approach that takes into account activities of antioxidant enzymes and the total oxyradical scavenging capacity, as well as measurement of oxidative damage (e.g., lipid peroxidation) to evaluate the physiological health of molluscs.

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Reference

  • Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Meth Enzymol 52:302–310

    Article  Google Scholar 

  • Chandran R, Sivakumar AA, Mohandass S, Aruchami M (2005) Effect of cadmium and zinc on antioxidant enzyme activity in the gastropod, Achatina fulica. Comp Biochem Physiol C 140:422–426

    Google Scholar 

  • Chelomin VP, Belcheva NN (1992) The effect of heavy metals on processes of lipid peroxidation in microsomal membranes from the hepatopancreas of bivalve mollusks Mizuhopecten yessoensis. Comp Biochem Physiol C 103:419–422

    Article  Google Scholar 

  • Chelomin VP, Zakhartsev MV, Kurilenko A, Belcheva NN (2005) An in vitro study of the effect of reactive oxygen species on subcellular distribution of deposited cadmium in digestive gland of mussel Crenomytilus grayanus. Aquat Toxicol 73:181–189

    Article  Google Scholar 

  • Company R, Serafim A, Bebiano MJ, Cosson R, Shillito B, Fiala-Medioni A (2004) Effect of cadmium and mercury on antioxidant enzyme activities and lipid peroxidation in the gills of the hydrothermal vent mussel Bathymodiolus azoricus. Mar Environ Res 58:377–381

    Article  Google Scholar 

  • Cossu C, Doyotte A, Babut M, Exinger A, Vasseur P (2000) Antioxidant biomarkers in freshwater bivalves Unio tumidus in response to different contamination profiles of aquatic sediments. Ecotoxicol Environ Saf 45:106–121

    Article  Google Scholar 

  • De Almeida EA, Miyamot S, Bainy AC, de Medeiros MHG, Di Mascio P (2004) Protective effect of phospholipid hydroperoxide glutathione peroxidase (PHGPx) against lipid peroxidation in mussels Perna perna exposed to different metals. Mar Pollut Bull 49:386–392

    Article  Google Scholar 

  • Di Giulio RT, Washburn PC, Wenning RJ, Winston GW, Jewell CS (1989) Biochemical responses in aquatic animals: a review of determinants of oxidative stress. Environ Toxicol Chem 8:1103–1123

    Article  Google Scholar 

  • Dovzhenko NV, Kurilenko AV, Belcheva NN, Chelomin VP (2005) Cadmium-induced oxidative stress in the bivalve mollusk Modiolus modiolus. Russ J Mar Biol 31:309–313

    Article  Google Scholar 

  • Folch J, Lees M, Stanley J (1957) A simple method for isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    Google Scholar 

  • Frenzilli G, Nigro M, Scarcelli V, Gorbi S, Regoli F (2001) DNA integrity and total oxyradical scavenging capacity in the Mediterranean mussel, Mytilus galloprovincialis: a field study in a highly eutrophicated coastal lagoon. Aquat Toxicol 53:19–32

    Article  Google Scholar 

  • George S (1982) Subcellular accumulation and detoxication of metals in aquatic animals. In: Vernberg WB, Calabrese A, Thurberg FP, Vernberg FJ (eds) Physiological Mechanisms of Marine Pollutant Toxicity, Academic Press, New York, pp 3–52

    Google Scholar 

  • Geret F, Serafim A, Barreira L, Bebianno MJ (2002) Response of antioxidant systems to copper in the gills of the clam Ruditapes decussatus. Mar Environ Res 54:413–417

    Article  Google Scholar 

  • Greenberg CS, Gaddock PR (1982) Rapid single-step membrane protein assay. Clin Chem 28:1725–1726

    Google Scholar 

  • Kavun V Ya, Shulkin VM (2005) Changes in the microelement composition in organs and tissues of the bivalve Crenomytilus grayanus acclimatized in a biotope with long-term heavy metal contamination. Russ J Mar Biol 31:109–114

    Article  Google Scholar 

  • Kovekovdova LT (1993) Tyazhelye metally v promyslovykh bespozvonochnykh zaliva Petra Velikogo v svyazi s usloviyami sushchestvovaniya (Heavy metals in fished invertebrates of Peter the Great Bay in connection with environment). Far Eastern Science Center, Vladivostok, pp 2–25 (In Russian)

    Google Scholar 

  • Livingston DP, Garcia-Martinez P, Winston GW (1989) Menadionstimulated oxyradical formation in digestive gland microsomes of the common mussel Mytilus edulis L. Aquat Toxicol 15:213–236

    Article  Google Scholar 

  • Livingston DP, Lips F, Martine PG, Pipe RK (1992) Antioxidant enzymes in the digestive gland of the common mussel Mytilus edulis. Mar Biol 112:265–276

    Article  Google Scholar 

  • Livingstone DR (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42:656–666

    Article  Google Scholar 

  • Livingstone DR (2003) Oxidative stress in aquatic organisms in relation to pollution and aquaculture. Rev Med Vet-Toulouse 154:427–430

    Google Scholar 

  • Manduzio H, Monsinjon T, Rocher B, Leboulenger F, Galap C (2003) Characterization of an inducible isoform of the Cu/Zn superoxide dismutase in the blue mussel Mytilus edulis. Aquat Toxicol 64:73–83

    Article  Google Scholar 

  • Nasci C, Da Ros L, Campesan G, Van Vleet ES, Salizzato M, Sperni L, Pavoni B (1999) Clam transplantation and stressrelated biomarkers as useful tools for assessing water quality in coastal environments. Mar Pollut Bull 39:255–260

    Article  Google Scholar 

  • Olivier F, Ridd M, Klampp D (2002) The use of transplanted cultured tropical oysters (Saccosrea commercialis) to monitor Cd levels in North Queensland coastal waters (Australia). Mar Pollut Bull 44:1051–1062

    Article  Google Scholar 

  • Paoletti F, Aldinuccio D, Mocali A, Carparrini A (1986) A sensitive spectrophotometric method for the determination of superoxide dismutase in tissue extracts. Anal Biochem 154:526–541

    Article  Google Scholar 

  • Perez E, Blasco J, Sole M (2004) Biomarker responses to pollution in two invertebrate species: Scrobicularia plana and Nereis diversicolor from the Cadiz bay (SW Spain). Mar Environ Res 58:275–279

    Article  Google Scholar 

  • Podgurskaya OV, Kavun V Ya (2005) Comparison of the subcellular distribution of heavy metals in organs of the bivalves Crenomytilus grayanus and Modiolus modiolus from a chronically polluted area. Russ J Mar Biol 31:435–442

    Article  Google Scholar 

  • Podorvanova NF, Ivashinnikova TS, Petrenko VS, Khomichuk LS (1989) Osnovnye cherty gidrokhimii zaligva Petra Velikogo, Yaponskoe more (The main hydrochemical features of Peter the Great Bay (the East Sea)). Far East Branch of the Russian Academy of Sciences, Vladivostok, pp 3–201 (In Russian)

    Google Scholar 

  • Regoli F (2000) Total oxyradical scavenging capacity (TOSC) in polluted and translocated mussels: a predictive biomarker of oxidative stress. Aquat Toxicol 50:351–361

    Article  Google Scholar 

  • Regoli F, Gorbi S, Frenzilli G, Nigro M, Corsi I, Focardi S, Winston GW (2002) Oxidative stress in ecotoxicology: from the analysis of individual antioxidants to a more integrated approach. Mar Environ Res 54:419–423

    Article  Google Scholar 

  • Regoli F, Hummel H, Amiard-Triquet C, Larroux C, Sukhotin A (1998a) Trace metals and variations of antioxidant enzymes in arctic bivalve populations. Arch Environ Contam Toxicol 35:594–601

    Article  Google Scholar 

  • Regoli F, Nigro M, Orlando E (1998b) Lysosomal and antioxidant responses to metals in the Antarctic scallop Adamussium colbecki. Aquat Toxicol 40:375–392

    Article  Google Scholar 

  • Regoli F, Principato G (1995) Glutathione, glutathione-depended 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

    Article  Google Scholar 

  • Ribera D, Narbonne JF, Michel X, Livingstone DR, O’Hara X (1991) Responses of antioxidants and lipid peroxidation in mussels to oxidative damage exposure. Comp Biochem Physiol C 100:177–181

    Article  Google Scholar 

  • Romeo-Ruiz A, Amezcua O, Rodriguez-Ortega MJ, Munoz JL, Alhama J, Rodriguez-Ariza A, Gomez-Ariza JL, Lopez-Barea J (2002) Oxidative stress biomarkers in bivalves transplanted to the Guadalquivir estuary after Aznalcollar spill. Environ Toxicol Chem 22:92–100

    Article  Google Scholar 

  • Shen Y, Sangiah S (1995) Na+, K+-ATPase, glutathione, and hydroxyl free radicals in cadmium chloride-induced testicular toxicity in mice. Arch Environ Contam Toxicol 29:174–179

    Article  Google Scholar 

  • Shimasaki H, Hirai N, Ueta N (1988) Comparison of fluorescence characteristics of products of peroxidation of membrane phospholipids with those of products derived from reaction of malonaldehyde with glycine as a model of lipofuscin fluorescent substances. J Biochem 104:761–766

    Google Scholar 

  • Shulkin VM, Kavun V Ya, Presley BJ (2003) Metal concentrations in mussel Crenomytilus grayanus and Crassostrea gigas in relation to contamination of ambient sediments. Environ Int 29:493–502

    Article  Google Scholar 

  • Shulkin VM, Kavun V Ya, Tkalin AV, Presley B (2002) The influence of metal concentration in bottom sediments on metal accumulation by mytilids Crenomytilus grayanus and Modiolus kurilensis. Russ J Mar Biol 28:53–61

    Article  Google Scholar 

  • Simkiss K, Taylor M, Mason AZ (1982) Metal detoxification and bioaccumulation in molluscs. Mar Biol Lett 3:187–201

    Google Scholar 

  • Tkalin AV, Samsonov DP, Lishavkaya TS, Chernik GV (2000) New data on organochlorine distributions in the marine environment near Vladivostok. Mar Pollut Bull 40:879–881

    Article  Google Scholar 

  • Torres MA, Testa CP, Gaspari C, Masutti MB, Panitz CMN, Curi-Pedrosa R, De Almeida EA, Di Mascio P, Filho DW (2002) Oxidative stress in mussel Mytella guyanensis from polluted mangroves on Santa Catarina Island, Brazil. Mar Pollut Bull 44:923–932

    Article  Google Scholar 

  • Viarengo A (1989) Heavy metals in marine invertebrates: mechanisms of regulation and toxicity at the cellular level. CRC Crit Rev Aquat Sci 1:295–317

    Google Scholar 

  • Viarengo A, Moore MN, Mancinelli G, Mazzucotelli A, Pipe RK, Farrar SV (1987) Metallothioneins and lysosomes in metal toxicity and accumulation in marine mussels: the effect of cadmium in the presence of phenanthrene. Mar Biol 94:251–257

    Article  Google Scholar 

  • Walker ST, Mantle D, Bythell JC, Thomason JC (2000) Oxidativestress: comparison of species specific and tissues specific effects in the marine bivalves Mytilus edulis (L.) and Dosinia lupinus (L.). Comp Biochem Physiol B 127:347–355

    Article  Google Scholar 

  • Wenning RJ, Di Giulio RT. Gallagher EP (1988) Oxidant-mediated biochemical effects of paraquat in the ribbed mussel, Geukensia demissa. Aquat Toxicol 12:157–170

    Article  Google Scholar 

  • Winston GW, Regoli F, Dugas AJ Jr, Fong JH, Blanchard KA (1998) A rapid gas chromatographic assay for determining oxyradical scavenging capacity of antioxidants and biological fluids. Free Rad Biol Med 24:480–493

    Article  Google Scholar 

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Authors and Affiliations

  1. V.I. Il’ichev Pacific Oceanological Institute, Far Eastern Branch, Russian Academy of Sciences, Vladivostok, 690041, Russia

    Nina N. Belcheva, Nadezhda V. Dovzhenko, Avianna F. Zhukovskaya & Victor P. Chelomin

  2. Institute of Pharmacy and Molecular Biotechnology (IPMB), University of Heidelberg, Im Neuenheimer Feld 364, Heidelberg, D-69120, Germany

    Maxim V. Zakhartsev

  3. A.V. Zhirmunsky Institute of Marine Biology, Far Eastern Branch, Russian Academy of Sciences, Vladivostok, 690041, Russia

    Victor Ya. Kavun

Authors
  1. Nina N. Belcheva
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  2. Maxim V. Zakhartsev
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  3. Nadezhda V. Dovzhenko
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  4. Avianna F. Zhukovskaya
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  5. Victor Ya. Kavun
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  6. Victor P. Chelomin
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Correspondence to Nina N. Belcheva.

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Belcheva, N.N., Zakhartsev, M.V., Dovzhenko, N.V. et al. Anthropogenic pollution stimulates oxidative stress in soft tissues of mussel Crenomytilus grayanus (Dunker1853). Ocean Sci. J. 46, 85–94 (2011). https://doi.org/10.1007/s12601-011-0008-9

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  • DOI: https://doi.org/10.1007/s12601-011-0008-9

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