Abstract
In this study, sublethal effects on the Mediterranean mussels (Mytilus galloprovincialis L.) collected from the Aegean coast of Turkey were determined. Enzymes such as glutathione-S-transferase (GST), superoxide dismutase (SOD), catalase (CAT), and acetylcholinesterase (AChE), metallothionein (MT) mRNA expressions, thiobarbituric acid reactive substances (TBARS) contents, determination of 14 heavy metals and micronucleus frequency were selected as multibiomarkers. Results show that heavy metals and an increase in the level of MT gene expression have been determined in tissues of mussels collected from all stations. The GST, SOD and CAT enzymes were increased in mussels of Aliaga and Old Foca, compared to the mussels of Urla, while it was showed inhibition at AChE levels. Extensive LP is determined on mussels of Aliaga. It was determined that mussels in Aliaga region have exposed more oxidative stress than Old Foca and Urla. These biomarkers were carried out for the first time in these stations to assess environmental quality.
Similar content being viewed by others
References
Aceto S, Formisano G, Carella F et al (2011) The metallothionein genes of Mytilus galloprovincialis: genomic organization, tissue expression and evolution. Mar Genomics 4:61–68
Amiard JC, Amiard-Triquet C, Barka S et al (2006) Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomarkers. Aquat Toxicol 76:160–202
Anandraj A, Marshall DJ, Gregory MA, McClurg TP (2002) Metal accumulation, filtration and O2 uptake rates in the mussel Pernaperna (Mollusca: Bivalvia) exposed to Hg2+, Cu 2+ and Zn2+. Comp Biochem Physiol C Pharmacol Toxicol 132:355–363
Bebianno MJ, Machado LM (1997) Concentrations of metals and metallothioneins in Mytilus galloprovincialis along the South coast of Portugal. Mar Pollut Bull 34:666–671
Beers RF Jr, Sizer IW (1951) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195(1):133–140
Bradford MM (1976) A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254
Cakal Arslan O, Boyacioglu M, Parlak H et al (2015) Assessment of micronuclei induction in peripheral blood and gill cells of some fish species from Aliaga Bay Turkey. Mar Pollut Bull 94:48–54
Canesi L, Ciacci C, Piccoli G et al (1998) In vitro and in vivo effects of heavy metals on mussel digestive gland hexokinase activity: the role of glutathione. Comp Biochem Physiol C 120:261–268
Caricato R, Lionetto MG, Schettino T (2010) Seasonal variation of biomarkers in Mytilus galloprovincialis sampled inside and outside Mar Piccolo of Taranto (Italy). Chem Ecol 26:143–153.
Chafik A, Cheggour M, Cossa D et al (2001) Quality of Moroccan Atlantic coastal water monitoring and mussel watching. Aquat Living Resour 14:239–249
Dondero F, Piacentini L, Banni M et al (2005) Quantitative PCR analysis of two molluscan metallothionein genes unveils differential expression and regulation. Gene 345:259–270
Ellman GL, Courtney KD, Andres V Jr et al (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95
Environmental Pollution Agency (EPA) (1999) Compendium Method TO-13A, Environmental Pollution Agency (EPA), Cincinatti
Ercal N, Gurer-Orhan H, Aykin-Burns N (2001) Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative damage. Curr Top Med Chem 1(6):529–539
Esen E, Küçüksezgin F, Uluturhan E (2010) Assessment of trace metal pollution in surface sediments of Nemrut Bay, Aegean Sea. Environ Monit Assess 160:257–266
Fitzpatrick PJ, Sheehan D (1993) Separation of multiple forms of glutathione S-transferase from the blue mussel; Mytilus edulis. Xenobiotica 23:851–861
Frenzilli G, Bocchetti R, Pagliarecci M et al (2004) Time-course evaluation of ROS-mediated toxicity in mussels Mytilus galloprovincialis during a field translocation experiment. Mar Environ Res 58:609–613
Gokdeniz N, Kontas A, Unsalan D et al (2012) Heavy metals cotamination levels at the Coast of Aliaga (Turkey) ship recycling zone. Mar Pollut Bull 64:882–887
Grattarola M, Carloni M, Dondero F et al (2006) Expression, purification and preliminary characterization of mussel (Mytilus galloprovincialis) metallothionein MT20. Mol Biol Rep 33:265–272
Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases. The first enzymatic step in mercapturic acid formation. J Biol Chem 249(22):7130–7139
Katalay S, Parlak H (2004) The effects of pollution on hematological parameters of black goby (Gobius niger L., 1758) in Foça and Aliağa Bays. Turk J Fish Aquat Sci 21:113–117
Kucuksezgin F, Kayatekin BM, Uluturhan E et al (2008) Preliminary investigation of sensitive biomarkers of trace metal pollution in mussel (Mytilus galloprovincialis) from Izmir Bay (Turkey). Environ Monit Assess 141:339–345
Lemoine S, Bigot Y, Sellos DE, Cosson RP, Laulier M (2000) Metallothionein isoforms in Mytilus edulis (Mollusca, Bivalvia): complementary DNA characterization and quantification of expression in different organs after exposure to cadmium, zinc, and copper. Mar Biotechnol 2:195–203
Lionetto MG, Caricato R, Giordano ME et al (2003) Integrated use of biomarkers (acetylcholinesterase and antioxidant enzyme activities) in Mytilus galloprovincialis and mullusbarbatus in an Italian coastal marine area. Mar Pollut Bull 46:324–330
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25(4):402–428
Livingstone DR (2001) Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Mar Pollut Bull 42:656–666
Mersh J, Beauvais MN, Nagel P (1996) Induction of micronuclei in haemocytes and gill cells of zebra mussels, Dreissena polymorpha, exposed to clastogens. Mutat Res 371:47–55
Nasci C, Nesto N, Monteduro RA, Da Ros L (2002) Field application of biochemical markers and a physiological index in the mussel, Mytilus galloprovincialis: transplantation and biomonitoring studies in the Lagoon of Venice (NE Italy). Mar Environ Res 54:811–816
Neser G, Kontas A, Unsalan D et al (2012) Heavy metals contamination levels at the Coast of Aliaga (Turkey) ship recycling zone. Mar Pollut Bull 64:882–887
Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95(2):351–358
Patra RC, Rautray AK, Swarup D (2011) Oxidative stress in lead and cadmium toxicity and its amelioration. Vet Med Int 2011:457327
Pazi I (2011) Assessment of heavy metal contamination in Candarli gulf sediment, Eastern Aegean Sea. Environ Monit Assess 174:199–208
Peakall DB (1992) Animal biomarkers as pollution indicators. Chapman and Hall, London
Phillips DJH, Rainbow PS (1989) Strategies of trace metal sequestration in aquatic organisms. Mar Environ Res 28:207–210
Ramsak A, Scancar J, Horvat M (2012) Evaluation of metallothioneins in blue mussels (Mytilus galloprovincialis) as a biomarker of mercury and cadmium exposure in the slovenian waters (Gulf of Trieste): a long-term field study. Acta Adriat 53(1):71–86
Regoli F (1998) Trace metals and antioxidant enzymes in gills and digestive gland of the mediterranean mussel Mytilus galloprovincialis. Arch Environ Contam Toxicol 34:48–63
Regoli F, Principato G (1995) Gluatathione, glutathione-dependent and antioxidant enzymes in mussel, Mytilus galloprovincialis, exposed to metal under field and laboratory conditions: implications for the use of biochemical biomarkers. Aquatic Toxicol 31:143–164
Remeo M, Gnassia-Barelli M (1997) Effect of heavy metals on lipid peroxidation in the mediterranean clam ruditapes decussatus. Comp Biochem Physiol C 118:33–37
Rouane-Hacenea O, Boutibaa Z, Belhaouaria B et al (2015) Seasonal assessment of biological indices, bioaccumulation and bioavailability of heavy metals in mussels Mytilus galloprovincialis from Algerian west coast, applied to environmental monitoring. J Oceano 57(4):362–374
Sato M, Bremner I (1993) Oxygen free radicals and metallothionein. Free Radic Biol Med 14(3):325–337
Sen A, Ulutas OK, Tutuncu B, Ertas N, Cok I (2010) Determination of 7- ethoxyresorufin-o-deethylase (EROD) induction in leaping mullet (Lizasaliens) from the highly contaminated Aliaga Bay, Turkey. Environ Monit Assess 165:87–96
Sponza D, Karaoglu N (2002) Environmental geochemistry and pollution studies of Aliağa metal industry district. Environ Int 27:541–553
Sridevi B, Reddy KV, Reddy SLN (1998) Effect of trivalent and hexavalent chromium on antioxidant enzyme activities and lipid peroxidation in a freshwater field crab, Barytelphusa guerini. Bull Environ Contam Toxicol 61:384–390
Venier P, Maron S, Canova S (1997) Detection of micronuclei in gill cells and haemocytes of mussels exposed to benzo[a]pyrene. Mutat Res 390:33–44
Viarengo A, Zanicchi G, Moore MN, Orunesu M (1981) Accumulation and detoxification of copper by the mussel Mytilus galoprovincialis Lam: a study of the subcellular distribution in the digestive gland cells. Aquatic Toxicol 1:147–157
Vioque-Fernández A, Alves de Almeida E, Ballesteros J et al (2007) Dõnana national park survey using crayfish (Procambarus clarkii) as bioindicator: esterase inhibition and pollutant levels. Toxicol Lett 168:260–268
Wóznicki P, Lewandowska R, Brzuzan P et al (2004) The level of DNA damage and the frequency of micronuclei in haemolymph of fresh water mussels Anodonta woodiana exposed to benzo[a] pyrene. Acta Toxicologia 12(1):41–45
Yavasoglu A, Ozkan D, Guner A, Katalay S, Oltulu F, Karabay Yavasoglu NU (2016) Histopathological and apoptotic changes on marine mussels Mytilus galloprovincialis (Lamark, 1819) following exposure to environmental pollutants. Mar Pollut Bull 109(1):184–191
UNEP/RAMOGE (1999) Manual on The Biomarkers Recommended for The MED POL Biomonitoring Programme. UNEP, Athens, p. 94
Acknowledgements
The study is supported by Ege University BAP project (2012-ÇSUAM-003).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ozkan, D., Dagdeviren, M., Katalay, S. et al. Multi-Biomarker Responses After Exposure to Pollution in the Mediterranean Mussels (Mytilus galloprovincialis L.) in the Aegean Coast of Turkey. Bull Environ Contam Toxicol 98, 46–52 (2017). https://doi.org/10.1007/s00128-016-1988-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00128-016-1988-z