Skip to main content
SpringerLink
Log in

Cellular Biomarkers in Mytilus galloprovincialis L. (Mediterranean Mussels) from Izmir Bay (Turkey)

  • Published:
Bulletin of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

In this study, cellular biomarkers and heavy metal concentration in the Mytilus galloprovincialis L. (Mediterranean mussels) collected from eight sites of Izmir Bay (Turkey) were determined to reveal water pollution for the first time in these stations. Results show that heavy metals (As, Cu, Hg, Zn, Cd, Sn, Pb) have been specified in mussels’ tissues collected from all stations. According to GST, SOD, CAT activities, and TBARS contents, mussels in the outer bay have exposed more oxidative stress than the ones in the inner bay. Digestive gland tissues of them were showed more inhibition at AChE levels than gills. Also, abnormal nucleus rates and micronucleus frequencies (MN) were found to be higher in the inner bay than in the outer bay. This study showed that heavy metal pollution in different levels is an environmental issue on the Izmir Bay. Especially the coastal regions of the bay have been extremely affected by anthropogenic effects due to growing population.

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

Similar content being viewed by others

References

  • Arslan OC, Parlak H, Katalay S et al (2010) Detecting micronuclei frequency in some aquatic organisms for monitoring pollution of Izmir Bay (Western Turkey). Environ Monit Assess 165(1–4):55–66

    Article  Google Scholar 

  • Atgin RS, El-Agha O, Zararsız A et al (2000) Investigation of the sediment pollution in Izmir Bay: trace elements. Spectrochim Acta Part B At Spectroscopy 55(7):1151–1164

    Article  Google Scholar 

  • Azizi G, Akodad M, Baghour M et al (2018) The use of Mytilus spp. mussels as bioindicators of heavy metal pollution in the coastal environment. J Mater Environ Sci 9(4):1170–1181

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Binelli A, Cogni D, Parolini M, Provini A (2010) Multi-biomarker approach to investigate the state of contamination of the R. Lambro/R. Po confluence (Italy) by zebra mussel (Dreissena polymorpha). Chemosphere 79(5):518–528

    Article  CAS  Google Scholar 

  • Bozcaarmutlu A, Arinc E (2004) Inhibitory effects of divalent metal ions on liver microsomal 7-ethoxyresorufin O- deethylase (EROD) activity of leaping mullet. Mar Environ Res 58:521–524

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Cardellicchio N, Buccolieri A, Di Leo A et al (2008) Levels of metals in reared mussels from Taranto Gulf (Ionian Sea, Southern Italy). Food Chem 107:890–896

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Chang LW, Magos L, Suzuki T (eds) (2019) Toxicology of Metals. Volume 1 CRC Lewis, Boca Raton, FL

    Google Scholar 

  • Da Ros L, Nasci C, Marigomez I, Soto M (2000) Biomarkers and trace metals in the digestive gland of indigenous and transplanted mussels, Mytilus galloprovincialis, in Venice Lagoon, Italy. Mar Environ Res 50(1–5):417–423

    Article  Google Scholar 

  • Dobal AV, Suárez P, Ruiz Y et al (2022) Activity of antioxidant enzymes in Mytilus galloprovincialis exposed to tar: Integrated response of different organs as pollution biomarker in aquaculture areas. Aquaculture 548:737638

    Article  CAS  Google Scholar 

  • Ellman GL, Courtney KD, Andres V Jr et al (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95

    Article  CAS  Google Scholar 

  • Environmental Pollution Agency (EPA) (1999) Compendium Method TO-13A, Cincinatti, OH, USA

  • 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

    Article  CAS  Google Scholar 

  • Ewing JF, Janero DR (1995) Microplate superoxide dismutase assay employing a nonenzymatic superoxide generator. Anal Biochem 232(2):243–248

    Article  CAS  Google Scholar 

  • Fitzpatrick PJ, Sheehan D (1993) Separation of multiple forms of glutathione S-transferase from The Blue Mussel; Mytilus edulis. Xenobiotica 23:851–861

    Article  CAS  Google Scholar 

  • Giamberini L, Auffert M, Pihan JC (1996) Haemocytes of the Freshwater Mussel, Dreissena polymorphia Pallas: Cytology, Cytochemistry and X-ray Microanalysis. J Mollusc Stu 62(3):367–379

    Article  Google Scholar 

  • Goyal MM, Basak A (2010) Human catalase: looking for complete identity. Protein Cell 1(10):888–897

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Hayashi M (2016) The micronucleus test-most widely used in vivo genotoxicity test. Genes Environ 38:18

    Article  Google Scholar 

  • IMST (1995) and 1997) MEDPOL II. Long-term scientific monitoring and measurement project in the Aegean Sea. Technical Final Report, Institute of Marine Sciences & Technology, Izmir, Turkey

  • Kucuksezgin F (2011) The Water Quality of Izmir Bay: a case study. Rev Environ Contam Tox 211:1–24

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kucuksezgin F, Kontaş A, Altay O et al (2006) Assessment of marine pollution in Izmir Bay: Nutrient, heavy metal and total hydrocarbon concentrations. Environ Int 32:41–51

    Article  CAS  Google Scholar 

  • Kucuksezgin F, Uluturhan E, Kontas A, Altay O (2002) Trace metal concentrations in edible fishes from Izmir Bay, Eastern Aegean. Mar Pollut Bull 44(8):827–832

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Lionetto MG, Caricato R, Giordano ME et al(2019) Pollution Biomarkers in Environmental and Human Biomonitoring, The Open Biomarkers J 9: 1–9. doi.10.2174/1875318301909010001

  • Livingstone DR (2003) Oxidative stress in aquatic organisms in relation to pollution and aquaculture. Revue M´ed V´et 154:427–430

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95(2):351–358

    Article  CAS  Google Scholar 

  • Ozkan D, Dagdeviren M, Katalay S et al (2017) 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(1):46–52

    Article  CAS  Google Scholar 

  • Patra RC, Rautray AK, Swarup D (2011) Oxidative stress in lead and cadmium toxicity and its amelioration. Vet Med Int 4:57327

    Google Scholar 

  • Peakall DB (1992) Animal Biomarkers as Pollution Indicators. Chapman and Hall, London

    Book  Google Scholar 

  • Prochazka ST, Cope WG, Recio L (2012) Genotoxic Response of Unionid Mussel Hemolymph to Hydrogen Peroxide and Polycyclic Aromatic Hydrocarbons. FMBC 15(2):113–125

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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. Aquat Toxicol 31:143–164

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Rigonato J, Mantovani MS, Jordao BQ (2005) Comet assay comparison of different Corbicula fluminea (Mollusca) tissues for the detection of genotoxicity. Gen Mol Biol 28(3):464–468

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Spada L, Annicchiarico C, Cardellicchio N et al (2013) Heavy metals monitoring in the mussel Mytilus galloprovincialis from the Apulian coast (Southern Italy). Mediterranean Mar Sci 14:99–108

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Stankovic S, Jovic M, Stankovic AR, Katsikas L (2012) Heavy Metals in Seafood Mussels. Risks for Human Health. In: Lichtfouse E, Schwarzbauer J, Robert D (eds) Environmental Chemistry for a Sustainable World, Volume 1: Nanotechnology and Health Risk. Springer, Dordrecht, pp 311–373

    Chapter  Google Scholar 

  • Taleb ZM, Benghali S, Kaddour A, Boutiba Z (2007) Monitoring the biological effects of pollution on the Algerian west coast using mussels Mytilus galloprovincialis. Oceanologia 49(4):543–564

    Google Scholar 

  • TUIK (2020) https://data.tuik.gov.tr/Bulten/Index?p=Adrese-Dayali-Nufus-Kayit-Sistemi-Sonuclari-2020-37210

  • Uluturhan E, Kucuksezgin F (2007) Heavy metal contaminants in Red Pandora (Pagellus erythrinus) tissues from the Eastern Aegean Sea, Turkey. Water Res 41:1185–1192

    Article  CAS  Google Scholar 

  • 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. Aquat Toxicol 1:147–157

    Article  CAS  Google Scholar 

  • Vioque-Fernández A, Alves de Almeida E, Ballesteros J et al (2007) Dõnana National Park Survey using Crayfish (Procambarusclarkii) As Bioindicator: esterase inhibition and pollutant levels. Toxicol Lett 168:260–268

    Article  Google Scholar 

  • Vlahogianni T, Dassenakis M, Scoullos MJ, Valavanidis A (2007) Integrated use of biomarkers (superoxide dismutase, catalase and lipid peroxidation) in mussels Mytilus galloprovincialis for assessing heavy metals’ pollution in coastal areas from the Saronikos Gulf of Greece. Mar Pollut Bull 54(9):1361–1367

    Article  CAS  Google Scholar 

  • Wojtal-Frankiewicz A, Bernasińska J, Frankiewicz P et al (2017) The role of environmental factors in the induction of oxidative stress in zebra mussel (Dreissena polymorpha). Aquat Ecol 51:289–306

    Article  CAS  Google Scholar 

  • Yavasoglu A, Ozkan D, Guner A et al (2016) Histopathological and apoptotic changes on marine mussels Mytilus galloprovincialis (Lamark, 1819) following exposure to environmental pollutants. Mar Pollut Bul 109(1):184–191

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Faculty of Science and Art, Department of Biology, Manisa Celal Bayar University, Muradiye-Manisa, Turkey

    Selma Katalay & Melike Merve Ayhan

  2. Faculty of Science, Department of Biology, Ege University, 35100, Bornova-Izmir, Turkey

    Cem Guler, Ceyda Aldag & N. Ulku Karabay Yavasoglu

  3. Center for Drug Research & Development and Pharmacokinetic Applications, Ege University, 35100, Bornova-Izmir, Turkey

    Tunay Kilic & N. Ulku Karabay Yavasoglu

Authors
  1. Selma Katalay
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Melike Merve Ayhan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cem Guler
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ceyda Aldag
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tunay Kilic
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. N. Ulku Karabay Yavasoglu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. Ulku Karabay Yavasoglu.

Ethics declarations

Conflict of interest

The authors declared no conflicts of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Katalay, S., Ayhan, M.M., Guler, C. et al. Cellular Biomarkers in Mytilus galloprovincialis L. (Mediterranean Mussels) from Izmir Bay (Turkey). Bull Environ Contam Toxicol 109, 799–807 (2022). https://doi.org/10.1007/s00128-022-03597-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00128-022-03597-1

Keywords

Search

Navigation