Abstract
Coastal areas, such as bays, estuaries, and harbors, are heavily polluted since these areas are the settlements to which toxic chemicals from industrial and domestic wastes are discharged. The genetic damage was evaluated using bioindicator mussel Mytilus galloprovincialis caused by toxic chemicals (metals and polycyclic aromatic hydrocarbons) in İzmir and Çandarlı Bays (the Eastern Aegean Sea) through comet assay. Three sampling sites from the two bays were selected and the study was conducted during the spring and autumn periods. The highest levels of DNA damage expressed as %Tail-DNA were observed in İzmir Bay (34.60 % Tail-DNA) in the spring. Analysis of the correlation between PAHs and metals in mussels and %T-DNA in the hemolymph and gill cells showed a statistically significant positive correlation between %T-DNA and ∑PAH, chromium (p < 0.05). This study determined the pollution level of the İzmir and Çandarlı Bays by using the DNA damage to the mussel, which can identify the effects of environmental pollutants at the cellular levels. These results confirm that comet assay can be used to determine the temporal and spatial differences of DNA damage, and as a suitable tool for the measurement of genotoxicity in regions with low pollutant concentrations.
Similar content being viewed by others
References
Akcha F, Burgeot T, Narbonne JF, Garrigues P (2003) PAHs: An Ecotoxicological Perspective. Metabolic Activation of PAHs. In: Douben PET (ed) Role of DNA Adduct Formation in Induced Carcinogenesis, Wiley, pp 65–79
Almeida C, Pereira C, Gomes T, Bebianno MJ, Cravo A (2011) DNA damage as a biomarker of genotoxic contamination in Mytilus galloprovincialis from the South coast of Portugal. J Environ Monitor 13:2559–2567
Almeida C, Pereira CG, Gomes T, Cardoso C, Bebianno MJ, Cravo A (2013) Genotoxicity in two bivalve species from a coastal lagoon in the south of Portugal. Mar Environ Res 89:29–38
Ameur WB, de Lapuente J, El Megdiche Y, Barhoumi B, Trabelsi S, Camps L, Serret J, Ramos-López D, Gonzalez-Linares J, Driss MR, Borràs M (2012) Oxidative stress, genotoxicity and histopathology biomarker responses in mullet (Mugil cephalus) and sea bass (Dicentrarchus labrax) liver from Bizerte Lagoon (Tunisia). Mar Pollut Bull 64:241–251
Andreatis J, Papadopoulou C (1982) A study of the distribution of chromium, cobalt, antimony and zinc in the edible mollusc Meretrix chitane from the Aegean Sea. VIth Rapp Comm Int Mer Médit CIESM, Cannes France, pp 299-303
Besada V, Andrade JM, Schultze F, Gonzalez JJ (2011) Comparison of the 2000 and 2005 spatial distributions of heavy metals in wild mussels from the North-Atlantic Spanish Coast. Ecotoxicol Environ Saf 74:373–381
Bhuvaneshwarı R, Babu Rajendran R, Kumar K (2013) Induction of DNA Damage and GADD45β gene Mutation in Zebra fish (Danio rerio) due to Environmentally Relevant Concentrations of Organochlorine Pesticides and Heavy Metals. Int J Environ Res 7(1):219–224
Binelli A, Cogni D, Parolini M, Riva C, Provini A (2009) In vivo experiments for the evaluation of genotoxic and cytotoxic effects of Triclosan in Zebra mussel hemocytes. Aquat Toxicol 91:238–244
Brandão F, Cappello T, Raimundo J, Santos MA, Maisano M, Mauceri A, Pacheco M, Pereira P (2015) Unravelling the mechanisms of mercury hepatotoxicity in wild fish (Liza aurata) through a triad approach: bioaccumulation, metabolomic profiles and oxidative stress. Metallomics 7(9):1352–1363
Brunelli E, Mauceri A, Maisano M, Bernabò I, Giannetto A, De Domenico E, Corapi B, Tripepi S, Fasulo S (2011) Ultrastructural and immunohistochemical investigation on the gills of the teleost, Thalassoma pavo L. exposed to cadmium. Acta Histochem 113(2):201–213
Cappello T, Maisano M, D’Agata A, Natalotto A, Mauceri A, Fasulo S (2013a) Effects of environmental pollution in caged mussels (Mytilus galloprovincialis). Mar Environ Res 91:52–60
Cappello T, Mauceri A, Corsaro C, Maisano M, Parrino V, Lo Paro G, Messina G, Fasulo S (2013b) Impact of environmental pollution on caged mussels Mytilus galloprovincialis using NMR-based metabolomics. Mar Pollut Bull 77(1-2):132–139
Cappello T, Maisano M, Giannetto A, Parrino V, Mauceri A, Fasulo S (2015) Neurotoxicological effects on marine mussel Mytilus galloprovincialis caged at petrochemical contaminated areas (eastern Sicily, Italy): 1H NMR and immunohistochemical assays. Comp Biochem Physiol C Toxicol Pharmacol 169:7–15
Cappello T, Brandão F, Guilherme S, Santos MA, Maisano M, Mauceri A, Canário J, Pacheco M, Pereira P (2016) Insights into the mechanisms underlying mercury-induced oxidative stress in gills of wild fish (Liza aurata) combining (1)H NMR metabolomics and conventional biochemical assays. Sci Total Environ 548–549:13–24
Cevik U, Damla N, Kobyaa AI, Bulut VN, Duran C, Dalgıc G, Bozacı R (2008) Assessment of metal element concentrations in mussel (M. galloprovincialis) in Eastern Black Sea, Turkey. J Hazard Mater 160:396–401
Ciacci C, Barmo C, Gallo G, Maisano M, Cappello T, D‘Agata A, Leonzio C, Mauceri A, Fasulo S, Canesi L (2012) Effects of sub-lethal, environmentally relevant concentrations of hexavalent chromium in the gills of Mytilus galloprovincialis. Aquat Toxicol 120–121:109–118
Claxton LD, Houk VS, Hughes TJ (1998) Genotoxicity of industrial wastes and effluents. Mutat Res 410:237–243
Crowe TP, Smith EL, Donkin P, Barnaby DL, Rowland SJ (2004) Measurements of sub-lethal effects on individual organisms indicates community level impacts of pollution. J Appl Ecol 41:114–123
D’Agata A, Cappello T, Maisano M, Parrino V, Giannetto A, Brundo MV, Ferrante M, Mauceri A (2014) Cellular biomarkers in the mussel Mytilus galloprovincialis (Bivalvia: Mytilidae) from Lake Faro (Sicily, Italy). Ital J Zool 81(1):43–54
Dailianis S, Tsarpali V, Melas K, Karapanagioti HK, Manariotis ID (2014) Aqueous phenanthrene toxicity after high-frequency ultrasound degradation. Aquat Toxicol 147:32–40
Debetto P, Luciani S (1988) Toxic effects of chromium on cellular metabolism. Sci Total Environ 71:365–367
FAO/WHO (2010) Joint FAO/WHO Expert Committee on Food Additives Report of the Seventy-Second Meeting of JECFA in the WHO Technical Report Series, Rome Italy, pp 3–13
Fasulo S, Iacono F, Cappello T, Corsaro C, Maisano M, D’Agata A, Giannetto A, De Domenico E, Parrino V, Lo Paro G, Mauceri A (2012a) Metabolomic investigation of Mytilus galloprovincialis (Lamarck 1819) caged in aquatic environments. Ecotoxicol Environ Saf 84:139–146
Fasulo S, Maisano M, Sperone E, Mauceri A, Bernabò I, Cappello T, D’Agata A, Tripepi S, Brunelli E (2012b) Toxicity of Foroozan crude oil to ornate wrasse (Thalassoma pavo, Osteichthyes, Labridae): ultrastructure and cellular biomarkers. Ital J Zool 79(2):182–199
Fernandez-Tajes J, Florez F, Pereira S, Rabade T, Laffon B, Mendez J (2011) Use of three bivalve species for biomonitoring a polluted estuarine environment. Environ Monit Assess 172:301–317
Ferrarese E, Andreottola G, Oprea IA (2008) Remediation of PAH contaminated sediments by chemical oxidation. J Hazard Mater 152:128–139
Galgani F, Martínez-Gómez C, Giovanardi F, Romanelli G, Caixach J, Cento A et al (2011) Assessment of polycyclic aromatic hydrocarbon concentrations in mussels (Mytilus galloprovincialis) from the Western basin of the Mediterranean Sea. Environ Monit Assess 177:289–300
Gichner T, Mukherjee A, Veleminsky J (2006) DNA staining with the fluorochromes EtBr, DAPI and YOYO-1 in the comet assay with tobacco plants after treatment with ethyl methanesulphonate, hyperthermia and DNase-I. Mutat Res 605:17–21
Halldórsson HP, Ericson G, Svavarsson J (2004) DNA strand breakage in mussels (Mytilus edulis L.) deployed in intertidal and subtidal zone in Reykjavík harbour. Mar Environ Res 58:763–767
Héberger K, Kolarevic S, Kracun-Kolarevic M, Sunjog K, Gacic Z, Kljajic Z, Milena Mitric M, Vukovic-Gaci B (2014) Evaluation of single-cell gel electrophoresis data: Combination of variance analysis with sum of ranking differences. Mutat Res 771:15–22
JECFA (2005). Summary and Conclusions. Joint FAO/WHO Expert Committee on Food Additives. Sixty-fourth meeting, 8-17 February, Rome, ftp://ftp.fao.org/es/esn/jecfa/jecfa64_summary.pdf
Jha AN (2008) Ecotoxicological applications and significance of the comet assay. Mutagenesis 23(3):207–221
Karacik B, Okay OS, Henkelmann B, Bernhoft S, Schramm KW (2009) Polycyclic aromatic hydrocarbons and effects on marine organisms in the Istanbul Strait. Environ Int 35:599–606
Kennish MJ (1998) Pollution in Estuarine and Marine Environments, Pollution Impacts on Marine Biotic Communities. Institute of Marine and Coastal Sciences, Rutgers University, New Jersey, 310p
Kleinjans JCS, Van Schooten FJ (2002) Ecogenotoxicology: the evolving field. Environ Toxicol Phar 11:173–179
Klobucar GIV, Pavlica M, Stambuk A, Hylland K, Pavlica M (2008) Detection of DNA damage in haemocytes of Mytilus galloprovincialis in the coastal ecosystems of Kastela and Trogir Bays, Croatia. Sci Total Environ 405:330–337
Kocatas A, Ergen Z, Katağan T, Önen M, Çınar ME, Öztürk B, Doğan A (1997) The Effects of the Pollution on the Distribution of Benthos in the Bay of Izmir. Marine Research in the Izmir Bay, September 17-19 Workshop Abstract, pp 90
Koprucu K (2007) Turkiye su urunleri uretiminin durumu ve değerlendirilmesi. Türk Tarım Dergisi 178:22–28 (In Turkish)
Kucuksezgin F (2011) The Water Quality of Izmir Bay: A Case Study. R Environ Contam T 211:1–24
Kucuksezgin F, Kacar A, Kucuksezgin G, Uluturhan E (2010) Monitoring metal contamination levels and fecal pollution in clam (Tapes decussatus) collected from Izmir Bay (Turkey). Environ Monit Assess 162(1-4):407–415
Kucuksezgin F, Pazı İ, Yucel-Gier G, Akçalı B, Galgani F (2013) Monitoring of heavy metal and organic compound levels along the Eastern Aegean coast with transplanted mussels. Chemosphere 93:1511–1518
Kumaravel TS, Jha AN (2006) Reliable Comet assay measurements for detecting DNA damage induced by ionising radiation and chemicals. Mutat Res 605:7–16
Langston WJ, Burt GR, Chesman BS (2007) Feminisation of male clams Scrobicularia plana from estuaries in Southwest UK and its induction by endocrine-disrupting chemicals. Marine Ecological Progress Series 333:173–184
Lök A, Acarlı S, Serdar S, Köse A, Yıldız H (2007) Growth and mortality of Mediterranean mussel Mytilus galloprovincialis Lam., 1819, in relation to size on longline in Mersin Bay, Izmir (Turkey–Aegean Sea). Aquac Res 38:819–826
Luch A, Baird WM (2005) In: Luch A (ed) Carcinogenic Effects Polycyclic Aromatic Hydrocarbons, Metabolic Activation and Detoxification of Polycyclic Aromatic Hydrocarbons. Imperial College Pres, USA, pp 19–96
Maanan M (2007) Biomonitoring of heavy metals using M. galloprovincialis in Safi coastal waters, Morocco. Environ Toxicol 22:525–531
MAFF (1995) Monitoring and surveillance of nonradioactive contaminants in the aquatic environment and activities regulating the disposal of wastes at sea. Directorate of Fisheries Research, Lowestoft, Aquatic environment monitoring report, 44
Magi E, Bianco R, Ianni C, Di Carro M (2002) Distribution of polycyclic aromatic hydrocarbons in the sediments of the Adriatic Sea. Environ Pollut 119:91–98
Martins M, Costa PM, Ferreira AM, Costa MH (2013) Comparative DNA damage and oxidative effects of carcinogenic and non-carcinogenic sediment-bound PAHs in the gills of a bivalve. Aquat Toxicol 142–143:85–95
Monserrat JM, Martínez PE, Laura AG, Amado LL, Martins CMG, Pinho GLL, Chaves IS, Cravo MF, Lima JV, Bianchini A (2007) Pollution biomarkers in estuarine animals: Critical review and new perspectives. Comp Biochem Phy C 146:221–234
Moore MN, Depledge MN, Readman JW, Leonard DRP (2004) An integrated biomarker-based strategy for ecotoxicological evaluation of risk in environmental management. Mutat Res 552:247–268
Narbonne JF, Djomo JE, Ribera D, Ferrier V, Garrigues P (1999) Accumulation kinetics of polycyclic aromatic hydrocarbons adsorbed to sediment by the mollusk Corbicula fluminea. Ecotox Environ Safe 42:1–8
Neser G, Unsalan D, Tekogul N, Stuer-Lauridsen F (2008) The ship breaking industry in Turkey: environmental, safety and health issues. J Clean Prod 16:350–358
Official Gazette (2005) TC Ministery of Forestry and Water Affairs. Su Ürünleri Yönetmeliği No: 22223 (In Turkish)
Official Gazette (2014) TC Ministery of Forestry and Water Affairs. Hayvan Deneyleri Etik Kurullarının Çalışma Usul ve Esaslarına Dair Yönetmelik 15 February, No: 28914 (In Turkish)
Okay OS, Karacık B, Güngördü A, Ozmen M, Yılmaz A, Koyunbaba NC, Yakan SD, Korkmaz V, Henkelmann B, Schramm KW (2014) Micro-organic pollutants and biological response of mussels in marinas and ship building/breaking yards in Turkey. Sci Total Environ 496:165–178
Orbea A, Cajaraville MP (2006) Peroxisome proliferation and antioxidant enzymes in transplanted mussels of four Basque estuaries with different levels of poly-cyclic aromatic hydrocarbon and polychlorinated biphenyl pollution. Environ Toxicol Chem 25:1616–1626
Parlak H, Katalay S, Büyükisik B (1999) Accumulation and Loss of Chromium by Mussels (M. galloprovincialis). B Environ Contam Tox 62:286–292
Petridis P, Jha AN, Langston WJ (2009) Measurements of the genotoxic potential of (xeno-) oestrogens in the bivalve mollusc Scrobicularia plana, using the Comet assay. Aquat Toxicol 94:8–15
Phillips DJH, Rainbow PS (1993) Biomonitoring of Aquatic trace Contaminants. Chapman and Hall, London
Qiao M, Wang C, Huang S, Wang D, Wang Z (2006) Composition, sources, and potential toxicological significance of PAHs in the surface sediments of the Meiliang Bay. Taihu Lake, China. Environ Int 32(1):28–33
Rank J, Jensen K, Jespersen PH (2005) Monitoring DNA damage in indigenous blue mussels (Mytilus edulis) sampled from coastal sites in Denmark. Mutat Res 585:33–42
Romeo M, Frasila C, Gnassia-Barelli M, Damiens G, Micu D, Mustata G (2005) Biomonitoring of trace metals in the Black Sea (Romania) using mussels Mytilus galloprovincialis. Water Res 39:596–604
Sponza D, Karaoğlu N (2002) Environmental geochemistry and pollution studies of Aliaga metal industry district. Environ Int 27(7):541–553
Steinert S, Streib-Montee R, Leather JM, Chadwick DB (1998) DNA damage in mussels at sites in San Diego Bay. Mutat Res Fund Mol M 399(1):65–85
Ucuncuoglu E, Arli O, Eronat AH (2006) Evaluating the impact of coastal land uses on water-clarity conditions from Landsat TM/ETM+ imagery: Candarli Bay, Aegean Sea. Int J Remote Sens 27(17):3627–3643
UNEP/FAO/IOC/IAEA (1984a) RSRM 7 Sampling of selected marine organisms and sample preparation for trace metal analysis. Reference Methods for Marine Pollution Studies No. 7 Rev. 2, UNEP, 15p
UNEP/FAO/IOC/IAEA (1984b) RSRM 11 Determination of total cadmium, zinc, lead and copper in selected marine organisms by flameless atomic absorption spectrophotometry. Reference Methods for Marine Pollution Studies No. 11, UNEP, 18p
UNEP/FAO/IOC/IAEA (1984c) RSRM 8 Determination of total mercury in selected marine organism by cold vapour atomic absorption spectrophotometry. Reference Methods for Marine Pollution Studies No. 8 Rev. 1 UNEP, 13p
UNEP/FAO/IOC/IAEA (1993) RSRM 6 Guidelines for monitoring chemical contaminants in the sea using marine organisms. Reference Methods for Marine Pollution Studies No. 6 UNEP, 28p
Valverde M, Rojas E (2009) Environmental and occupational biomonitoring using the Comet assay. Mutat Res 681:93–109
Wang G, Lu Y, Han J, Luo W, Shi Y, Wang T, Sun Y (2010) Hexachlorobenzene sources, levels and human exposure in the environment of China. Environ Int 36:122–130
Wenzl T, Simon R, Anklam E, Kleiner J (2006) Analytical methods for polycyclic aromatic hydrocarbons (PAHs) in food and the environment needed for new food legislation in the European Union. Trends Anal Chem 25:716–725
Wogan GN, Hecht SS, Felton JS, Conney AH, Loeb LA (2004) Environmental and chemical carcinogenesis. Semin Cancer Biol 14:473–486
Yakan SD, Henkelmann B, Schramm KW, Okay OS (2013) Bioaccumulation—Depuration kinetics and effects of phenanthrene on Mediterranean mussel (Mytilus galloprovincialis). J Environ Sci Heal A 48:1037–1046
Yang F, Zhang Q, Guo H, Zhang S (2010) Evaluation of cytotoxicity, genotoxicity and teratogenicity of marine sediments from Qingdao coastal areas using in vitro fish cell assay, comet assay and zebrafish embryo test. Toxicol in Vitro 24:2003–2011
Acknowledgements
This study was supported by The Scientific and Technological Research Council of Turkey (Project number: TUBITAK 113Y540).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Cinta Porte
Rights and permissions
About this article
Cite this article
Kacar, A., Pazi, I., Gonul, T. et al. Marine pollution risk in a coastal city: use of an eco-genotoxic tool as a stress indicator in mussels from the Eastern Aegean Sea. Environ Sci Pollut Res 23, 16067–16078 (2016). https://doi.org/10.1007/s11356-016-6783-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-016-6783-1