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Heavy metal bioaccumulation, oxidative stress and genotoxicity in African catfish Clarias gariepinus from Orontes river

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Abstract

One of the major problems affecting the ecosystem health is the exposure of heavy metals due to anthropogenic activities. These exposures may induce toxiogenetic damage and carcinogenesis in aquatic organism. DNA damage biomarkers for fish species detect genotoxic parameters for ecological risk assessment. In the present study, the effect of heavy metals (Cr, Cd, Cu, Fe and Mn) on DNA damage and oxidative stress of Clarias gariepinus was examined by Comet assay at Reference site and two different sampling sites of the Orontes River. Moreover, the relationship between DNA damage and physiological response to oxidative stress caused in C. gariepinus was investigated by sampling seasonal water and fish samples for one year. In this study, Cr, Cd and Cu in water column of Orontes River and the concentrations of Fe and Mn in liver tissue of C. gariepinus were highly exceed the maximum permissible limit set by EPA (1999, 2016) WHO (1989) and TEG (2012) that can cause adverse effects on environment health. SOD activities in liver tissues were significantly higher than those in muscle tissues. SOD, CAT activity and MDA levels of both Site 1 and Site 2 at Orontes River were higher than those of the Reference site. In result of the COMET analysis, the highest levels of DNA damage were found at gill and liver tissues in Site 2 (17.746 ± 1.072% T-DNA; 16.014 ± 0.710% T-DNA respectively) at Orontes river. A higher level of DNA damage in gill cells compared to liver cells was observed in all regions of the Orontes River. In Principal component analysis (PCA), the heavy metals Cd, Cr and Cu (in the water column) and MDA in liver and muscle revealed strong contribution to the observed DNA damage that were scattered opposite to each other’s along the principal components. Moreover, correlations between parameters revealed a positive significant relationship between Cd, Cr and Cu in water and DNA damage levels in C. gariepinus. Pearson correlation analysis detected a positive relationship between MDA, CAT and SOD and DNA damage levels in African catfish. Consequently, this study exposed genotoxic damage and oxidative stress of C. gariepinus due to metal pollution in Orontes River and lead to the better understanding of genotoxicty, oxidative stress and heavy metal relationships.

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References

  • Abdel-Moneim AM, Abu El-Saad AM, Hussein HK, Dekinesh SI (2012) “Gill oxidative stress and histopathological biomarkers of pollution impacts in Nile Tilapia from Lake Mariut and Lake Edku, Egypt”. J Aquat Anim Health 24(3):148–160

    CAS  Google Scholar 

  • Ahmad I, Ahmad M (2016) Fresh water fish, Channa punctatus, as a model for pendimethalin genotoxicity testing: A new approach toward aquatic environmental contaminants. Environ Toxicol 31(11):1520–1529

    CAS  Google Scholar 

  • Ahmed MK, Baki MA, Islam MS, Kundu GK, Habibullah-Al-Mamun M, Sarkar SK, Hossain MM (2015) Human health risk assessment of heavy metals in tropical fish and shellfish collected from the river Buriganga, Bangladesh. Environmen Sci Pollut Res 22(20):15880–15890

    CAS  Google Scholar 

  • Amin KA, Hashem KS (2012) Deltamethrin-induced oxidative stress and biochemical changes in tissues and blood of catfish (Clarias gariepinus): antioxidant defense and role of alpha-tocopherol. Vet Res 8(45):2–8

    Google Scholar 

  • Anonymous (2017) The Water Quality Monitoring Report of the Ministry of Environment and Urbanization, The Ministry of Environment and Urbanization, Hatay, Turkey 2017:p 150

  • Anderson MR, Scruton DA, Williams UP, Payne JF (1995) Mercury in fish in the Smallwood Reservoir, Labrador, twenty one years after impoundment. Water Air Soil Pollut 80(1-4):927–930

    CAS  Google Scholar 

  • Arojojoye OA, Oyagbemi AA, Afolabi JM (2018) Toxicological assessment of heavy metal bioaccumulation and oxidative stress biomarkers in Clarias gariepinus from Igbokoda River of South Western Nigeria, Bulletin of Environ. Contam Toxicol 100:765–771

    CAS  Google Scholar 

  • Bano Z, Abdullah S, Ahmad W, Zia MA, Hassan W (2017) Assessment of heavy metals and antioxidant enzyme in different organs of fish from farm, hatchery and Indus River of Pakistan. Pak J Zool 49(6):2227–2233

    CAS  Google Scholar 

  • Baršienė J, Rybakovas A, Lang T, Andreikėnaitė L, Michailovas A (2013) Environmental genotoxicity and cytotoxicity levels in fish from the North Sea offshore region and Atlantic coastal waters. Mar Pollut Bull 68(1-2):106–116

    Google Scholar 

  • Bat L, Öztekin HC, Üstün F (2015) Heavy metal levels in four commercial fishes caught in Sinop coasts of the Black Sea, Turkey. Turk. J Fish Aquat Sci 15(4):399–405

    Google Scholar 

  • Bonanno G, Giudice RL (2010) Heavy metal bioaccumulation by the organs of Phragmites australis (common reed) and their potential use as contamination indicators. Ecol Indic 10(3):639–645

    CAS  Google Scholar 

  • Boyd CE (1990) Water Quality in Ponds for Aquaculture. Birmingham Publishing Co., Birmingham, Alabama

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

    CAS  Google Scholar 

  • Butrimavičienė L, Baršienė J, Greiciūnaitė J, Stankevičiūtė M, Valskienė R (2018) Environmental genotoxicity and risk assessment in the Gulf of Riga (Baltic Sea) using fish, bivalves, and crustaceans. Environ Sci Pollut Res 25(25):24818–24828

    Google Scholar 

  • Cabrera F, Conde B, Flores V (1992) Heavy metals in the surface sediments of the tidal river Tinto (SW Spain). Fresenius Environ Bull 1:400–405

    CAS  Google Scholar 

  • Cavalcante DGSM, Martinez CBR, Sofia SH (2008) Genotoxic effects of Roundup® on the fish Prochilodus lineatus. Mutat Res Gen Toxicol Environ Mutagen 655(1-2):41–46

    CAS  Google Scholar 

  • Chang C, Janzen HH (1996) Long-term fate of nitrogen from annual feedlot manure applications. J Environ Qual 25(4):785–790

    CAS  Google Scholar 

  • Colin N, Porte C, Fernandes D, Barata C, Padrós F, Carrassón M, Maceda-Veiga A (2016) Ecological relevance of biomarkers in monitoring studies of macro-invertebrates and fish in Mediterranean rivers. Sci Tot Environ 540:307–323

    CAS  Google Scholar 

  • Calışkan E (2005) Investigation of Heavy Metal Accumulation in water, sediment and catfish in Asi River. Mustafa Kemal University, Department of Aquaculture, Master Thesis, Antakya

    Google Scholar 

  • Das D, Moniruzzaman M, Sarbajna A, Chakraborty SB (2017) Effect of heavy metals on tissue-specific antioxidant response in Indian major carps. Environ. Sci Pollut R 24(22):18010–18024

    CAS  Google Scholar 

  • De Lemos CT, Rödel PM, Terra NR, de Oliveira NCDA, Erdtmann B (2007) River water genotoxicity evaluation using micronucleus assay in fish erythrocytes. Ecotox Envıron Safe 66(3):391–401

    Google Scholar 

  • Elia AC, Magara G, Righetti M, Dörr AJM, Scanzio T, Pacini N, Prearo M (2017) Oxidative stress and related biomarkers in cupric and cuprous chloride-treated rainbow trout. Environ Sci Pollut Res 24(11):10205–10219

    CAS  Google Scholar 

  • EPA (1989) Assessing human health risks from chemically contaminated fish and shellfish: A guidance manual,” EPA-503/8-89-002. United States Environmental Protection Agency (EPA), Office of Research and Development, Washingto

  • EPA (1999) Environmental Protection Agency, National Recommended Water Quality Criteria-Aquatic Life Criteria, Washington, USA

  • EPA (2016) Environmental Protection Agency, National Recommended Water Quality Criteria, Washington, USA

  • Faria JJ, Dyer JR, Clément RO, Couzin ID, Holt N, Ward AJ, Krause J (2010) A novel method for investigating the collective behaviour of fish: introducing ‘Robofish’. Behav Ecol Sociobiol 64(8):1211–1218

    Google Scholar 

  • Fatima M, Usmani N, Firdaus F, Zafeer MF, Ahmad S, Akhtar K, Hossain MM (2015) In vivo induction of antioxidant response and oxidative stress associated with genotoxicity and histopathological alteration in two commercial fish species due to heavy metals exposure in northern India (Kali) river. Comp Biochem Phys C: Toxicol Pharm 176:17–30

    Google Scholar 

  • Genc E, Sangun MK, Dural M, Can F, Altunhan C (2008) Element concentrations in the swimbladder parasite Anguillicola crassus (nematoda) and its host the European eel, Anguilla anguilla from Asi River (Hatay-Turkey). Environ Monit Assess 141:59–65

    CAS  Google Scholar 

  • Götze S, Matoo OB, Beniash E, Saborowski R, Sokolova IM (2014) Interactive effects of CO2 and trace metals on the proteasome activity and cellular stress response of marine bivalves Crassostrea virginica and Mercenaria mercenaria. Aquat Toxicol 149:65–82

    Google Scholar 

  • Gravato C, Teles M, Oliveira M, Santos MA (2006) Oxidative stress, liver biotransformation and genotoxic effects induced by copper in Anguilla anguilla L.–the influence of pre-exposure to β-naphthoflavone. Chemosphere 65:1821–1830

    CAS  Google Scholar 

  • Greani S, Lourkisti R, Berti L, Marchand B, Giannettini J, Santini J, Quilichini Y (2017) Effect of chronic arsenic exposure under environmental conditions on bioaccumulation,.oxidative stress, and antioxidant enzymatic defenses in wild trout Salmo trutta (Pisces, Teleostei). Ecotoxicol 26:930–941

    CAS  Google Scholar 

  • Hermenean A, Damache G, Albu P, Ardelean A, Ardelean G, Ardelean DP, Kéki S (2015) Histopatological alterations and oxidative stress in liver and kidney of Leuciscus cephalus following exposure to heavy metals in the Tur River, North Western Romania. Ecotoxicol Environ Safe 119:198–205

    CAS  Google Scholar 

  • Javed M, Ahmad I, Usmani N, Ahmad M (2016) Studies on biomarkers of oxidative stress and associated genotoxicity and histopathology in Channa punctatus from heavy metal polluted canal. Chemosphere 151:210–219

    CAS  Google Scholar 

  • Javed M, Ahmad MI, Usmani N, Ahmad M (2017) Multiple biomarker responses (serum biochemistry, oxidative stress, genotoxicity and histopathology) in Channa punctatus exposed to heavy metal loaded waste water. Sci Rep 7(1):1–11

    CAS  Google Scholar 

  • Javed M, Usmani N, Ahmad I, Ahmad M (2015) Studies on the oxidative stress and gill histopatalogy in Channa punctatus of the canal receiving heavy metal-loaded effluent of Kasimpur Thermal Power Plant. Environ Monit Assess 187:4179–4189

    Google Scholar 

  • Jomova K, Valko M (2011) Advances in metal-induced oxidative stress and human disease. Toxicol 283(2-3):65–87

    CAS  Google Scholar 

  • Karakılçık Y, Erkul H (2002) Management of Asi River’. Detay Publications, Ankara, Turkey, p 356

  • Kurelec B (1993) The genotoxic disease syndrome. Mar Environ Res 35:341–348

    Google Scholar 

  • Lenhardt L, Bro R, Zeković I, Dramićanin T, Dramićanin MD (2015) Fluorescence spectroscopy coupled with PARAFAC and PLS DA for characterization and classification of honey. Food Chem 175:284–291

    CAS  Google Scholar 

  • Lin YL (2007) Mesoscale dynamics, vol. 630. Cambridge University Press, Cambridge

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein Measurement with the Folin Phenol Reagent. J Biol Chem 19:265–275

    Google Scholar 

  • Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101(1):13–30

    CAS  Google Scholar 

  • Marcon AE, Ferreira DM, Moura MFV, Campos TFC, Amaral VS, AgnezLima LF, Medeiros SBR (2010) Genotoxic analysis in aquatic environment under influence of cyanobacteria, metal and radioactivity. Chemosphere 81:773–780

    CAS  Google Scholar 

  • Martins M, Costa PM (2017) Chapter 1: The comet assay in aquatic (Eco) genotoxicology using non-conventional model organisms: relevance, constraints and prospects, In: Larramendy ML (ed) Ecotoxicology and Genotoxicology: Non-traditional Aquatic Models, Cambridge University Press, Cambridge, UK., p 1–32

  • Matos LA, Cunha AC, Sousa AA, Maranhão JP, Santos NR, de MC, Gonçalves M, de Alencar MV (2017) The influence of heavy metals on toxicogenetic damage in a Brazilian tropical river. Chemosphere 185:852–859

    CAS  Google Scholar 

  • Mitchelmore CL, Chipman JK (1998) DNA strand breakage in aquatic organisms and the potential value of the comet assay in environmental monitoring. Mutat Res-Fund Mol M 399(2):135–147

    CAS  Google Scholar 

  • Nagarani N, Devi VJ, Kumaraguru AK (2012) Identification of DNA damage in marine fish Therapon jarbua by comet assay technique. J Environ Biol 33(4):699

    CAS  Google Scholar 

  • Nahlik AM, Blocksom KA, Herlihy AT, Kentula ME, Magee TK, Paulsen SG (2019) Use of national-scale data to examine human-mediated additions of heavy metals to wetland soils of the US. Envıron Monıt Assess 191(1):336

    CAS  Google Scholar 

  • Nigro SA, Stirk WA, Van Staden J (2002) Optimising heavy metal adsorbance by dried seaweeds. S Afr J Sci 68(3):333–341

    CAS  Google Scholar 

  • Odemis B, Sangün MK, Büyüktas D (2007) Temporal variations in water quantity and quality of Orontes River Turkey. Asian J Chem 19(1):711–1723

    CAS  Google Scholar 

  • Osman AG, Abuel-Fadl KY, Kloas W (2012) In situ evaluation of the genotoxic potential of the river Nile: II. Detection of DNA strand-breakage and apoptosis in Oreochromis niloticus niloticus (Linnaeus, 1758) and Clarias gariepinus (Burchell, 1822). Mutat Res Gen Toxicol Environ Mut 747(1):14–21

    CAS  Google Scholar 

  • Ozyilmaz G, Tukel SS, Alptekin O (2007) Kinetic properties and storage stability of catalase immobilized on to florisil. Indı J Bıochem Bıo 44:38–43

    CAS  Google Scholar 

  • Pacheco M, Santos MA (2002) Biotransformation, genotoxic, and histopathological effects of environmental contaminants in European eel (Anguilla anguilla L.). Ecotoxicol Environ 53(3):331–347

    CAS  Google Scholar 

  • Padmini E, Geetha BV, Rani MU (2008) Liver oxidative stress of the grey mullet Mugil cephalus presents seasonal variations in Ennore estuary, Braz. J Med Bıol Res 41:951–955

    CAS  Google Scholar 

  • Pastorino P, Elia AC, Caldaroni B, Menconi V, Abete MC, Brizio P, Pizzul E, Prearo M (2020) Oxidative stress ecology in brook trout (Salvelinus fontinalis) from a high-mountain lake (Cottian Alps). Sci Total Environ 715:136946

  • Ploetz E, Laimgruber S, Berner S, Zinth W, Gilch P (2007) Femtosecond stimulated Raman microscopy. Appl Phys B-Lasers 87(3):389–393

    CAS  Google Scholar 

  • Polat F, Akın Ş, Yıldırım A, Dal T (2016) The effects of point pollutants-originated heavy metals (lead, copper, iron and cadmium) on fish living in Yeşilırmak River, Turkey. Toxicol Ind Health 32:1439–1449

    Google Scholar 

  • Romeo M, Giamberini L, Amiard-Triquet C, Amiard JC, Rainboe PS (2013) History of biomarkers. Ecological Biomarkers, Indicators of Ecotoxicological Effects. CRC Press Taylor and Francis Group, Boca Raton London, New York

    Google Scholar 

  • Sevcikova M, Modra H, Slaninova A, Svobodova Z (2011) Metals as a cause of oxidative stress in fish: a review. Vet Med 56(11):537–546

    CAS  Google Scholar 

  • Singh NP, Mccoy MT, Tice RR, Schneider EL (1988) A simple technique for quantitation of low-levels of DNA damage in individual cells, experiment. Cell Res 175:184–191

    CAS  Google Scholar 

  • Sun Y, Oberley LW, Li Y (1988) A simple method for clinical assay of superoxide dismutase. Clin Chem 3413:497–500

    Google Scholar 

  • Tasdemir M, Göksu ZL (2001) Some water quality criteria of Asi River (Hatay). E U J FAS 18(1–2):55–64

    Google Scholar 

  • TEG (2012) Turkish Enviromental Guidelines 2012 Publications of Turkish Foundation of Environment, Ankara, Turkey

  • Turan C, Yalçın S, Turan F, Okur E, Akyurt I (2005) Morphometric comparisons of African catfish, Clarias gariepinus, populations in Turkey. Fol Zool 54(1–2):165–172

    Google Scholar 

  • Türkmen M, Çalışkan E (2011) Seasonal and spatial distributions of the metals in the water from the River Asi in Southern East Mediterranean Area of Turkey. J Black Sea Sci 2(1):35–42

    Google Scholar 

  • UNEP (1984) 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, Rev. 1. UNEP

  • US-EPA (2011) Integrated Risk Information System (IRIS) U.S. Environmental Protection Agency, National Center for Environmental Assessment; Washington, DC

  • Valko MMHCM, Morris H, Cronin MTD (2005) Metals, toxicity and oxidative stress. Curr Med Chem 12(10):1161–1208

    CAS  Google Scholar 

  • WHO (1989) Assessing Human Health Risks from Chemically Contaminated Fish and Shellfish: A Guidance Manual, World Health Organization, Geneva

  • Yalçın Ş, Solak K, Akyurt İ (2001) Certain reproductive characteristics of the catfish (Clarias gariepinus Burchell, 1822) living in the river Asi, Turkey. Turk J Zoo 25:453–460

    Google Scholar 

  • Yılmaz AB, Doğan M (2008) Heavy metals in water and in tissues of himri (Carasobarbus luteus) from Orontes (Asi) River. Turk Envıron Monıt Assess 144(1-3):437–444

    Google Scholar 

  • Yong-Bo T, Cheng-Bin L, Hao-Xue Q (2014) Calculations on polarization properties of alkali metal atoms using Dirac—Fock plus core polarization method. Chin Phys B 23(6):063101

    Google Scholar 

  • Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice Hall Inc, Englewood Cliffs

    Google Scholar 

  • Zheng XQ, Shi YJ, Lu YL, Xu XB (2016) Growth inhibition and DNA damage in the earthworm (Eisenia fetida) exposed to perfluorooctane sulphonate and perfluorooctanoic acid. Chem Ecol 32(2):103–116

    CAS  Google Scholar 

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Acknowledgements

This study was supported by The Scientific and Technological Research Council of Turkey (TUBITAK) (116Y262).

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Authors and Affiliations

  1. Faculty of Marine Science and Technology, Iskenderun Technical University, P.O. Box: 31200, Iskenderun, Hatay, Turkey

    Funda Turan, Meltem Eken & Serpil Karan

  2. Faculty of Arts and Sciences, Hatay Mustafa Kemal University, P.O. Box: 31060, Antakya, Hatay, Turkey

    Gul Ozyilmaz & Haluk Uluca

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  1. Funda Turan
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  2. Meltem Eken
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Correspondence to Funda Turan.

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Turan, F., Eken, M., Ozyilmaz, G. et al. Heavy metal bioaccumulation, oxidative stress and genotoxicity in African catfish Clarias gariepinus from Orontes river. Ecotoxicology 29, 1522–1537 (2020). https://doi.org/10.1007/s10646-020-02253-w

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