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Oxidative and cellular stress as bioindicators for metal contamination in freshwater mollusk Lamellidens marginalis

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Abstract

The concentrations of 14 metals, namely, chromium (Cr), manganese (Mn), cobalt (Co), nickel (Ni), copper (Cu), zinc (Zn), selenium (Se), arsenic (As), strontium (Sr), cadmium (Cd), tin (Sn), antimony (Sb), mercury, (Hg), and lead (Pb), have been studied in freshwater mollusk Lamellidens marginalis collected from Dhimbe reservoir. In addition, also studied the cellular and antioxidative status to assess metal contamination as pollution biomarkers. The levels of all the 14 metals were elevated in different sampling sites of Dhimbe reservoir. The level of metals in the L. marginalis was followed as Mn > Zn > Ni > Sr > Cr > Cu > Hg > Se > Sn > Pb > As > Co > Cd > Sb. The oxidative biomarkers viz. catalase (CAT), superoxide dismutase (SOD), and glutathione-S-transferase (GST); glycolytic enzymes viz. lactate dehydrogenase (LDH) and malate dehydrogenase (MDH); and protein metabolic enzymes viz. aspartate amino transferase (AST), alanine amino transferase (ALT), and lipid peroxidation (LPO) were significantly (p < 0.01) higher, while neurotransmitter enzymes such as acetylcholine esterase (AChE) were significantly inhibited in muscle of L. marginalis (p < 0.01) collected from different sampling sites. Therefore, based on our results, we could recommend that the Dhimbe reservoir is moderately metal contaminated and investigation based on biochemical parameters such as antioxidative enzymes, cellular biomarkers, and AChE are strong indicators for metal contamination; hence, these parameters are successfully applied as reliable biomarkers for monitoring contaminated freshwater ecosystems.

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References

  • Akcha F, Izuel C, Venier P, Budzinski H, Burgeot T, Narbonne JF (2000) Enzymatic biomarker measurement and study of DNA adduct formation in benzo[a]pyrene-contaminated mussels, Mytilus galloprovincialis. Aquat Toxicol 49:269–287

    Article  CAS  Google Scholar 

  • Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 53:1331–1341

    Article  CAS  Google Scholar 

  • Calabrese EJ, Canada AT, Sacco C (1985) Trace elements and public health. Annu Rev Public Health 6:131–146

    Article  CAS  Google Scholar 

  • Casas S, Gonzalez JL, Andral B, Cossa D (2008) Relation between metal concentration in water and metal content of marine mussels (Mytilus galloprovincialis): impact of physiology. Environ Toxicol Chem 27:1543–1552

    Article  CAS  Google Scholar 

  • Casillas E, Meyers M, Ames W (1983) Relationship of serum chemistry values to liver and kidney histopathology in English sole (Parophrys vetulus) after acute exposure to carbon tetrachloride. Aquat Toxicol 3:61–78

    Article  CAS  Google Scholar 

  • Chase ME, Jones SH, Hennigar P, Sowless J, Harding GCH, Freeman K, Wells PG, Krahforst C, Coombs K, Crawford R (2001) Gulf watch: monitoring spatial and temporal patterns of trace metal and organic contaminants in the Gulf of Maine (1991–1997) with the blue mussel Mytilus edulis L. Mar Pollut Bull 42:491–505

    Article  CAS  Google Scholar 

  • Chen MH, Chen CY (1999) Bioaccumulation of sediment bound heavy metals in gray mullet, Liza macrolepis. Mar Pollut Bull 39:239–244

    Article  CAS  Google Scholar 

  • Costa LG (1998) Biochemical and molecular neurotoxicology: relevance to biomarker development, neurotoxicity testing and risk assessment. Toxicol Lett 102-103:417–421

    Article  CAS  Google Scholar 

  • De Almeida EA, Miyamoto S, Bainy ACD, Medeiros MHG, DiMascio P (2004) Protective effect of phospholipid hydroperoxide glutathione peroxidase (PHGPx) against lipid per oxidation in mussels Perna perna exposed to different metals. Mar Pollut Bull 49:386–392

    Article  CAS  Google Scholar 

  • EC (2001) Commission Regulation No. 466/2001 of 8 March 2001. Official Journal of European Communities 1.77/1

  • FAO (1983) Compilation of legal limits for hazardous substance in fish and fishery products (Food and agricultural organization). FAO fishery circular, No. 464. pp. 5–100

  • Ganther HE, Goudie C, Sunde ML, Kopecky MJ, Wagner P, Oh SH (1972) Selenium: relation to decreased toxicity of methyl mercury added to diets containing tuna. Science 175:1122–1124

    Article  CAS  Google Scholar 

  • Geret F, Serafim A, Barreira L, Bebianno MJ (2002) Effect of Cd on antioxidant enzymes in the gills of the clam Ruditapes decussatus. Biomarkers 7:242–256

    Article  CAS  Google Scholar 

  • Ghabbour EA, Shaker M, El-Toukhy A, Abid IM, Davies G (2006) Thermodynamics of metal cation binding by a solid soil-derived humic acid. Binding of Fe(III), Pb(II), and Cu(II). Chem 63:477–483

    CAS  Google Scholar 

  • Giarratano E, Amin OA (2010) Heavy metals monitoring in the southern most mussel farm of the world (Beagle Channel, Argentina). Ecotoxicol Environ Saf 73:1378–1384

    Article  CAS  Google Scholar 

  • Giller E, Schwartz JH (1971) Acetylcholinesterase in identified neurons of the abdominal ganglion of Aplysia californica. J Neurophysiol 34:108–115

    CAS  Google Scholar 

  • Goswami P, Hariharan G, Godhantaraman N, Munuswamy N (2014) An integrated use of multiple biomarkers to investigate the individual and combined effect of copper and cadmium on the marine grren mussel (Perna viridis). J Environ Sci Health A Tox Hazard Subst Environ Eng 49(13):1564–1577

    Article  CAS  Google Scholar 

  • Gul S, Belge-Kuruta E, Yildiz E, Sahan A, Doran F (2004) Pollution correlated modifications of liver antioxidant systems and histopathology of fish (Cyprinidae) living in Seyhan Dam Lake, Turkey. Environ Int 30:605–609

    Article  CAS  Google Scholar 

  • Gupta SK, Singh J (2011) Evaluation of mollusks as sensitive indicators of heavy metal pollution in aquatic system: a review. IIOAB Journal 2(1):49–57

    Google Scholar 

  • Habing WH, Pabst MN, Bjacoby W, Glutathion S (1974) Transferase, the first enzymatic step in mercatpopunc acid formation. J Biol Chem 249:7130–7139

    Google Scholar 

  • Halliwell B (1995) How to characterize an antioxidant—an update. Biochem Soc Symp 61:73–101

    Article  CAS  Google Scholar 

  • Hamer B, Hamer DP, Muller WEG, Batel R (2004) Stress-70 proteins in marine mussel Mytilus galloprovincialis as biomarkers of environmental pollution: a field study. Environ Int 30:873–882

    Article  CAS  Google Scholar 

  • Hanlon RT, Bidwell JP, Tait R (1989) Strontium is required for statolith development and thus normal swimming behaviour of hatchling cephalopods. J Exp Biol 141:187–195

    CAS  Google Scholar 

  • Hestrin S (1949) The reaction of acetyl choline esters and other carboxylic acid derivatives with hydroxylamine and its analytical application. J Bio Chem 180:249–261

    CAS  Google Scholar 

  • Kappus H, Sies H (1981) Toxic drug effects associated with oxygen metabolism: redox cycling and lipid peroxidation. Experientia 37:1233–1241

    Article  CAS  Google Scholar 

  • Karageorgis AP, Nikolaidis NP, Karamanos H, Skoulikidis N (2003) Water and sediment quality assessment of the Axios River and its coastal environment. Cont Shelf Res 23:1929–1944

    Article  Google Scholar 

  • Kumar N, Prabhu AJ, Pal AK, Remya S, Aklakur M, Rana RS, Gupta S, Raman RP, Jadhao SB (2011a) Anti-oxidative and immuno-hematological status of tilapia (Oreochromis mossambicus) during acute toxicity test of endosulfan. Pest Biochem Physiol 99:45–52

    Article  CAS  Google Scholar 

  • Kumar N, Jadhao SB, Chandan NK, Rana RS (2011b) Dietary choline, betaine and lecithin mitigates endosulfan induced stress in Labeo rohita fingerlings. Fish Physiol Biochem 38:989–1000

    Article  Google Scholar 

  • Kumar N, Jadhao SB, Chandan NK, Akhlak M, Rana RS (2012) Methyl donors potentiates growth, metabolic status and neurotransmitter enzyme in Labeo rohita fingerlings exposed to endosulfan and temperature. Fish Physiol Biochem 38(5):1343–1353

    Article  CAS  Google Scholar 

  • Kumar N, Gupta S, Chandan NK, Aklakur M, Pal AK, Jadhao SB (2014a) Lipotropes protect against pathogen-aggravated stress and mortality in low dose pesticide-exposed fish. PLoS One 9(4):e93499

    Article  Google Scholar 

  • Kumar N, Minhas PS, Ambasankar K, Krishnani KK, Rana RS (2014b) Dietary lecithin potentiates thermal tolerance and cellular ctress protection of milk fish (Chanos chanos) reared under low dose endosulfan induced stress. J Therm Biol 46:40–46

    Article  CAS  Google Scholar 

  • Kumar N, Sharma R, Tripathi G, Kumar K, Dalvi RS, Krishna G (2014c) Cellular metabolic, stress and histological response on exposure to acute toxicity of endosulfan in Tilapia (Oreochromis mossambicus). Environ Toxicol 31(1):106–115

  • Kumar N, Ambasankar K, Krishnani KK, Gupta SK, Bhushan S, Minhas PS (2016a) Acute toxicity, biochemical and histopathological responses of endosulfan in Chanos chanos. Ecotoxicol Environ Saf 131:79–88

    Article  CAS  Google Scholar 

  • Kumar N, Ambasankar K, Krishnani KK, Bhushan S, Minhas PS (2016b) Dietary pyridoxine protects against stress and maintains immune-hematological status in Chanos chanos exposed to endosulfan. Basic Clin Pharmacol Toxicol 119(3):297–308

    Article  CAS  Google Scholar 

  • Kumar N, Ambasankar K, Krishnani KK, Kumar P, Akhtar MS, Bhushan S, Minhas PS (2016c) Dietary pyridoxine potentiates thermal tolerance, heat shock protein and protect against cellular stress of milk fish (Chanos chanos) under endosulfan-induced stress. Fish Shellfish Immunol 55:407–414

    Article  CAS  Google Scholar 

  • Kumar N, Ambasankar K, Krishnani KK, Gupta SK, Minhas PS (2016d) Dietary pyridoxine promotes growth and cellular metabolic plasticity of Chanos chanos fingerlings exposed to endosulfan induced stress. Aqua Res. doi:10.1111/are.13042

  • Kumar N, Krishnani KK, Meena KK, Gupta SK, Singh NP (2017a) Oxidative and cellular metabolic stress of Oreochromis mossambicus as biomarkers indicators of trace element contaminants. Chemosphere 171:265–274

    Article  CAS  Google Scholar 

  • Kumar N, Krishnani KK, Kumar P, Jha AK, Gupta SK, Singh NP (2017b) Dietary zinc promotes immuno-biochemical plasticity and protects fish against multiple stresses. Fish Shellfish Immunol 62:184–194

    Article  CAS  Google Scholar 

  • Kumar N, Krishnani KK, Brahmane MP, Gupta SK, Kumar P, Singh NP (2017c) Temperature induces lead toxicity in Pangasius hypophthalmus: An acute test, antioxidative status and cellular metabolic stress. Int J Environ Sci Technol. doi:10.1007/s13762-017-1364-5

  • Kumar N, Krishnani KK, Gupta SK, Singh NP (2017d) Cellular stress and histopathological tools used as biomarkers in Oreochromis mossambicus for assessing metal contamination. Environ Toxicol Pharmacol 49:137–147

  • Lowry OH, Ronebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with folin phenol reagent. JBiol Chem 193:265–276

    CAS  Google Scholar 

  • Mason KE, Young JO (1967) Effectiveness of selenium and zinc in protecting against cadmium induced injury to the rat testes. In: Muth OH (ed) Symposium: selenium in biopmedicine. AVI, West port, Conn, pp 383–394

    Google Scholar 

  • Miller G, Shulaev V, Mitter R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133:481–489

    Article  CAS  Google Scholar 

  • Misra HP, Fridovich I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 247:3170–3175

    CAS  Google Scholar 

  • Mohanty M, Kumar Patra H (2013) Effect of ionic and chelate assisted hexavalent chromium on mung bean seedlings (Vigna radiata L. wilczek. Var k-851) during seedling growth. JSPB 9(2):232–241

    Google Scholar 

  • Muthappa NA, Gupta S, Yengkokpam S, Debnath D, Kumar N, Pal AK, Jadhao SB (2014) Lipotropes promote immunobiochemical plasticity and protect fish against low-dose pesticide-induced oxidative stress. Cell Stress Chaperone 19(1):61–81

    Article  CAS  Google Scholar 

  • Najimi S, Bouhaimi A, Daubeze M, Zekhnini A, Pellerin J, Narbone JF, Moukrim A (1997) Use of acetylcholinesterase in Perna perna and Mytilus galloprovincialis as a biomarker of pollution in Agadir Marine Bay (south of Morocco). Bull Environ Contam Toxicol 58:901–908

    Article  CAS  Google Scholar 

  • NAS-NRC (1974) National Academy of Sciences-National Research Council. Food and nutrition board. Recommended Dietary allowances. National Academic Press, Washington DC

    Google Scholar 

  • Ochoa S (1955) Malic dehydrogenase and ‘malic’ enzyme. In: Coloric SP, Kaplan N (eds) Methods of enzymology, vol I. Academic Press, New York, pp 735–745

    Chapter  Google Scholar 

  • Oner M, Atli G, Canli M (2009) Effects of metal (Ag, Cd, Cr, Cu, Zn) exposures on some enzymatic and non-enzymatic indicators in the liver of Oreochromis niloticus. Bull Environ Contam Toxicol 82:317–321

    Article  Google Scholar 

  • Pandey S, Parvez S, Ansari RA, Ali M, Kaur M, Hayat F, Ahmad F, Raisuddin S (2008) Effects of exposure to multiple trace metals on biochemical, histological and ultrastructural features of gills of a freshwater fish, Channa punctata Bloch. Chem Biol Interact 178:183–192

    Article  Google Scholar 

  • Rainbow PS, Wolowicz M, Fialkowski W, Smith BD, Sokolowski A (2000) Biomonitoring of trace metals in the gulf of gdansk, using mussels (Mytilus trossulus) and barnacles (Balanus improvisus). Wat Res 34:1823–1829

    Article  CAS  Google Scholar 

  • Rajamanickam V, Muthuswamy N (2008) Effect of heavy metals induced toxicity on metabolic biomarkers in common carp (Cyprinus carpio L.) Mj Int J Sci Tech 2(1):192–200

    CAS  Google Scholar 

  • Rocher B, Le Goff J, Peluhet L, Briand M, Manduzio H, Gallois J, Devier MH, Geffard O, Gricourt L, Augagneur S, Budzinski H, Pottier D, Andre V, Lebailly P, Cachot J (2006) Genotoxicant accumulation and cellular defence activation in bivalves chronically exposed to waterborne contaminants from the Seine River. Aquat Toxicol 79:65–77

    Article  CAS  Google Scholar 

  • Roesijadi G, Robinson WE (1994) Metal regulation in aquatic animals: mechanisms of uptake, accumulation, and release. In: Malins DC, Ostrander GK (eds) Aquatic toxicology—molecular, biochemical, and cellular perspectives. Lewis, Boca Raton, p 387

    Google Scholar 

  • Salanki J (1986) Biological monitoring of the state of the environment: bioindicators I.U.B.S. Monograph series No. 1 for I.C.S.U. by I.R.L

  • Sanstead HH (1976) Interaction of cadmium and lead with essential minerals. In: Nordberg GF (ed) Effects and dose-response relationships of toxic metals. Elsevier, Amsterdam, pp 511–525

    Google Scholar 

  • Soreq H, Seidman S (2001) Acetylcholinesterase-new roles for an old actor. Nat Neurosci 2:295–303

    Google Scholar 

  • Stohs SJ, Hagchi D, Hassoun E, Bagshi M (2000) Oxidative mechanisms in the toxicity of chromium and cadmium ions. J Environ Pathol Toxicol Oncol 19:201–213

    CAS  Google Scholar 

  • Takahara S, Hamilton BH, Nell JV, Kobra TY, Ogura Y, Nishimura ET (1960) Hypocatalesemia, a new generis carrier state. J Clinical Investig 29:610–619

    Article  Google Scholar 

  • Torres MA, Dangl JL, Jones JDG (2002) Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proc Natl Acad Sci U S A 99:517–522

    Article  CAS  Google Scholar 

  • Uchiyama M, Mihara M (1978) Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal Biochem 86:271–278

    Article  CAS  Google Scholar 

  • Underwood EJ (1977) Trace elements in human and animal nutrition, 4th edn. Academic, New York

    Google Scholar 

  • USFDA (1993a) Food and drug administration. Guidance document for chromium in shellfish. DHHS/ PHS/ FDA/ CFSAN/ Office of Seafood, Washington, DC

    Google Scholar 

  • USFDA (1993b) Food and Drug Administration. Guidance document for arsenic in shellfish. DHHS/PHS/FDA/CFSAN/Office of Seafood, Washington, DC

    Google Scholar 

  • Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M (2006) Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol Environ Saf 64:178

    Article  CAS  Google Scholar 

  • Velmurugan B, Selvanayagam M, Cengiz EI, Uysal E (2008) Levels of transaminases, alkaline phosphatase, and protein in tissues of Clarias gariepienus fingerlings exposed to sublethal concentrations of cadmium chloride. Environ Toxicol 23(6):672–678

    Article  CAS  Google Scholar 

  • Vlahogianni TH, Valavanidis A (2007) Heavy-metal effects on lipid peroxidation and antioxidant defense enzymes in mussels Mytilus galloprovincialis. Chem Ecol 23(5):361–371

    Article  CAS  Google Scholar 

  • Walker CH, Hopkin SP, Sibly RM, Peakall DB (2001) Principles of ecotoxicology, 2nd edn. Taylor and Francis, London

    Google Scholar 

  • Wootton IDP (1964) Microanalysis in medical biochemistry. J & A Churchill Ltd., London, pp 101–103

    Google Scholar 

  • Wroblewski L, LaDue JS (1955) Lactic dehydrogenase activity in blood. Proc Soc Exp Biol Med 90:210–213

    Article  CAS  Google Scholar 

  • Wu JF, Yu ZM, Song XX, Wang Y (2006) Response of integrated biomarkers of fish (Lateolabrax japonicus) exposed to benzo[a]-pyrene and sodium dodecylbenzene sulfonate. Ecotoxicol Environ Saf 65:230–236

    Article  CAS  Google Scholar 

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Acknowledgements

The authors express sincere gratitude to Director, ICAR-National Institute of Abiotic Stress Management, Baramati, Pune, for providing all the facility to conduct the present study. We also would like to thank Ms. Supriya, Mrs. Yogita, Ms. Sonam, and Mr. Yuvraj Sanas for their technical assistance.

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  1. ICAR-National Institute of Abiotic Stress Management, Malegaon, Baramati, Pune, 413 115, India

    Neeraj Kumar, Kishore Kumar Krishnani & Narendra Pratap Singh

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  1. Neeraj Kumar
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Kumar, N., Krishnani, K.K. & Singh, N.P. Oxidative and cellular stress as bioindicators for metal contamination in freshwater mollusk Lamellidens marginalis . Environ Sci Pollut Res 24, 16137–16147 (2017). https://doi.org/10.1007/s11356-017-9266-0

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