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The Effects of Salinity and Salinity+Metal (Chromium and Lead) Exposure on ATPase Activity in the Gill and Intestine of Tilapia Oreochromis niloticus

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Abstract

Freshwater organisms are highly sensitive to increases in salinity because they causes serious osmoregulation problems. Salinity of inland waters can be increased as a result of anthropogenic activities. In this study, freshwater fish Oreochromis niloticus were exposed individually to increased salinities (0, 2, and 8 ppt) alone and salinity+metal [1 μg/mL chromium (Cr) or lead (Pb) exposure at 2 and 8 ppt] exposures for different time periods (1, 7, and 14 days) to investigate the response of Na+/K+-ATPase and Mg2+-ATPase in the osmoregulatory tissues (gill and intestine). Results showed that enzyme activity varied depending on salinity, tissue, metal, and exposure duration. Metal levels in controls and salinity-exposed groups were lower than the detection limit, although significant Cr and Pb accumulation occurred in the salinity+metal combination groups. In salinity-exposed groups, there were increasing trends in the enzyme activity, whereas there were decreasing trends in the metal+salinity groups. Gill ATPases were more affected by the exposure conditions compared with intestine ATPases. Results showed that salinity+metal exposure both played significant roles on ATPase activities in the osmoregulatory tissues, although the alterations in the activity were mostly insignificant supporting compensation mechanisms. Results also suggest that the osmoregulation of freshwater fish should be investigated in toxicity- monitoring programs in inland waters.

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References

  • Adeyemi JA, Deaton LE, Pesacreta TC, Klerks PL (2012) Effects of copper on osmoregulation in sheepshead minnow, Cyprinodon variegatus acclimated to different salinities. Aquat Toxicol 109:111–117

    Article  CAS  Google Scholar 

  • Alves LC, Wood CM (2006) The chronic effects of dietary lead in freshwater juvenile rainbow trout (Onchorhynchus mykiss) fed increased calcium diets. Aquat Toxicol 78:217–232

    Article  CAS  Google Scholar 

  • Atkinson A, Gatemby AO, Lowe AG (1973) The determination of inorganic orthophosphate in biological systems. Biochim Biophys Acta 320:195–204

    Article  CAS  Google Scholar 

  • Atli G, Canli M (2007) Enzymatic responses to metal exposures in a freshwater fish Oreochromis niloticus. Comp Biochem Physiol C Toxicol Pharmacol 145:282–287

    Article  Google Scholar 

  • Atli G, Canli M (2010) Response of antioxidant system of freshwater fish Oreochromis niloticus to acute and chronic metal (Cd, Cu, Cr, Zn, Fe) exposures. Ecotoxicol Environ Saf 73:1884–1889

    Article  CAS  Google Scholar 

  • Atli G, Canli M (2011) Alterations in ion levels of freshwater fish Oreochromis niloticus following acute and chronic exposures to five heavy metals. Turk J Zool 35(5):725–736

    CAS  Google Scholar 

  • Atli G, Canli M (2012) Metals (Ag+, Cd2+, Cr6+) affect ATPase activity in the gill, kidney and muscle of freshwater fish Oreochromis niloticus following acute and chronic exposures. Environ Toxicol. doi:10.1002/tox.20766

  • Avella M, Berhaut J, Bornancin M (1993) Salinity tolerance of two tropical fishes, Oreochromis aureus and O. niloticus. I. Biochemical and morphological changes in the gill epithelium. J Fish Biol 42:243–254

    Article  CAS  Google Scholar 

  • Ay Ö, Kalay M, Tamer L, Canli M (1999) Copper and lead accumulation in tissues of a freshwater fish Tilapia zillii and its effects on the branchial Na, K-ATPase activity. Bull Environ Contam Toxicol 62:160–168

    Article  CAS  Google Scholar 

  • Basha PS, Rani AU (2003) Cadmium-induced antioxidant defense mechanism in freshwater teleost Oreochromis mossambicus (Tilapia). Ecotoxicol Environ Saf 56:218–221

    Article  CAS  Google Scholar 

  • Bianchini A, Grosell M, Gregory SM, Wood CM (2002) Acute silver toxicity in aquatic animals is a function of sodium uptake rate. Environ Sci Technol 36:1763–1766

    Article  CAS  Google Scholar 

  • Blanchard J, Grosell M (2006) Copper toxicity across salinities from freshwater to seawater in the euryhaline fish Fundulus heteroclitus: is copper an ionoregulatory toxicant in high salinities? Aquat Toxicol 80:131–139

    Article  CAS  Google Scholar 

  • Bury NR, Shaw J, Glover C, Hogstrand C (2002) Derivation of a toxicity-based model to predict how water chemistry influences silver toxicity to invertebrates. Comp Biochem Physiol C Toxicol Pharmacol 133:259–270

    Article  CAS  Google Scholar 

  • Canli M, Stagg RM (1996) The effects of in vivo exposure to cadmium, copper, and zinc on the activities of gill ATPases in the Norway lobster Nephrops norvegicus. Arch Environ Contam Toxicol 31:491–501

    Article  Google Scholar 

  • Carfagna MA, Ponsler GD, Muhoberac BB (1996) Inhibition of ATPase activity in rat synaptic plasma membranes by simultaneous exposure to metals. Chem Biol Interact 100:53–65

    Article  CAS  Google Scholar 

  • Choi CY, An KW (2008) Cloning and expression of Na+/K+-ATPase and osmotic stress transcription factor 1 mRNA in black porgy, Acanthopagrus schlegeli during osmotic stress. Comp Biochem Physiol B Biochem Mol Biol 149:91–100

    Article  Google Scholar 

  • Cioni C, De Merich D, Cataldi E, Cataudella S (1991) Fine structure of chloride cells in freshwater- and seawater-adapted Oreochromis niloticus (Linnaeus) and Oreochromis mossambicus (Peters). J Fish Biol 91(39):197–209

    Article  Google Scholar 

  • Dethloff GM, Schlenk D, Khan S, Bailey HC (1999) The effects of copper on blood and biochemical parameters of rainbow trout (Oncorhynchus mykiss). Arch Environ Contam Toxicol 36:415–423

    Article  CAS  Google Scholar 

  • Grosell M, Nielsen C, Bianchini A (2002) Sodium turnover rate determines sensitivity to acute copper and silver exposure in freshwater animals. Comp Biochem Physiol C Toxicol Pharmacol 133:287–303

    Article  Google Scholar 

  • Haque MS, Roy SK, Shahjahan M (2011) Arsenic impairs the effect of low temperature on the regulation of Na(+)-K(+)-ATPase activity in skeletal muscle of fish (Channa punctata). Turk J Fish Aquat Sci 11:485–489

    Article  Google Scholar 

  • Heath AG (1987) Water pollution and fish physiology. CRC Press, Boca Raton

    Google Scholar 

  • Hogstrand C, Ferguson EA, Galvez F, Shaw R, Webb NA, Wood CM (1999) Physiology of acute silver toxicity in the starry flounder (Platichthys Stellatus) in seawater. J Comp Physiol B 169:461–473

    Article  CAS  Google Scholar 

  • Jürss K, Bittorf T, Vökler T, Wacke R (1984) Biochemical investigations into the influence of environmental salinity on starvation of the tilapia, Oreochromis mossambicus. Aquaculture 40:171–182

    Article  Google Scholar 

  • Kalay M, Canli M (2000) Elimination of essential (Cu, Zn) and non-essential (Cd, Pb) metals from tissues of a freshwater fish Tilapia zilli. Turk J Zool 24:429–436

    CAS  Google Scholar 

  • Kamal AHMM, Mair GC (2005) Salinity tolerance in superior genotypes of tilapia, Oreochromis niloticus, Oreochromis mossambicus and their hybrids. Aquaculture 247:189–201

    Article  Google Scholar 

  • Kaushal SS, Groffman PM, Likens GE, Bet KT, Stack WP, Kelly VR et al (2005) Increased salinization of fresh water in the northeastern United States. Proc Natl Acad Sci USA 102:13517–13520

    Article  CAS  Google Scholar 

  • Kinne-Saffran E, Schultz H, Scholermann B, Girard D, Kine R (1986) Effect of cadmium on epithelial transport systems in Squalus acanthias: studies with isolated plasma membrane vesicles. Bull Mount Desert Isl Lab 26:15–17

    Google Scholar 

  • Kramer HJ, Gonick HC, Lu E (1986) In vitro inhibition of Na+-K+-ATPase by trace metals: relation to renal and cardiovascular damage. Nephron 44:329–336

    Article  CAS  Google Scholar 

  • Li ZH, Li P, Randak T (2011) Evaluating the toxicity of environmental concentrations of waterborne chromium (VI) to a model teleost, Oncorhynchus mykiss: a comparative study of in vivo and in vitro. Comp Biochem Physiol C Toxicol Pharmacol 153:402–407

    Article  Google Scholar 

  • Lin CH, Lee TH (2005) Sodium or potassium ions activate different kinetics of gill Na, K-ATPase in three seawater- and freshwater-acclimated euryhaline teleosts. J Exp Zool 303:57–65

    Article  Google Scholar 

  • Lionetto MG, Giordano ME, Vilella S, Schettino T (2000) Inhibition of eel enzymatic activities by cadmium. Aquat Toxicol 48:561–571

    Article  CAS  Google Scholar 

  • Loretz CA (1995) Electrophysiology of ion transport in the teleost intestinal cells. In: Wood CM, Shuttleworth TJ (eds) Cellular and molecular approaches to fish ionic regulation. Academic Press, Toronto, pp 25–56

    Google Scholar 

  • Lorz HW, McPherson B (1976) Effects of copper or zinc in fresh water on the adaptation to sea water and ATPase activity, and the effects of copper on migratory disposition of Coho Salmon (Onchorhynchus kisutch). J Fish Res Board Can 33:2023–2030

    CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr NJ, Randall RJ (1951) Protein measurements with the folin phenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  • Marshall WS, Grosell M (2005) Ion transport, osmoregulation and acid–base balance. In: Evans D, Claiborne JB (eds) The physiology of fishes. CRC Press, Boca Raton, pp 177–230

    Google Scholar 

  • McGeer JC, Szebedinszky C, McDonald DG, Wood CM (2000) Effects of chronic sublethal exposure to waterborne Cu, Cd or Zn in rainbow trout. 1. Iono-regulatory disturbance and metabolic costs. Aquat Toxicol 50:231–243

    Article  CAS  Google Scholar 

  • Monserrat JM, Martinez PE, Geracitano LA, Amado LL, Martins CMG, Pinho GLL et al (2007) Pollution biomarkers in estuarine animals: critical review and new perspectives. Comp Biochem Physiol C Toxicol Pharmacol 146:221–234

    Article  Google Scholar 

  • Monteiro SM, Mancera JM, Fontainhas-Fernandes A, Sousa M (2005) Copper induced alterations of biochemical parameters in the gill and plasma of Oreochromis niloticus. Comp Biochem Physiol C Toxicol Pharmacol 141:375–383

    Article  Google Scholar 

  • Morgan IJ, Henry RP, Wood CM (1997) The mechanism of acute silver nitrate toxicity in freshwater rainbow trout (Oncorhynchus mykiss) is inhibition of gill Na+ and Cl− transport. Aquat Toxicol 38:145–163

    Article  CAS  Google Scholar 

  • Oner M, Atli G, Canli M (2008) Changes in serum biochemical parameters of freshwater fish Oreochromis niloticus following prolonged metal (Ag, Cd, Cr, Cu, Zn) exposures. Environ Toxicol Chem 27:360–366

    Article  CAS  Google Scholar 

  • Parvez S, Sayeed I, Raisuddin S (2006) Decreased gill ATPase activities in the freshwater fish Channa punctata (Bloch) exposed to a diluted paper mill effluent. Ecotoxicol Environ Saf 65:62–66

    Article  CAS  Google Scholar 

  • Pinkney AE, Wright DA, Jepson MA, Towle DW (1989) Effects of tributyltin compounds on ionic regulation and gill ATPase activity in estuarine fish. Comp Biochem Physiol C 92:125–129

    Article  CAS  Google Scholar 

  • Popma T, Masser M (1999) Tilapia life history and biology. Southern Regional Aquaculture Center Publication 283

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

    Google Scholar 

  • Rogers JT, Wood CM (2004) Characterization of branchial lead–calcium interaction in the freshwater rainbow trout Oncorhynchus mykiss. J Exp Biol 207:813–825

    Article  CAS  Google Scholar 

  • Sanchez W, Palluel O, Meunier L, Coquery M, Porcher JM, Ait-Aissa S (2005) Copper-induced oxidative stress in three-spined stickleback: relationship with hepatic metal levels. Environ Toxicol Pharmacol 19:177–183

    Article  CAS  Google Scholar 

  • Sancho E, Fernandez-Vega C, Ferrando MD, Andreu-Moliner E (2003) Eel ATPase activity as biomarker of thiobencarb exposure. Ecotoxicol Environ Saf 56:434–441

    Article  CAS  Google Scholar 

  • Stagg RM, Shuttleworth TJ (1982) The effects of copper on ionic regulation by the gills of the seawater-adapted flounder (Platichthys fl esus L.). J Comp Physiol 149:83–90

    CAS  Google Scholar 

  • Stagg R, Goksoyr A, Rodger G (1992) Changes in branchial Na+, K+-ATPase, metallothionein and P450 1A1 in dab Limanda limanda in the German bight: indicators of sediment contamination? Mar Ecol Prog Res 91:105–115

    Article  CAS  Google Scholar 

  • Stickney RR (1986) Tilapia tolerance of saline waters: a review. Prog Fish Cult 48:161–167

    Article  Google Scholar 

  • Thaker J, Chhaya J, Nuzhat S, Mittal R, Mansuri AP, Kundu R (1996) Effects of chromium (VI) on some ion-dependent ATPases in gills, kidney and intestine of a coastal teleost Periophthalmus dipes. Toxicology 112:237–244

    Article  CAS  Google Scholar 

  • Watson TA, Beamish FWH (1981) The Effects of zinc on branchial adenosine triphosphatase enzymes in vitro from rainbow trout, Salmo gairdneri. Comp Biochem Physiol C 68:167–173

    Article  Google Scholar 

  • Watson CF, Benson WH (1987) Comparative activity of gill ATPase in three freshwater teleosts exposed to cadmium. Ecotoxicol Environ Saf 14:252–259

    Article  CAS  Google Scholar 

  • Wendelaar Bonga SE, Lock RAC (1992) Toxicants and osmoregulation in fish. Neth J Zool 42:478–493

    Article  Google Scholar 

  • Wong CKC, Wong MH (2000) Morphological and biochemical changes in the gills of tilapia (Oreochromis mossambicus) to ambient cadmium exposure. Aquat Toxicol 48:517–527

    Article  CAS  Google Scholar 

  • Yang J, Chen HC (2003) Effects of gallium on common carp (Cyprinus carpio): acute test, serum biochemistry, and erythrocyte morphology. Chemosphere 53:877–882

    Article  CAS  Google Scholar 

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Acknowledgments

This study was supported by a grant (Grant No. FEF 2010YL23) to E. Baysoy from Çukurova University (Turkey).

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  1. Department of Biology, Faculty of Science and Letters, Çukurova University, 01330, Balcali, Adana, Turkey

    Emine Baysoy, Gülüzar Atli & Mustafa Canli

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  1. Emine Baysoy
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  2. Gülüzar Atli
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Correspondence to Mustafa Canli.

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Baysoy, E., Atli, G. & Canli, M. The Effects of Salinity and Salinity+Metal (Chromium and Lead) Exposure on ATPase Activity in the Gill and Intestine of Tilapia Oreochromis niloticus . Arch Environ Contam Toxicol 64, 291–300 (2013). https://doi.org/10.1007/s00244-012-9825-9

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