Skip to main content
SpringerLink
Log in

Essential metal (Cu, Zn) exposures alter the activity of ATPases in gill, kidney and muscle of tilapia Oreochromis niloticus

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

An acute (96 h—0.1, 0.5, 1.0, 1.5 μg/ml) and chronic (up to 30 days—0.05 μg/ml) protocols of Cu and Zn were applied to freshwater fish Oreochromis niloticus to investigate these essential metal effects on the activities of gill, kidney and muscle Na+/K+-ATPase, Mg2+-ATPase and Ca2+-ATPase. In vitro effects of both metals (20 min—0.1, 0.5, 1.0, 1.5 μg/ml) were also measured to be able to compare both exposure routes. Data showed that ATPase activities, in general, decreased following all the exposure conditions, though there were some increases especially in Mg2+-ATPase activity. Among the enzymes, Na+/K+-ATPase and Ca2+-ATPase appeared to be more sensitive than Mg2+-ATPase to the metals. The data also indicated that effects of Cu on ATPase activity in the tissues of O. niloticus were stronger than the effects of Zn, possibly due to higher toxic effects of Cu. In vivo and in vitro exposures of metals showed similar trends with a few exceptions, especially in the gill. Variability of ATPase activity is determined by tissue type, metal species, concentration and duration. This work showed that even essential metals can alter significantly activities of ATPases in fish and thus suggests using them as a sensitive biomarker in metal contaminated waters.

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
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Almeida JA, Diniz YS, Marques SFG, Faine LA, Ribas BO, Burneiko RC, Novelli ELB (2002) The use of the oxidative stress responses as biomarkers in Nile Tilapia (Oreochromis niloticus) exposed to in vivo cadmium contamination. Environ Int 27:673–679

    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

    CAS  Google Scholar 

  • Atli G (2010) Effects of copper, zinc, cadmium, chromium and silver on the Na+/K+-ATPase, Ca2+-ATPase and Mg2+-ATPase in gill, kidney and Ca2+-ATPase enzyme activities in muscle tissue of Oreochromis niloticus. PhD Thesis, Çukurova University, Turkey

  • Atli G, Canli M (2003) Natural occurrence of metallothionein-like proteins in the liver of fish Oreochromis niloticus and effects of cadmium, lead, copper, zinc, and iron exposures on their profiles. Bull Environ Contam Toxicol 70:619–627

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Atli G, Canli M (2008) Responses of metallothionein and reduced glutathione in a freshwater fish Oreochromis niloticus following metal exposures. Environ Toxicol Pharmacol 25:33–38

    Article  CAS  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 Safe 73:1884–1889

    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 Toxicol 62:160–168

    Article  CAS  Google Scholar 

  • Bansal SK, Murthy RC, Chandra SV (1985) The effects of some divalent metals on cardiac and branchial Ca2+-ATPase in a freshwater fish Saccobranchus fossilis. Ecotoxicol Environ Safe 9:373–377

    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 

  • De Boeck G, Vlaeminck A, Balm PHM, Lock RAC, De Wachter B, Blust R (2001) Morphological and metabolic changes in common carp, Cyprinus carpio, during short-term copper exposure: interactions between Cu2+ and plasma cortisol elevation. Environ Toxicol Chem 20(2):374–381

    Google Scholar 

  • De la Torre FR, Salibian A, Ferrari L (2000) Biomarkers assessment in juvenile Cyprinus carpio exposed to waterborne cadmium. Environ Pollut 109:277–282

    Article  Google Scholar 

  • De la Torre FR, Salibian A, Ferrari L (2007) Assessment of the pollution impact on biomarkers of effect of a freshwater fish. Chemosphere 68:1582–1590

    Article  Google Scholar 

  • Ebrahimpour M, Alipour H, Rakhshah S (2010) Influence of water hardness on acute toxicity of copper and zinc on fish. Toxicol Ind Health 26:361–365

    Article  CAS  Google Scholar 

  • Eroglu K, Atli G, Canli M (2005) Effects of metal (Cd, Cu, Zn) interactions on the profiles of metallothionein-like proteins in the Nile fish Oreochromis niloticus. Bull Environ Contam Toxicol 75:390–399

    Article  CAS  Google Scholar 

  • Eyckmans M, Tudorache C, Darras VM, Blust R, De Boeck G (2011) Hormonal and ion regulatory response in three freshwater fish species following waterborne copper exposure. Comp Biochem Physiol 152C:270–278

    Google Scholar 

  • Grosell M, Wood CM, Walsh PJ (2003) Copper homeostasis and toxicity in the elasmobranch Raja erinacea and the teleost Myoxocephalus octodecemspinosus during exposure to elevated water-borne copper. Comp Biochem Physiol 135C:179–190

    CAS  Google Scholar 

  • Grosell M, McDonald MD, Walsh PJ, Wood CM (2004) Effects of prolonged copper exposure in the marine gulf toadfish (Opsanus beta) II: Copper accumulation, drinking rate and Na+–K+ ATPase activity in osmoregulatory tissues. Aquat Toxicol 68:263–275

    Article  CAS  Google Scholar 

  • Handy RD, Eddy FB, Baines H (2002) Sodium-dependent copper uptake across epithelia: a review of rationale with experimental evidence from gill and intestine. Biochim Et Biophys Acta 1566:104–115

    Article  CAS  Google Scholar 

  • Heath AG (1987) Water Pollution and Fish Physiology. CRC Press, Florida, p 245

    Google Scholar 

  • Hogstrand C, Verbost PM, Bonga SE, Wood CM (1996) Mechanisms of zinc uptake in gills of freshwater rainbow trout: interplay with calcium transport. Am J Physiol 270:R1141–R1147

    CAS  Google Scholar 

  • Hollis L, McGeer JC, McDonald DG, Wood CM (2000) Effects of long term sublethal Cd exposure in rainbow trout during soft water exposure: Implications for biotic ligand modelling. Aquat Toxicol 51:93–105

    Article  CAS  Google Scholar 

  • Kamunde C, Clayton C, Wood CM (2002) Waterborne vs. dietary copper uptake in rainbow trout and the effects of previous waterborne copper exposure. Am J Physiol Reg Integr Comp Physiol 283:R69–R78

    CAS  Google Scholar 

  • Larsson A, Haux C, Sjobeck ML (1985) Fish physiology and metal pollution: results and experiences from laboratory and field studies. Ecotoxicol Environ Saf 9:250–281

    Article  CAS  Google Scholar 

  • Lauren DJ, McDonald DG (1987) Acclimation to copper by rainbow trout, Salmo gairdneri: biochemistry. Can J Fish Aquat Sci 44:105–111

    Article  CAS  Google Scholar 

  • Lemaire-Gony S, Mayer-Gostan N (1994) In vitro dose–response study of the effect of cadmium on eel (Anguilla anguilla) gill Na+–K+-ATPase activities. Ecotoxicol Environ Saf 28:43–52

    Article  CAS  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 

  • 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 

  • McGeer JC, Wood CM (1998) Protective effects of water Cl− on physiological responses to waterborne silver in rainbow trout. Can J Fish Aquat Sci 55(11):2447–2454

    Article  CAS  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, Chaves ISC, Ferreira-Cravo M, Ventura-Lima J, Bianchini A (2007) Pollution biomarkers in estuarine animals: critical review and new perspectives. Comp Biochem Physiol 146C:221–234

    CAS  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 (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 

  • Pratap HB, Wendelaar Bonga SE (1993) Effect of ambient and dietary cadmium on pavement cells, chloride cells, and Na+/K+-ATPase activity in the gills of the freshwater telesot Oreochromis mossambicus at normal and high calcium levels in the ambient water. Aquat Toxicol 26:133–150

    Article  CAS  Google Scholar 

  • Reddy PM, Philip GH, Bashamohideen M (1991) Inhibition of Mg2+ and Na(+)–K+ ATPases in selected tissues of fish, Cyprinus carpio under fenvalerate toxicity. Biochem Int 23:715–721

    CAS  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 Safe 56:434–441

    Article  CAS  Google Scholar 

  • Schlenk D, Benson WH (2001) Target organ toxicity in marine and freshwater teleosts. Taylor and Francis, London, p 372

    Book  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 

  • Watson TA, Beamish FWH (1980) Effects of zinc on branchial ATPase activity in vivo in rainbow trout, Salmo gairdneri. Comp Biochem Physiol 66C:77–82

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • WHO (2001) Environmental health criteria. World Health Organization, Genova

    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 

Download references

Acknowledgment

This study supported by a Research Fund (FEF2003D14) to Gülüzar ATLI from Çukurova University.

Author information

Authors and Affiliations

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

    Gülüzar Atli & Mustafa Canli

Authors
  1. Gülüzar Atli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mustafa Canli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gülüzar Atli.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Atli, G., Canli, M. Essential metal (Cu, Zn) exposures alter the activity of ATPases in gill, kidney and muscle of tilapia Oreochromis niloticus . Ecotoxicology 20, 1861–1869 (2011). https://doi.org/10.1007/s10646-011-0724-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-011-0724-z

Keywords

Search

Navigation