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Combined effects of water temperature and copper ion concentration on catalase activity in Crassostrea ariakensis

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Abstract

A central composite experimental design and response surface method were used to investigate the combined effects of water temperature (18–34°C) and copper ion concentration (0.1–1.5 mg/L) on the catalase (CAT) activity in the digestive gland of Crassostrea ariakensis. The results showed that the linear effects of temperature were significant (P<0.01), the quadratic effects of temperature were significant (P<0.05), the linear effects of copper ion concentration were not significant (P>0.05), and the quadratic effects of copper ion concentration were significant (P<0.05). Additionally, the synergistic effects of temperature and copper ion concentration were not significant (P>0.05), and the effect of temperature was greater than that of copper ion concentration. A model equation of CAT enzyme activity in the digestive gland of C. ariakensis toward the two factors of interest was established, with R 2, Adj. R 2 and Pred. R 2 values as high as 0.943 7, 0.887 3 and 0.838 5, respectively. These findings suggested that the goodness of fit to experimental data and predictive capability of the model were satisfactory, and could be practically applied for prediction under the conditions of the study. Overall, the results suggest that the simultaneous variation of temperature and copper ion concentration alters the activity of the antioxidant enzyme CAT by modulating active oxygen species metabolism, which may be utilized as a biomarker to detect the effects of copper pollution.

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References

  • Banni M, Hajer A, Sforzini S, Oliveri C, Boussetta H, Viarengo A. 2014. Transcriptional expression levels and biochemical markers of oxidative stress in Mytilus galloprovincialis exposed to nickel and heat stress. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 160: 23–29.

    Google Scholar 

  • Bayne B L. 1965. Growth and the delay of metamorphosis of the larvae of Mytilus edulis (L.). Ophelia, 2(1): 1–47.

    Article  Google Scholar 

  • Bebianno M J, Géret F, Hoarau P, Serafim M A, Coelho M R, Gnassia-Barelli M, Roméo M. 2004. Biomarkers in Ruditapes decussatus: a potential bioindicator species. Biomarkers, 9(4–5): 305–330.

    Article  Google Scholar 

  • Bougrier S, Geairon P, Deslous-Paoli JM, Bacher C, Jonquières G. 1995. Allometric relationships and effects of temperature on clearance and oxygen consumption rates of Crassostrea gigas (Thunberg). Aquaculture, 134(1–2): 143–154.

    Article  Google Scholar 

  • Cancio I, Ibabe A, Cajaraville M P. 1999. Seasonal variation of peroxisomal enzyme activities and peroxisomal structure in mussels Mytilus galloprovincialis and its relationship with the lipid content. Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology, 123(2): 135–144.

    Google Scholar 

  • Chakraborty S, Ray M, Ray S. 2010. Toxicity of sodium arsenite in the gill of an economically important mollusc of India. Fish & Shellfish Immunology, 29(1): 136–148.

    Article  Google Scholar 

  • Coglianese M P, Martin M. 1981. Individual and interactive effects of environmental stress on the embryonic development of the Pacific oyster, Crassostrea gigas. I. The toxicity of copper and silver. Marine Environmental Research, 5(1): 13–27.

    Article  Google Scholar 

  • de Almeida E A, Miyamoto S, Bainy A C D, de Medeiros M H G, Di Mascio P. 2004. Protective effect of phospholipid hydroperoxide glutathione peroxidase (PHGPx) against lipid peroxidation in mussels Perna perna exposed to different metals. Marine Pollution Bulletin, 49(5–6): 386–392.

    Article  Google Scholar 

  • Donaghy L, Volety A K. 2011. Functional and metabolic characterization of hemocytes of the green mussel, Perna viridis: in vitro impacts of temperature. Fish & Shellfish Immunology, 31(6): 808–814.

    Google Scholar 

  • Drążkiewicz M, Skórzyńska-Polit E, Krupa Z. 2004. Copper-induced oxidative stress and antioxidant defence in Arabidopsis thaliana. BioMetals, 17(4): 379–387.

    Article  Google Scholar 

  • Fan Z J, Yang A G, Liu Z H. 2004. Effects of Cu2+ on immune factor Chlamys farreri. Journal of Fishery Sciences of China, 11(6): 576–579. (in Chinese with English abstract)

    Google Scholar 

  • Fearman J, Moltschaniwskyj N A. 2010. Warmer temperatures reduce rates of gametogenesis in temperate mussels, Mytilus galloprovincialis. Aquaculture, 305(1–4): 20–25.

    Article  Google Scholar 

  • Geret F, Serafim A, Barreira L, João Bebianno M. 2002. Response of antioxidant systems to copper in the gills of the clam Ruditapes decussatus. Marine Environmental Research, 54(3–5): 413–417.

    Article  Google Scholar 

  • Gomes T, Pereira C G, Cardoso C, Pinheiro J P, Cancio I, Bebianno M J. 2012. Accumulation and toxicity of copper oxide nanoparticles in the digestive gland of Mytilus galloprovincialis. Aquatic Toxicology, 118–119: 72–79.

    Article  Google Scholar 

  • Guo H Y, Zhang D C, Cui S, Chen M Q, Wu K C, Li Y, Su T F, Jiang S G. 2011. Molecular characterization and mRNA expression of catalase from pearl oyster Pinctada fucata. Marine Genomics, 4(4): 245–251.

    Article  Google Scholar 

  • Hochachka P W, Somero G N. 1984. Biochemical Adaptation. Princeton University Press, Princeton. p.356–449.

    Google Scholar 

  • Isani G, Monari M, Andreani G, Fabbri M, Carpene E. 2003. Effect of copper exposure on the antioxidant enzymes in bivalve mollusc Scapharca inaequivalvis. Veterinary Research Communications, 27(1): 691–693.

    Article  Google Scholar 

  • Jiang T J, Niu T. 2006. Effects of heavy metals on superoxide dismutase (SOD) of Crassostrea rivularis. Ecology and Environment, 15(2): 289–294. (in Chinese with English abstract)

    Google Scholar 

  • Jing G, Li Y, Xie L P, Zhang R Q. 2006. Metal accumulation and enzyme activities in gills and digestive gland of pearl oyster (Pinctada fucata) exposed to copper. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 144(2): 184–190.

    Google Scholar 

  • Jing G, Li Y, Xie L P, Zhang R Q. 2007. Different effects of Pb2+ and Cu2+ on immune and antioxidant enzyme activities in the mantle of Pinctada fucata. Environmental Toxicology and Pharmacology, 24(2): 122–128.

    Article  Google Scholar 

  • Kargin F, Cogun H Y. 1999. Metal interactions during accumulation and elimination of zinc and cadmium in tissues of the freshwater fish Tilapia nilotica. Bulletin of Environmental Contamination and Toxicology, 63(4): 511–519.

    Article  Google Scholar 

  • Lacoste A, Jalabert F, Malham S, Cueff A, Gélébart F, Cordevant C, Lange M, Poulet S A. 2001. A Vibrio splendidus strain is associated with summer mortality of juvenile oysters Crassostrea gigas in the Bay of Morlaix (North Brittany, France). Diseases of Aquatic Organisms, 46(2): 139–145.

    Article  Google Scholar 

  • Lesser M P, Kruse V A. 2004. Seasonal temperature compensation in the horse mussel, Modiolus modiolus: Metabolic enzymes, oxidative stress and heat shock proteins. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 137(3): 495–504.

    Article  Google Scholar 

  • Li Y F, Gu Z Q, Liu H, Shen H D, Yang J L. 2012. Biochemical response of the mussel Mytilus coruscus (Mytiloida: Mytilidae) exposed to in vivo sub-lethal copper concentrations. Chinese Journal of Oceanology and Limnology, 30(5): 738–745.

    Article  Google Scholar 

  • Littlewood D T J, Ford S E. 1990. Physiological responses to acute temperature elevation in oysters, Crassostrea virginica, parasitized by Haplosporidium nelsoni (MSX). Journal of Shellfish Research, 8: 159–163.

    Google Scholar 

  • Liu H M, Dong Y H, Huo L H, Lin Z H, Wang Z P. 2012. Acute toxicity of Cu2+ and its effects on antioxidant enzymes in Sinonovacula constricta juveniles. Journal of Fishery Sciences of China, 1 9(1): 182–187. (in Chinese with English abstract)

    Article  Google Scholar 

  • Livingstone D R. 2001. Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Marine Pollution Bulletin, 42(8): 656–666.

    Article  Google Scholar 

  • Lushchak V I, Bagnyukova T V. 2006. Temperature increase results in oxidative stress in goldfish tissues. 2. Antioxidant and associated enzymes. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 143(1): 36–41.

    Google Scholar 

  • Lushchak V I. 2011. Environmentally induced oxidative stress in aquatic animals. Aquatic Toxicology, 101(1): 13–30.

    Article  Google Scholar 

  • Maria V L, Bebianno M J. 2011. Antioxidant and lipid peroxidation responses in Mytilus galloprovincialis exposed to mixtures of benzo(a)pyrene and copper. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 154(1): 56–63.

    Google Scholar 

  • Mubiana V K, Blust R. 2007. Effects of temperature on scope for growth and accumulation of Cd, Co, Cu and Pb by the marine bivalve Mytilus edulis. Marine Environmental Research, 63(3): 219–235.

    Article  Google Scholar 

  • Myung I A, Cheol Y C. 2010. Activity of antioxidant enzymes and physiological responses in ark shell, Scapharca broughtonii, exposed to thermal and osmotic stress: effects on hemolymph and biochemical parameters. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 155(1): 34–42.

    Google Scholar 

  • Parihar M S, Javeri T, Hemnani T, Dubey A K, Prakash P. 1997. Responses of superoxide dismutase, glutathione peroxidase and reduced glutathione antioxidant defenses in gills of the freshwater catfish (Heteropneustes fossilis) to short-term elevated temperature. Journal of Thermal Biology, 22(2): 151–156.

    Article  Google Scholar 

  • Pipe R K, Coles J A, Carissan F M M, Ramanathan K. 1999. Copper induced immunomodulation in the marine mussel, Mytilus edulis. Aquatic Toxicology, 46(1): 43–54.

    Article  Google Scholar 

  • Regoli F, Nigro M, Orlando E. 1998. Lysosomal and antioxidant responses to metals in the Antarctic scallop Adamussium colbecki. Aquatic Toxicology, 40(4): 375–392.

    Article  Google Scholar 

  • Solé M, Porte C, Albaiges J. 1995. Seasonal variation in the mixed-function oxygenase system and antioxidant enzymes of the mussel Mytilus galloprovincialis. Environmental Toxicology and Chemistry, 14(1): 157–164.

    Article  Google Scholar 

  • Stebbing A R D. 1982. Hormesis-the stimulation of growth by low levels of inhibitors. Science of the Total Environment, 22(3): 213–234.

    Article  Google Scholar 

  • Sun Y Y, Gao R C, Wen Y M, Chen N, Wang S. 2008. Effects of Temperature on hydrolase and antioxidase activities in liver of clam Hiatula chinensis and H. diphos. Fisheries Science, 27(10): 543–544. (in Chinese with English abstract)

    Google Scholar 

  • Verlecar X N, Jena K B, Chainy G B N. 2007. Biochemical markers of oxidative stress in Perna viridis exposed to mercury and temperature. ChemicoBiological Interactions, 167(3): 219–226.

    Article  Google Scholar 

  • Verlecar X N, Jena K B, Chainy G B N. 2008. Modulation of antioxidant defences in digestive gland of Perna viridis (L.), on mercury exposures. Chemosphere, 71(10): 1 977–1 985.

    Article  Google Scholar 

  • Viarengo A, Canesi L, Pertica M, Livingstone D R. 1991. Seasonal variations in the antioxidant defence systems and lipid peroxidation of the digestive gland of mussels. Comparative Biochemistry and Physiology Part C: Comparative Pharmacology, 100(1–2): 187–190.

    Article  Google Scholar 

  • Vlahogianni T, Dassenakis M, Scoullos M J, Valavanidis A. 2007. Integrated use of biomarkers (superoxide dismutase, catalase and lipid peroxidation) in mussels Mytilus galloprovincialis for assessing heavy metals’ pollution in coastal areas from the Saronikos Gulf of Greece. Marine Pollution Bulletin, 54(9): 1 361–1 371.

    Article  Google Scholar 

  • Vlahogianni T H, Valavanidis A. 2007. Heavy-metal effects on lipid peroxidation and antioxidant defence enzymes in mussels Mytilus galloprovincialis. Chemistry and Ecology, 23(5): 361–371.

    Article  Google Scholar 

  • Wang H, Liu J H, Yang H S, Liu Z G. 2014. Effect of simultaneous variation in temperature and ammonia concentration on percent fertilization and hatching in Crassostrea ariakensis. Journal of Thermal Biology, 41: 43–49.

    Article  Google Scholar 

  • Wu Y C, Lv X, Wang F, Zhao Y F, Liu C F. 2005. Accumulation of Copper in Chlamys farreri tissues and its effect on catalase activity. Chinese Journal of Applied & Environmental Biology, 11(5): 559–562. (in Chinese with English abstract)

    Google Scholar 

  • Xiao X, Deng R P, Chen Z L, Han Y L. 2003. The comparison of the characteristics of catalase in oyster and Tegillarca granosa. Food Science, 24(9): 32–34. (in Chinese)

    Google Scholar 

  • Zanette J, de Almeida E A, da Silva A Z, Guzenski J, Ferreira J F, Mascio P D, Marques M R F, Bainy A C D. 2011. Salinity influences glutathione S-transferase activity and lipid peroxidation responses in the Crassostrea gigas oyster exposed to diesel oil. Science of the Total Environment, 409(10): 1 976–1 983.

    Article  Google Scholar 

  • Zhang Y, Fu D K, Yu F, Liu Q Y, Yu Z N. 2011. Two catalase homologs are involved in host protection against bacterial infection and oxidative stress in Crassostrea hongkongensis. Fish & Shellfish Immunology, 31(6): 894–903.

    Article  Google Scholar 

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Correspondence to Zhigang Liu  (刘志刚).

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Supported by the Guangdong Province Science & Technology Project (No. 2010B020201014), the Guangdong Province Education Department (No. GCZX-A0909), the Guangdong Province Ocean and Fisheries Science & Technology Extension Project (No. 20120980), the Guangdong Province Industry-University-Science Partnership Project (No. 20110908), and the Sci & Tech Plan of Huaiyin Normal University (No. 00wh0031)

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Wang, H., Yang, H., Liu, J. et al. Combined effects of water temperature and copper ion concentration on catalase activity in Crassostrea ariakensis . Chin. J. Ocean. Limnol. 33, 905–912 (2015). https://doi.org/10.1007/s00343-015-4212-9

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  • DOI: https://doi.org/10.1007/s00343-015-4212-9

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