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Effect of cadmium on the defense response of Pacific oyster Crassostrea gigas to Listonella anguillarum challenge

  • Biology
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Abstract

Heavy metal pollution can affect the immune capability of organisms. We evaluated the effect of cadmium (Cd) on the defense responses of the Pacific oyster Crassostrea gigas to Listonella anguillarum challenge. The activities of several important defensive enzymes, including superoxide dismutase (SOD), glutathione peroxidase (GPx), acid phosphatase (ACP), Na+, K+ -ATPase in gills and hepatopancreas, and phenoloxidase-like (POL) enzyme in hemolymph were assayed. In addition, the expression levels of several genes, including heat shock protein 90 (HSP90), metallothionein (MT), and bactericidal/permeability increasing (BPI) protein were quantified by fluorescent quantitative PCR. The enzyme activities of SOD, ACP, POL, and GPx in hepatopancreas, and the expression of HSP90 were down-regulated, whereas GPx activity in the gill, Na+, K+-ATPase activities in both tissues, and MT expression was increased in Cdexposed oysters post L. anguillarum challenge. However, BPI expression was not significantly altered by co-stress of L. anguillarum infection and cadmium exposure. Our results suggest that cadmium exposure alters the oysters’ immune responses and energy metabolism following vibrio infection.

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References

  • Aladaileh S, Nair S V, Birch D, Raftos D A. 2007. Sydney rock oyster (Saccostrea glomerata) hemocytes: morphology and function. J. Invertebr. Pathol., 96: 48–63.

    Article  Google Scholar 

  • Bado-Nilles A, Renault T, Faury N, Le Floch S, Quentel C, Auffret M, Thomas-Guyon H. 2010. In vivo effects of LCO soluble fraction on immune-related functions and gene transcription in the Pacific oyster, Crassostrea gigas (Thunberg). Aquat. Toxicol., 97: 196–203.

    Article  Google Scholar 

  • Barral J M, Broadley S A, Schaffar G, Hartl F U. 2004. Roles of molecular chaperones in protein misfolding diseases, Semin. Cell Dev. Biol., 15: 17–29.

    Article  Google Scholar 

  • Bouilly K, Gagnaire B, Bonnard M, Thomas-Guyon H, Renault T, Miramand P, Lapègue S. 2006. Effects of cadmium on aneuploidy and hemocyte parameters in the Pacific oyster, Crassostrea gigas. Aquat. Toxicol., 78: 149–156.

    Article  Google Scholar 

  • Brown C. 1981. A prodiginine pigment toxic to embryos and larvae of Crassostrea virginica. J. Invertebr. Pathol., 38: 281–293.

    Article  Google Scholar 

  • Brulle F, Mitta G, Leroux R, Lemière S, Leprêtre A, Vandenbulcke F. 2007. The strong induction of metallothionein gene following cadmium exposure transiently affects the expression of many genes in Eisenia Fetida: a trade-off mechanism?. Comp. Biochem. Physiol. C, 144: 334–341.

    Google Scholar 

  • Calabrese E J. 2008. Hormesis: why it is important to toxicology and toxicologists. Environ. Toxicol. Chem., 27: 1 451–1 474.

    Article  Google Scholar 

  • Cherkasov A S, Biswas P K, Ridings D M, Ringwood A H, Sokolova I M. 2006. Effects of acclimation temperature and cadmium exposure on cellular energy budgets in a marine mollusk Crassostrea virginica: linking cellular and mitochondrial responses. J. Exp. Biol., 209: 1 274–1 284.

    Article  Google Scholar 

  • Chester R. 1990. Marine Geochemistry, 1st edn. Allen & Unwin, London.

    Book  Google Scholar 

  • Cong M, Song L, Wang L, Zhao J, Qiu L, Li L, Zhang H. 2008. The enhanced immune protection of zhikong scallop Chlamys farreri on the secondary encounter with Listonella anguillarum. Comp. Biochem. Physiol. B, 151: 191–196.

    Article  Google Scholar 

  • Cossu C, Doyotte A, Jacquin M C, Babut M, Exinger A, Vasseur P. 1997. Glutathione reductase, seleniumdependent glutathione peroxidase, glutathione levels and lipid peroxidation in freshwater bivalves, Unio turmidus as biomarkers of aquatic contamination in field studies. Ecotox. Environ. Saf., 38: 122–131.

    Article  Google Scholar 

  • Deng H, Sui X L, Wang Z S. 1992. Primary study on vibrios of the Pacific oyster, Crassostrea gigas. Fish. Sci., 11: 1–4. (in Chinese with English abstract)

    Google Scholar 

  • Elsbach P, Weiss J. 1993. Bactericida/permeablity increasing protein and host defense against gram-negative bacteria and endotoxin. Curr. Opin. Immunol., 5: 103–107.

    Article  Google Scholar 

  • Fang Y, Yang H, Wang T, Liu B, Zhao H, Chen M. 2009. Metallothionein and superoxide dismutase responses to sublethal cadmium exposure in the clam Mactra veneriformis. Comp. Biochem. Physiol. C, 151: 325–333.

    Google Scholar 

  • Flick J G J. 2007. Pathogenic vibrios in shellfish. Global Aquaculture Advocate, 10: 46–48.

    Google Scholar 

  • Fridovich I. 1975. Superoxide dismutases. Annu. Rev. Biochem., 44: 147–159.

    Article  Google Scholar 

  • Giannapas M, Karnis L, Dailianis S. 2012. Generation of free radicals in haemocytes of mussels after exposure to low molecular weight PAH components: immune activation, oxidative and genotoxic effects. Comp. Bioc hem. Physiol. C, 155: 182–189.

    Google Scholar 

  • Hauton C, Hawkins L E, Hutchinson S. 2000. The effects of salinity on the interaction between a pathogen (Listonella anguillarum) and components of a host (Ostrea edulis) immune system. Comp. Biochem. Physiol. B, 127: 203–212.

    Article  Google Scholar 

  • Ivanina A V, Eilers S, Kurochkin I O, Chung J S, Techa S, Piontkivska H, Sokolov E P, Sokolova I M. 2010. Effects of cadmium exposure and intermittent anoxia on nitric oxide metabolism in eastern oysters, Crassostrea virginica. J. Exp. Biol., 213: 433–444.

    Article  Google Scholar 

  • Jing G, Li Y, Xie L, Zhang R. 2007. Different effects of Pb2+ and Cu2+ on immune and antioxidant enzyme activities in the mantle of Pinctada fucata. Environ. Toxicol. Phar., 24: 122–128.

    Article  Google Scholar 

  • Jo P G, Choi Y K, Choi C Y. 2008. Cloning and mRNA expression of antioxidant enzymes in the Pacific oyster, Crassostrea gigas in response to cadmium exposure. Comp. Biochem. Physiol. C, 147: 460–469.

    Google Scholar 

  • Jorgensen P L, Pedersen P A. 2001. Structure-function relationships of Na+, K+, ATP, or Mg2+ binding and energy transduction in Na, K-ATPase. Biochim. Biophys. Acta, 1505: 57–74.

    Article  Google Scholar 

  • Kannan K, Jain S K. 2000. Oxidative stress and apoptosis. Pathophysiology, 7: 153–163.

    Article  Google Scholar 

  • Labreuche Y, Lambert C, Soudant P, Boulo V, Huvet A, Nicolas J. 2006. Cellular and molecular hemocyte responses of the Pacific oyster, Crassostrea gigas, following bacterial infection with Vibrio aestuarianus strain 01/32. Dev. Comp. Immunol., 8: 2 715–2 724.

    Google Scholar 

  • Li R, Zhou Y, Ji J, Wang L. 2011. Oxidative damages by cadmium and the protective effects of low-molecularweight chitosan in the freshwater crab (Sinopotamon yangtsekiense Bott 1967). Aquac. Res., 42: 506–515.

    Article  Google Scholar 

  • Liu F, Wang D Z, Wang W X. 2012. Cadmium-induced changes in trace element bioaccumulation and proteomics perspective in four marine bivalves. Environ. Toxicol. Chem., 31: 1 292–1 300.

    Google Scholar 

  • Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods, 25: 402–408.

    Article  Google Scholar 

  • Luna-Acosta A, Bustamante P, Godefroy J, Fruitier-Arnaudin I, Thomas-Guyon H. 2010. Seasonal variation of pollution biomarkers to assess the impact on the health status of juvenile Pacific oysters Crassostrea gigas exposed in situ. Environ. Sci. Pollut. Res. Int., 17: 999–1 008.

    Article  Google Scholar 

  • Masters S L, O’Neill L A J. 2011. Disease-associated amyloid and misfolded protein aggregates activate the inflammasome. Trends Mol. Med., 17: 276–282.

    Article  Google Scholar 

  • Mattson M P. 2008. Hormesis defined. Ageing Res. Rev., 7: 1–7.

    Article  Google Scholar 

  • McCord J M. 1993. Human disease, free radicals, and the oxidant/antioxidant balance. Clin. Biochem., 26: 351–357.

    Article  Google Scholar 

  • Sokolova I M, Evans S, Hughes F M. 2004. Cadmium-induced apoptosis in oyster hemocytes involves disturbance of cellular energy balance but no mitochondrial permeability transition. J. Exp. Biol., 207: 3 369–3 380.

    Google Scholar 

  • Sokolova I M, Frederich M, Bagwe R, Lannig G, Sukhotin A A. 2012. Energy homeostasis as an integrative tool for assessing limits of environmental stress tolerance in aquatic invertebrates. Mar. Environ. Res., 79: 1–15.

    Article  Google Scholar 

  • Pena-Llopis S, Ferrando M D. 2003. Fish tolerance to organophosphate-induced oxidative stress is dependent on the glutathione metabolism and enhanced by NH2 — acetylcysteine. Aquat. Toxicol., 65: 337–360.

    Article  Google Scholar 

  • Pauley G B, Van Der Raay B M, Troutt D. 1988. Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (Pacific Northwest): Pacific oyster. Fish and Wildlife Service Biological Report, 82(11.85): 28.

    Google Scholar 

  • Qin Y, Meng W, Zheng B, Su Y. 2006. Heavy metal pollution in tidal zones of Bohai Bay using the dated sediment cores. J. Environ. Sci., 18: 610–615. (in Chinese with English abstract)

    Google Scholar 

  • Sies H. 1993. Strategies of antioxidant defense. Eur. J. Biochem., 215: 213–219.

    Article  Google Scholar 

  • Thompson F L, Thompson C C, Dias G M, Naka H, Dubay C, Crosa J H. 2011. The genus Listonella Macdonell and Colwell 1986 is a later heterotypic synonym of the genus Vibrio Pacini 1854 (approved lists 1980)-a taxonomic opinion. Int. J. Syst. Evol. Micr., 61: 3 023–3 027.

    Article  Google Scholar 

  • Verma S R, Rani S, Dalela R C. 1980. Effects of phenol and dinitrophenol on acid and alkaline phosphatases in tissues of a fish, Notopterus notopterus. Arch. Environ. Contam. Toxicol., 9: 451–459.

    Article  Google Scholar 

  • Wang L, Song L, Ni D, Zhang H, Liu W. 2009. Alteration of metallothionein mrna in bay scallop Argopecten irradians under cadmium exposure and bacteria challenge. Comp. Biochem. Physiol. C, 149: 50–57.

    Google Scholar 

  • Wu H, Wang W X. 2011. Tissue-specific toxicological effects of cadmium in green mussels (Perna viridis): nuclear magnetic resonance-based metabolomics study. Environ. Toxicol. Chem., 30: 806–812.

    Article  Google Scholar 

  • Zhang L, Liu X, You L, Zhou D, Yu J, Zhao J, Feng J, Wu H. 2011. Toxicological effects induced by cadmium in gills of manila clam Ruditapes philippinarum using NMRbased metabolomics. Clean Soil Air Water, 39: 989–995.

    Article  Google Scholar 

  • Zhang X. 2001. Investigation of pollution of Pb, Cd, Hg, as in sea water and deposit of Bohai Sea area. Heilongjiang Environ. J., 25: 87–90. (in Chinese with an English abstract)

    Google Scholar 

  • Zhang Z, Zhang Q. 2012. Molecular cloning, characterization and expression of heat shock protein 70 gene from the oyster Crassostrea hongkongensis responding to thermal stress and exposure of Cu2+ and malachite green. Gene, 497: 172–180.

    Article  Google Scholar 

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Authors and Affiliations

  1. Key Laboratory of Coastal Zone Environment Processes, Chinese Academy of Sciences; Shandong Provincial Key Laboratory of Coastal Zone Environment Processes, Yantai Institute of Coastal Zone Research, Chinese Academy of Sciences, Yantai, 264003, China

    Ming Cong  (丛明), Huifeng Wu  (吴惠丰) & Jianmin Zhao  (赵建民)

  2. Biology School of Yantai University, Yantai, 264005, China

    Jiasen Lü  (吕家森)

Authors
  1. Ming Cong  (丛明)
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  2. Jiasen Lü  (吕家森)
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  3. Huifeng Wu  (吴惠丰)
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  4. Jianmin Zhao  (赵建民)
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Correspondence to Huifeng Wu  (吴惠丰).

Additional information

Supported by the 100 Talents Program of Chinese Academy of Sciences, the Development Plan of Science and Technology in Shandong Province (No. 2012GGA06032), and the Key Deployment Program of Chinese Academy of Sciences (No. KZZD-EW-14-03)

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Cong, M., Lü, J., Wu, H. et al. Effect of cadmium on the defense response of Pacific oyster Crassostrea gigas to Listonella anguillarum challenge. Chin. J. Ocean. Limnol. 31, 1002–1009 (2013). https://doi.org/10.1007/s00343-013-2280-2

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  • DOI: https://doi.org/10.1007/s00343-013-2280-2

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