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Putative Roles for Metallothionein and HSP70 Genes in Relation with Heavy Metal Accumulation and Parasitic Cymothoid in the Fish Nemipterus furcosus

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Abstract

To assess stress level induced by multiple stressors in aquatic organism, biomarkers have been adopted as early warning indicator due to their high accuracy, rapidity, and sensitivity. We investigated the effects of ectoparasitic isopod infection on heavy metal bioaccumulation (Fe, Cu, Zn, and Cd) in the fish Nemipterus furcosus and profiled the expression of metallothionein (MT) and heat shock proteins 70 (HSP70) genes of the fish host. Sixty individuals (parasitized and nonparasitized with Cymothoa truncata) were collected from three sites differing in the levels of anthropogenic activities off the South China Sea. Our results revealed no significant difference in heavy metal concentrations between infected and nonparasitized fish. We observed a positive correlation between heavy metal bioaccumulation in the fish host and anthropogenic activities. Accordingly, expression analysis of MT genes in fish liver showed significant differences in expression level between sampling sites, with lowest level in the least exploited site (Batu Rakit). A reverse pattern in HSP70 gene expression was demonstrated in fish muscle, showing the highest expression at Batu Rakit. While cymothoid infection in N. furcosus had no significant impact on fish MT gene expression, it resulted in a reduction of HSP70 level in liver of parasitized fish. These findings highlight the putative roles of MT in heavy metal assessment. Future studies should determine the kinetics of cymothoid infection and other potential stressors in characterizing the HSP70 gene expression profile.

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References

  • Agusa T, Kunito T, Yasunaga G, Iwata H, Subramanian A, Ismail A, Tanabe S (2005) Concentration of trace elements in marine fish and its risk assessment in Malaysia. Mar Pollut Bull 51:896–911

    Article  CAS  Google Scholar 

  • Ameur WB, de Lapuente J, El Megdiche Y, Barhoumi B, Trabelsi S, Camps L, Serret J, Ramos-López D, Gonzalez-Linares J, Driss MR, Borràs M (2012) Oxidative stress, genotoxicity and histopathology biomarker responses in mullet (Mugil cephalus) and sea bass (Dicentrarchus labrax) liver from Bizerte Lagoon (Tunisia). Mar Pollut Bull 64:241–251

    Article  Google Scholar 

  • Ashraf MA, Maah MJ, Yusoff I (2012) Bioaccumulation of heavy metals in fish species collected from former tin mining catchment. Int J Environ Res 6:209–218

    CAS  Google Scholar 

  • Atli G, Canli M (2008) Enzymatic responses to metal exposures in a freshwater fish Oreochromis niloticus. Comp Biochem Physiol C 145:282–287

    Google Scholar 

  • Basu N, Kennedy CJ, Iwama GK (2003) The effects of stress on the association between HSP70 and the glucocorticoid receptor in rainbow trout. Comp Biochem Physiol A 134:655–663

    Article  CAS  Google Scholar 

  • Bio-Rad Laboratories Inc. (2006) Real-time PCR applications guide. Bulletin 5279

    Google Scholar 

  • Deane EE, Woo NY (2006) Impact of heavy metals and organochlorines on HSP70 and HSC70 gene expression in black sea bream fibroblasts. Aquat Toxicol 79:9–15

    Article  CAS  Google Scholar 

  • Dhaneesh KV, Gopi M, Ganeshamurthy R, Ajith Kumar TT, Balasubramanian T (2012) Bioaccumulation of metals on reef associated organisms of Lakshadweep Archipelago. Food Chem 131:985–991

    Article  CAS  Google Scholar 

  • Dzik JM (2006) Molecules released by helminth parasites involved in host colonization. Acta Biochim Pol 53:33–64

    CAS  Google Scholar 

  • Farag AM, Skaar D, Nimick DA, MacConnell E, Hogstrand C (2003) Characterizing aquatic health using salmonid mortality, physiology, and biomass estimates in streams with elevated concentrations of arsenic, cadmium, copper, lead, and zinc in the Boulder River watershed, Montana. Trans Am Fish Soc 132:450–467

    Article  CAS  Google Scholar 

  • Fazio G, Moné H, Lecomte-Finiger R, Sasal P (2008) Differential gene expression analysis in European eels (Anguilla anguilla, L 1758) naturally infected by macroparasites. J Parasitol 94:571–577

    Article  CAS  Google Scholar 

  • Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282

    Article  CAS  Google Scholar 

  • Frank SN, Godehardt S, Nachev M, Trubiroha A, Kloas W, Sures B (2013) Influence of the cestode Ligula intestinalis and the acanthocephalan Polymorphous minutus on levels of heat shock proteins (HSP70) and metallothioneins in their fish and crustacean intermediate hosts. Environ Pollut 180:173–179

    Article  CAS  Google Scholar 

  • Fuad MM, Shazili NAM, Faridah M (2013) Trace metals and rare earth elements in Saccostrea cucullata along the east coast of Peninsular Malaysia. Aquat Ecosyst Health Manag 16:78–87

    CAS  Google Scholar 

  • Giguère A, Couillard Y, Campbell PGC, Perceval O, Hare L, Pinel-Alloul B, Pellerin J (2003) Steady-state distribution of metals among metallothionein and other cytosolic ligands and links to cytotoxicity in bivalves living along a polymetallic gradient. Aquat Toxicol 64:185–200

    Article  Google Scholar 

  • Guardiola FA, Gónzalez-Párraga P, Meseguer J, Cuesta A, Esteban MA (2014) Modulatory effects of deltamethrin-exposure on the immune status, metabolism and oxidative stress in gilthead seabream (Sparus aurata L.). Fish Shellfish Immunol 36:120–129

    Article  CAS  Google Scholar 

  • Gupta SC, Sharma A, Mishra M, Mishra R, Chowdhuri DK (2010) Heat shock proteins in toxicology: how close and how far? Life Sci 86:377–384

    Article  CAS  Google Scholar 

  • Javed M (2005) Heavy metal contamination of freshwater fish and bed sediments in the river Ravi stretch and related tributaries. Pak J Biol Sci 8:1337–1341

    Article  CAS  Google Scholar 

  • Jawale S, Fartade A, Borde S (2011) Biochemical studies of Caryophyllidean tapeworms in fresh water fish Clarias batrachus. Recent Res Sci Tech 3:35–36

    Google Scholar 

  • Kalay M, Ay O, Canli M (1999) Heavy metal concentrations in fish tissues from the Northeast Mediterrenean Sea. Bull Environ Contam Toxicol 63:673–681

    Article  CAS  Google Scholar 

  • Kim JH, Rhee JS, Dahms HU, Lee YM, Han KN, Lee JS (2012) The yellow catfish, Pelteobagrus fulvidraco (Siluriformes) metallothionein cDNA: molecular cloning and transcript expression level in response to exposure to the heavy metals Cd, Cu, and Zn. Fish Physiol Biochem 38:1331–1342

    Article  CAS  Google Scholar 

  • Knapen D, Reynders H, Bervoets L, Verheyen E, Blust R (2007) Metallothionein gene and protein expression as a biomarker for metal pollution in natural gudgeon populations. Aquat Toxicol 82:163–172

    Article  CAS  Google Scholar 

  • Man AKY, Woo NYS (2008) Upregulation of metallothionein and glucose-6-phosphate dehydrogenase expression in silver sea bream, Sparus sarba, exposed to sublethal levels of cadmium. Aquat Toxicol 89:214–221

    Article  CAS  Google Scholar 

  • Marijić VF, Smrzlić IV, Raspor B (2013) Effect of acanthocephalan infection on metal, total protein, and metallothionein concentrations in European chub from a Sava River section with low metal contamination. Sci Total Environ 463–464:772–780

    Google Scholar 

  • Ming J, Xie J, Xu P, Liu W, Ge X, Liu B, He Y, Cheng Y, Zhou Q, Pan L (2010) Molecular cloning and expression of two HSP70 genes in the Wuchang bream (Megalobrama amblycephala). Fish Shellfish Immunol 28:407–418

    Article  CAS  Google Scholar 

  • Monserrat JM, Martinez PE, Geracitano LA, Amado LL, Martins CM, Pinho GL, Chaves IS, Ferreira-Cravo M, Ventura-Lima J, Bianchini A (2007) Pollution biomarkers in estuarine animals: critical review and new perspectives. Comp Biochem Physiol C 146:221–234

    Google Scholar 

  • Oyoo-Okoth E, Admiraal W, Osano O, Hoitinga L, Kraak MHS (2010) Metal specific partitioning in a parasite-host assemblage of the cestode Ligula intestinalis and the cyprinid fish Rastrineobola argentea. Sci Total Environ 408:1557–1562

    Article  CAS  Google Scholar 

  • Oyoo-Okoth E, Admiraal W, Osano O, Kraak MHS, Gichuki J, Ogwai C (2012) Parasites modify sub-cellular partitioning of metals in the gut of fish. Aquat Toxicol 106–107:76–84

    Article  Google Scholar 

  • Padmini E, Geetha BV, Usha Rani M (2009) Pollution-induced nitrative stress and heat shock 70 proteins over expression in fish liver mitochondria. Sci Total Environ 407:1307–1317

    Article  CAS  Google Scholar 

  • Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36

    Article  Google Scholar 

  • Pina B, Casado M, Quiros L (2007) Analysis of gene expression as a new tool in ecotoxicology and environmental monitoring. Trends Anal Chem 26:1145–1154

    Article  CAS  Google Scholar 

  • Scheil V, Zurn A, Kohler HR, Triebskorn R (2009) Embryo development, stress protein (HSP70) responses, and histopathology in zebrafish (Danio rerio) following exposure to nickel chloride, chlorpyrifos, and binary mixtures of them. Environ Toxicol 25:83–93

    Google Scholar 

  • Squadrone S, Prearo M, Brizio P, Gavinelli S, Pellegrino M, Scanzio T, Guarise S, Benedetto A, Abete MC (2013) Heavy metals distribution in muscle, liver, kidney and gill of European catfish (Silurus glanis) from Italian rivers. Chemosphere 90:358–365

    Article  CAS  Google Scholar 

  • Sures B (2002) Competition for minerals between Acanthocephalus lucii and its definitive host perch (Perca fluviatilis). Int J Parasitol 32:1117–1122

    Article  CAS  Google Scholar 

  • Sures B (2008) Host-parasite interactions in polluted environments. J Fish Biol 73:2133–2142

    Article  Google Scholar 

  • Sures B, Siddall R (1999) Pomphorhynchus laevis: the intestinal acanthocephalan as a lead sink for its fish host, chub (Leuciscus cephalus). Exp Parasitol 93:66–72

    Article  CAS  Google Scholar 

  • Sures B, Dezfuli B, Krug H (2003) The intestinal parasite Pomphorhynchus laevis (Acanthocephala) interferes with the uptake and accumulation of lead (210Pb) in its fish host chub (Leuciscus cephalus). Int J Parasitol 33:1617–1622

    Article  CAS  Google Scholar 

  • Tom M, Moran O, Jabukov E, Cavari B, Rinkevitch B (1998) Molecular characterization of metallothionein-cDNA of Sparus aurata used for detecting heavy metal pollution along the Mediterranean coast of Israel. Mar Pollut Bull 36:131–137

    Article  CAS  Google Scholar 

  • Wang WX, Rainbow PS (2010) Significance of Metallothioneins in metal accumulation kinetics in marine animals. Comp Biochem Physiol C 152:1–8

    Google Scholar 

  • Weber P, Behr ER, Knorr CL, Vendruscolo DS, Flores EMM, Dressler VL, Baldisserotto B (2013) Metals in the water, sediment, and tissues of two fish species from different trophic levels in a subtropical Brazilian river. Microchem J 106:61–66

    Article  CAS  Google Scholar 

  • Yılmaz AB (2003) Levels of heavy metals (Fe, Cu, Ni, Cr, Pb, and Zn) in tissue of Mugil cephalus and Trachurus mediterraneus from Iskenderun Bay, Turkey. Environ Res 92:277–281

    Article  Google Scholar 

  • Yudkovski Y, Rogowska-Wrzesinska A, Yankelevich I, Shefer E, Herut B, Tom M (2008) Quantitative immunochemical evaluation of fish metallothionein upon exposure to cadmium. Mar Environ Res 65:427–436

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was funded by the Ministry of Higher Education, Malaysia under the Fundamental Research Grant Scheme (FRGS Vote No. 59291). The experiments and analyses were conducted at Institute of Tropical Aquaculture, Institute of Marine Biotechnology, Institute of Oceanography, and School of Fisheries and Aquaculture Sciences (University of Malaysia, Terengganu). The authors thank science officers in these institutes and school for their technical assistance.

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Authors and Affiliations

  1. Institute of Aquaculture Tropical, Universiti Malaysia Terengganu, 21030, Kuala-Terengganu, Terengganu, Malaysia

    Do Dinh Thinh, Mohamad Hafiz Farhan Abdul Rasid, Zulaikha Mat Deris & Li Lian Wong

  2. Institute of Marine Environment and Resources, Vietnam Academy of Science and Technology, 246 Danang Street, Haiphong, Vietnam

    Do Dinh Thinh

  3. Institute of Oceanography and Environment, Universiti Malaysia Terengganu, 21030, Kuala-Terengganu, Terengganu, Malaysia

    Noor Azhar Mohamed Shazili

  4. Systemic Physiological and Ecotoxicological Research, Department of Biology, University of Antwerp, Antwerp, Belgium

    Gudrun De Boeck

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  1. Do Dinh Thinh
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Correspondence to Li Lian Wong.

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Thinh, D.D., Rasid, M.H.F.A., Deris, Z.M. et al. Putative Roles for Metallothionein and HSP70 Genes in Relation with Heavy Metal Accumulation and Parasitic Cymothoid in the Fish Nemipterus furcosus . Arch Environ Contam Toxicol 71, 530–540 (2016). https://doi.org/10.1007/s00244-016-0310-8

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