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Partitioning of Cd, Zn and Fe in the Tissues and Cytosols of Blood Cockles (Anadara granosa) from the Gulf of Thailand

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Abstract

Anadara granosa is a bivalve blood cockle occurring abundantly in tropical estuarine intertidal sediments. The accumulation of Cd, Zn and Fe and their partitioning at the sub-cellular level in the cytosol has been investigated in the gills, digestive gland, body and foot of A. granosa from seven estuaries in the Gulf of Thailand. Cadmium and Zn were bioaccumulated predominantly in the gills with smaller concentrations distributed equally throughout the other tissues. Iron was present at relatively low concentrations in gills but was higher, and more evenly distributed, in the digestive gland, body and foot. The concentrations of metallothionein-like protein (MTLP) were found to be in the range 1–11 mg g−1 (dry weight) with the highest values being in the digestive gland at all sites. Partitioning of the metals in the cytosols between low molecular weight (LMW) compounds, MTLP and high molecular weight compounds (HMW) indicated that 16–39% of total Cd, 6.5–15% of total Fe and < 6% of total Zn were bound with MTLP. However, 23–27% of total Zn was bound with the HMW fraction, ascribed potentially to its association with the blood pigment haemoglobin (Hb). The metal-handling strategy, involving Zn, is likely important to blood cockles in supporting their uptake of dissolved oxygen in under-saturated tropical waters.

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References

  • Benson, B.B., and D. Krause. 1984. The concentration and isotopic fractionation of oxygen dissolved in freshwater and seawater in equilibrium with the atmosphere. Limnology and Oceanography 29 (3): 620–632.

    Article  CAS  Google Scholar 

  • Boonyatumanond, R., G. Wattayakorn, A. Togo, and H. Takada. 2006. Distribution and origins of polycyclic aromatic hydrocarbons (PAHs) in riverine, estuarine and marine sediments in Thailand. Marine Pollution Bulletin 52: 943–956.

    Article  CAS  Google Scholar 

  • Bordalo, A.A., W. Nilsumranchit, and K. Chalermwat. 2001. Water quality and uses of the Bang Pakong river (Eastern Thailand). Water Research 35 (15): 3635–3642.

    Article  CAS  Google Scholar 

  • Borgese, T.A., J.P. Harrington, D. Hoffman, R.C. San George, and R.L. Nagel. 1987. Anadara ovalis hemoglobins—distinct dissociation and ligand-binding. Comparative Biochemistry and Physiology B–Biochemistry & Molecular Biology 86: 155–165.

    Article  CAS  Google Scholar 

  • Broom, M.J. 1982. Analysis of the growth of Anadara granosa (L) (Bivalvia: Arcidae) in natural artificially seeded and experimental populations. Marine Ecology Progress Series 9: 69–79.

    Article  Google Scholar 

  • Bryan, G.W., and W.J. Langston. 1992. Bioavailability, accumulation and effects of heavy metals in sediments with special reference to United Kingdom estuaries—a review. Environmental Pollution 76 (2): 89–131.

    Article  CAS  Google Scholar 

  • CCME. 1992. Canadian Council of Ministers of the Environment. Task Force on Water Quality Guidelines of the Canadian Council of Ministers of the Environment, Eco-Health, Ottawa, Ontario, Canada.

  • Censi, P., S.E. Spoto, F. Saiano, M. Sprovieri, S. Mazzola, G. Nardone, S.I. Di Geronimo, R. Punturo, and D. Ottonello. 2006. Heavy metals in coastal water systems. A case study from the northwestern Gulf of Thailand. Chemosphere 64 (7): 1167–1176.

    Article  CAS  Google Scholar 

  • Censi, P., M. Sprovieri, F. Saiano, S.I. Di Geronimo, D. Larocca, and F. Placenti. 2007. The behaviour of REEs in Thailand’s Mae Klong estuary: suggestions from the Y/Ho ratios and lanthanide tetrad effects. Estuarine, Coastal and Shelf Science 71 (3-4): 569–579.

    Article  Google Scholar 

  • Chan, M.K., R. Othman, D. Zubir, and S. Salmijah. 2002. Induction of a putative metallothionein gene in the blood cockle Anadara granosa exposed to cadmium. Comparative Biochemistry and Physiology-C Toxicology and Pharmacology 131: 123–132.

    Article  CAS  Google Scholar 

  • Cheevaporn, V., and P. Menasveta. 2003. Water pollution and habitat degradation in the Gulf of Thailand. Marine Pollution Bulletin 47 (1-6): 43–51.

    Article  CAS  Google Scholar 

  • Cheevaporn, V., G.S. Jacinto, and M.L. San Diego-McGlone. 1995. Heavy metal fluxes in Bang Pakong river estuary, Thailand: sedimentary vs diffusive fluxes. Marine Pollution Bulletin 31 (4-12): 290–294.

    Article  CAS  Google Scholar 

  • Choi, K.Y., S.H. Kim, and H.T. Chon. 2012. Relationship between total concentration and dilute HCl extraction of heavy metals in sediments of harbors and coastal areas in Korea. Environmental Geochemistry and Health 34 (2): 243–250.

    Article  CAS  Google Scholar 

  • Dash, S., G.J. Brewer, and F.J. Oelshleger. 1974. Effect of zinc on haemoglobin binding by red blood cell membranes. Nature 250 (5463): 251–252.

    Article  CAS  Google Scholar 

  • Davenport, J., and T.M. Wong. 1986. Responses of the blood cockle Anadara granosa (L.) (Bivalvia Arcidae) to salinity, hypoxia and aerial exposure. Aquaculture 56 (2): 151–162.

    Article  Google Scholar 

  • Eapen, J.T., and B. Patel. 1989. Haematological evaluation of naphthalene intoxication in the tropical arcid blood clam Anadara granosa. Marine Biology 100 (2): 223–226.

    Article  CAS  Google Scholar 

  • Edward, F.B., C.K. Yap, A. Ismail, and S.G. Tan. 2009. Interspecific variation of heavy metal concentrations in the different parts of the tropical intertidal bivalves. Water, Air, and Soil Pollution 196 (1-4): 297–309.

    Article  CAS  Google Scholar 

  • FAO Yearbook. 2016. FAO Fishery and Aquaculture Statistics 2014. Rome, Italy.

  • Giguére, A., Y. Couillard, P.G.C. Campbell, O. Perceval, L. Hare, B. Pinel-Alloul, and J. Pellerin. 2003. Steady state distribution of metals amongst metallothionein and other cytosolic ligands and links to cytotoxicity in bivalves living along a polymetallic gradient. Aquatic Toxicology 64 (2): 185–200.

    Article  CAS  Google Scholar 

  • Gilman, J.G., and G.J. Brewer. 1978. The oxygen-linked zinc binding site of human haemoglobin. Biochemistry Journal 169 (3): 625–632.

    Article  CAS  Google Scholar 

  • Ibrahim, N. 1995. Trace element content of Malaysian cockles (Anadara granosa). Food Chemistry 54 (2): 133–135.

    Article  CAS  Google Scholar 

  • Islam, M., and M. Tanaka. 2004. Impacts of pollution on coastal and marine ecosystems including coastal and marine fisheries and approach for management: a review and synthesis. Marine Pollution Bulletin 48 (7-8): 624–649.

    Article  CAS  Google Scholar 

  • Jacob, C., W. Maret, and B.L. Vallee. 1998. Control of zinc transfer between thionein, metallothionein and zinc proteins. Proceedings of the National Academy of Sciences USA 5: 3489–3494.

    Article  Google Scholar 

  • Kalfakakou, V., and T.J.B. Simons. 1990. Anionic mechanisms of zinc uptake across the human red cell membrane. Journal of Physiology 421 (1): 485–497.

    Article  CAS  Google Scholar 

  • Kiefer, L.L., S.A. Paterno, and C.A. Fierke. 1995. Hydrogen-bond network in the metal-binding site of carbonic-anhydrase enhances zinc affinity and catalytic efficiency. Journal of the American Chemical Society 117: 6831–6837.

    Article  CAS  Google Scholar 

  • Krężel, A., and W. Maret. 2007. Dual nanomolar and picomolar Zn(II) binding properties of metallothionein. Journal of the American Chemical Society 129 (35): 10911–10921.

    Article  CAS  Google Scholar 

  • Langston, W.J., and M. Zhou. 1986. Evaluation of the significance of metal-binding proteins in the gastropod Littorina littorea. Marine Biology 92 (4): 505–515.

    Article  CAS  Google Scholar 

  • Langston, W.J., and M. Zhou. 1987. Cadmium accumulation, distribution and elimination in the bivalve Macoma baltica: neither metallothionein nor metallothionein-like proteins are involved. Marine Environmental Research 21 (3): 225–237.

    Article  CAS  Google Scholar 

  • Langston, W.J., M.J. Bebianno, and G.R. Burt. 1998. Metal handling strategies in molluscs. In Metal metabolism in aquatic environments, ed. W.J. Langston and M.J. Bebianno, 219–283. Dordrecht: Kluwer Academic Publishers.

    Chapter  Google Scholar 

  • Langston, W.J., B.S. Chesman, G.R. Burt, N.D. Pope, and J. McEvoy. 2002. Metallothionein in liver of eels Anguilla anguilla from the Thames Estuary: an indicator of environmental quality? Marine Environmental Research 53 (3): 263–293.

    Article  CAS  Google Scholar 

  • Marigómez, I., M. Soto, M.P. Cajaraville, E. Angulo, and L. Giamberini. 2002. Cellular and subcellular distribution of metals in molluscs. Microscopy Research and Technique 56 (5): 358–392.

    Article  Google Scholar 

  • McLaren, R.G., K. Kanjanapa, P. Navasumrit, S.R. Gooneratne, and M. Ruchirawat. 2004. Cadmium in the water and sediments of the Chao Phraya river and associated waterways, Bangkok, Thailand. Water, Air and Soil Pollution 154 (1-4): 385–398.

    Article  CAS  Google Scholar 

  • Mirasadeghi, S.A., M.P. Zakaria, C.K. Yap, and F. Gobas. 2013. Evaluation of the potential bioaccumulation ability of the blood cockle (Anadara granosa L.) for assessment of environmental matrices of mudflats. Science of the Total Environment 454-455: 584–597.

    Article  CAS  Google Scholar 

  • Patel, B., V.S. Bangera, S. Patel, and M.C. Balani. 1985. Heavy metals in Bombay harbour. Marine Pollution Bulletin 16 (1): 22–28.

    Article  CAS  Google Scholar 

  • Pengthamkeerati, P., N. Kormkanitnan, S. Sawangarreruks, N. Wanichacheva, C. Wainiphithapong, and N. Sananwai. 2013. Assessment of heavy metals in sediments of the Don Hoi area in the Mae Klong estuary, Thailand. Journal of Environmental Science & Health, Part A, Toxic/Hazardous Substances and Environmental Engineering 48: 1356–1364.

    Article  CAS  Google Scholar 

  • Perutz, M.F. 1979. Regulation of oxygen affinity of hemoglobin: influence of structure of the globin on the heme iron. Annual Review of Biochemistry 48: 327–386.

    Article  CAS  Google Scholar 

  • Phillips, D.J.H., and K. Muttarasin. 1985. Trace metals in bivalve molluscs from Thailand. Marine Environmental Research 15 (3): 215–234.

    Article  CAS  Google Scholar 

  • Pradit, S., M.A.N. Shazili, P. Towatana, and W. Saengmanee. 2016. Accumulation of trace metals in Anadara granosa and Anadara inaequivalis from Pattani Bay and the Setiu Wetlands. Bulletin of Environmental Contamination and Toxicology 96: 472–477.

    Article  CAS  Google Scholar 

  • Rifkind, J.M., and J.M. Heim. 1977. Interaction of zinc with haemoglobin: binding of zinc and the oxygen affinity. Biochemistry 16 (20): 4438–4443.

    Article  CAS  Google Scholar 

  • Ruiz, C., J. Mendieta, and A.R. Rodriguez. 1995. The electrochemical behaviour of cd, Zn thioneins depending on the solution pH using differential pulse polarography. Analytica Chimica Acta 305 (1-3): 285–294.

    Article  CAS  Google Scholar 

  • Sany, S.B.T., R. Hashim, M. Rezayi, A. Salleh, M.A. Rahman, O. Safan, and A. Sasekumar. 2014. Human health risk of polycyclic aromatic hydrocarbons from consumption of blood cockles and exposure to contaminated sediments and water along the Klang Strait, Malaysia. Marine Pollution Bulletin 84 (1-2): 268–279.

    Article  CAS  Google Scholar 

  • Serra, R., E. Crapené, A.C. Marcantonio, and G. Isani. 1995. Cadmium accumulation and Cd-binding proteins in the bivalve Scapharca inaequivalvis. Comparative Biochemistry and Physiology 11C: 165–174.

    Google Scholar 

  • Silva, C.A.R., B.D. Smith, and P.S. Rainbow. 2006. Comparative biomonitors of coastal trace metal contamination in tropical South America (N. Brazil). Marine Environmental Research 61 (4): 439–455.

    Article  CAS  Google Scholar 

  • Smith, J., M. Bibikova, F.G. Whitby, A.R. Reddy, S. Chandrasegaran, and D. Carroll. 2000. Requirements for double-strand cleavage by chimeric restriction enzymes with zinc finger DNA-recognition domains. Nucleic Acids Research 28 (17): 3361–3369.

    Article  CAS  Google Scholar 

  • de Sousa Machado, A.A., K. Spencer, W. Kloas, M. Toffolon, and C. Zarfl. 2016. Metal fate and effects in estuaries: a review and conceptual model for better understanding toxicity. Science of the Total Environment 541: 268–281.

    Article  CAS  Google Scholar 

  • Taylor, A.M., and W.A. Maher. 2012. Exposure-dose-response of Anadara trapezia to metal contaminated estuarine sediments. 1. Cadmium spiked sediments. Aquatic Toxicology 109: 234–242.

    Article  CAS  Google Scholar 

  • Thillart, van den G., van G. Lieshout, K. Storey, P. Cortesi, and de A. Zwaan. 1992. Influence of long-term hypoxia on the energy metabolism of the haemoglobin-containing bivalve Scapharca inaequivalvis critical O2 levels for metabolic depression. Journal of Comparative Physiology B 162 (4): 297–304.

    Article  Google Scholar 

  • Tu, N.P.C., N.N. Ha, T. Agusa, T. Ikemoto, B.C. Tuyen, S. Tanabe, and I. Takeuchi. 2011. Trace elements in Anadara spp. (Mollusca: Bivalva) collected along the coast of Vietnam, with emphasis on regional differences and human health assessment. Fishery Science 77: 10331043.

    Article  CAS  Google Scholar 

  • Wallace, W.G., B.-G. Lee, and S.N. Luoma. 2003. Subcellular compartmentalization of Cd and Zn in two bivalves. I. Significance of metal-sensitive fractions (MSF) and biologically detoxified metal (BDM). Marine Ecology Progress Series 249: 183–197.

    Article  CAS  Google Scholar 

  • Weber, R.E., and S.N. Vinogradov. 2001. Nonvertebrate hemoglobins: functions and molecular adaptations. Physiological Reviews 81 (2): 569–628.

    Article  CAS  Google Scholar 

  • Wijaya, A.R., A.K. Ouchi, K. Tanaka, M.D. Cohen, S. Sirirattanachai, R. Shinjo, and S. Ohde. 2013. Evaluation of heavy metal contents and Pb isotopic compositions in the Chao Phraya river sediments: implications for anthropogenic inputs from urbanised areas, Bangkok. Journal of Geochemical Exploration 126-127: 45–54.

    Article  CAS  Google Scholar 

  • Yap, C.K., Y. Hatta, F.B. Edward, and S.G. Tan. 2008. Comparison of heavy metal concentrations (Cd, Cu, Fe, Ni and Zn) in the shells and different soft tissues of Anadara granosa collected from Jeram, Kuala Juru and Kuala Kurau, Peninsular Malaysia. Pertanika Journal of Tropical Agriculture 31: 205–215.

    Google Scholar 

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Acknowledgments

Dr. C. Rattikunsukha thanks the Ministry of Resources and Environment, Bangkok, Thailand for funds to carry out this research and to colleagues at the Pollution Control Department for field and laboratory support. Professor G.E. Millward thanks the Scientific Committee on Oceanic Research (SCOR) for a Visiting Scholarship to Walailak University, Thailand. Dr. W. Langston is grateful to the Marine Biological Association for an Associate Fellowship and the facilities to carry out this work.

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Authors and Affiliations

  1. School of Engineering and Resources, Walailak University, Tha Sala, 80161, Thailand

    C. Rattikansukha

  2. Marine Institute, Plymouth University, Drake Circus, Plymouth, PL4 8AA, UK

    G. E. Millward

  3. Marine Biological Association of the UK, Citadel Hill, Plymouth, PL1 2PB, UK

    W. J. Langston

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  1. C. Rattikansukha
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  2. G. E. Millward
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  3. W. J. Langston
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Correspondence to G. E. Millward.

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Communicated by Wen-Xiong Wang

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Rattikansukha, C., Millward, G.E. & Langston, W.J. Partitioning of Cd, Zn and Fe in the Tissues and Cytosols of Blood Cockles (Anadara granosa) from the Gulf of Thailand. Estuaries and Coasts 42, 237–249 (2019). https://doi.org/10.1007/s12237-018-0452-1

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