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Arsenic toxicity in a sediment-dwelling polychaete: detoxification and arsenic metabolism

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Abstract

The accumulation, subcellular distribution and speciation of arsenic in the polychaete Arenicola marina were investigated under different laboratory exposure conditions representing a range of metal bioavailabilities, to gain an insight into the physiological mechanisms of how A. marina handles bioaccumulated arsenic and to improve our understanding of the potential ecotoxicological significance of bioaccumulated arsenic in this deposit-feeder. The exposure conditions included exposure to sublethal concentrations of dissolved arsenate, exposure to sublethal concentrations of sediment-bound metal mining mixtures, and exposure to lethal concentrations of sediment-bound metal mining mixtures and arsenic- and multiple metal-spiked sediments. The sub-lethal exposures indicate that arsenic bioaccumulated by the deposit-feeding polychaete A. marina is stored in the cytosol as heat stable proteins (~50%) including metallothioneins, possibly as As (III)-thiol complexes. The remaining arsenic is mainly accumulated in the fraction containing cellular debris (~20%), with decreasing proportions accumulated in the metal-rich granules, organelles and heat-sensitive proteins fractions. A biological detoxified metal compartment including heat stable proteins and the fraction containing metal-rich granules is capable of binding arsenic coming into the cells at a constant rate under sublethal arsenic bioavailabilities. The remaining arsenic entering the cell is bound loosely into the cellular debris fraction, which can be subsequently released and diverted to an expanding detoxified pool. Our results suggest that a metal sensitive compartment comprising the cellular debris, enzymes and organelles fractions may be more representative of the toxic effects observed.

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Acknowledgments

This project was financially supported by the European Community’s Seventh Framework Program through a Marie Curie Intra-European Fellowship to M.C. Casado-Martinez (FP7/2007-2013 under grant agreement no. PIEF-GA-2008-219781), and from the Ecochemistry Laboratory, University of Canberra, Australia. The authors are grateful to Catherine Unsworth from the EMMA Laboratories at the Natural History Museum for the metal analyses and her advice for the preparation of subcellular fraction solutions prior to metal quantification and Dr Lauren Howard for the SEM characterisation of precipitates. MCCM acknowledges the financial support from the multidisciplinary research and education project Environmental Waste Management (EWMA) during the writing of this manuscript at the University of Tromsø.

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  1. M. C. Casado-Martinez

    Present address: Department of Arctic and Marine Biology, Faculty of Biosciences, Fishery and Economics, University of Tromsø, 9037, Tromsø, Norway

Authors and Affiliations

  1. Department of Zoology, The Natural History Museum, Cromwell Rd, London, SW7 5BD, UK

    M. C. Casado-Martinez, B. D. Smith & P. S. Rainbow

  2. Ecochemistry Laboratory, Institute for Applied Ecology, University of Canberra, Australian Capital Territory 2601, Canberra, Australia

    E. Duncan & W. A. Maher

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  1. M. C. Casado-Martinez
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Correspondence to M. C. Casado-Martinez.

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Casado-Martinez, M.C., Duncan, E., Smith, B.D. et al. Arsenic toxicity in a sediment-dwelling polychaete: detoxification and arsenic metabolism. Ecotoxicology 21, 576–590 (2012). https://doi.org/10.1007/s10646-011-0818-7

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