Sources and forms of trace metals taken up by hydrothermal vent mussels, and possible adaption and mitigation strategies

Abstract

Ventmussels are ubiquitous inmost hydrothermal fields, despite the metalrich environment they live in, with dissolved metal ions, colloidal and particulate metal forms in concentrations orders of magnitude higher than in ambient seawater. Different studies at various hydrothermally active sites on theMid-Atlantic Ridge and East Pacific Rise have shown that metal concentrations in the tissues of the mussel generally reflect metal loads of their environments, displaying spatial gradients, with bioconcentration factors up to 105. Gills and digestive glands accumulate the highest amounts of metals, which is related to their direct role in food uptake, while mantle and foot show moderate metal enrichments. Metal uptake in the form of mineral particles has been identified as an important source of metals in the mussel tissues. While closer to the active vent sites metal sulfides forming during mixing of hot hydrothermal fluid and seawater are more dominant, with increasing distance iron oxides with metals adsorbed from seawater play a more important role for metal accumulation by the vent mussels. Although the shells of hydrothermal mussels have low metal concentrations compared to the soft tissues, they are a record of the chemical composition of the seawater-hydrothermal fluidmixture. Different species of Bathymodiolus mussels from the Pacific and Atlantic display similar metal accumulations and adaptation strategies, while vent clams show some similarities, but also some differences compared to Bathymodiolus.Some of the metals (e.g., alkali and earth alkaline elements, Zn and Mn) taken up by the mussels appear to be bioregulated. They are essential elements and their concentration ranges in the mussel tissues are usually less variable than other heavy metals, although their variability in the fluids is comparably high. Strategies of thevent mussels to cope with high concentrations of potentially toxic metals such as Cu, Cd, and Hg include binding to metallothioneins, which are strongly metalbinding proteins, and possibly immobilization of the metals in the form of granules stored in the tissue. These ways of mitigating heavy metal toxicity have also been found for other organisms including non-vent bivalves. Another yet to be proven possibility is the excretion of organic ligands into the water which binds to the metals and makes them less bioavailable. Due to the challenges of sampling hydrothermal vent mussels and their environmental compartments, many questions remain open or hypotheses still need to be tested; studies often differ in their approach and a comparison of results is not straightforward. Hence, more systematic studies focusing on specific metal groups, experiments under defined conditions and a comparison of different species of vent mussels are desirable. Apart from the many open questions that refer directly to the understanding of metal accumulation and adaptation of hydrothermal vent mussels to their challenging environment, a better knowledge in this field may also help to support other fields of research. These include estimation of hydrothermal metal fluxes into the ocean and elucidation of survival strategies of organisms in other metal-rich environments.