Tissue partitioning of micro-essential metals in the vent bivalve Bathymodiolus azoricus and associated organisms (endosymbiont bacteria and a parasite polychaete) from geochemically distinct vents of the Mid-Atlantic Ridge

Abstract

Hydrothermal communities are built on highly specialised organisms possessing effective adaptation mechanisms to tolerate elevated levels of toxic heavy metals typical of these extreme habitats. Bioavailability and tissue compartmentalisation of micro-essential metals (Cu, Zn, and Fe) were investigated in the bivalve Bathymodiolus azoricus from three geochemically distinct hydrothermal vents (Rainbow, Lucky Strike, Menez Gwen). Additionally , in order to make inferences on the effect of biological interactions on the metal uptake, the bivalves' endosymbiont bacteria and commensal parasite Branchipolynoe seepensis were analysed for metal bioaccumulation. Micro-essential metal concentrations in byssus threads exceeded many-fold concentrations in the gill and digestive gland, which in turn were consistently one order of magnitude above levels measured in the mantle. In spite of its high metal concentrations, the byssus is unlikely to be an active bioaccumulator. Its high surface to mass ratio and its binding sites for metals suggest a reversible adsorption of micro-essential metals in the vent mussel. Inter-site comparison showed highest Fe concentrations in tissues of mussels from the Rainbow site, whereas Zn and Cu in all tissues were highest in mussels from the Lucky Strike site, reflecting metal concentrations in the water surrounding macro-invertebrates at these vent sites. The omnipresence of the commensal parasite polychaete in gills of B. azoricus from the Lucky Strike vent field, unlike the other sites, is suggested to be an adaptation to the typically elevated Fe concentrations in the water column near mussel beds. Unprecedented Fe concentrations measured in the digestive gland of mussels from the Rainbow site (4000 μg g − 1 , three times higher than levels in bivalves from polluted sites) call for further post-capture ecotoxicological investigations of potentially novel Fe-handling strategies. We provide the first information on the bioaccumulation potential of hydrothermal organisms by calculation of concentration factors for Cu, Zn and Fe in the gills of the bivalve host and also in its endosymbiont and/or parasites. Adaptation strategies (biochemical, physiological, morphological and life-history adaptations) of vent organisms to elevated levels of micronutrients and non-essential metallic elements are discussed.