Stimulatory effect of sulphide on thiotaurine synthesis in three hydrothermal-vent species from the East Pacific Rise

Abstract

Symbiotic associations between marine invertebrates and sulphur-oxidising bacteria are a common feature in communities from sulphide-rich environments, such as those flourishing in the vicinity of hydrothermal vents. While the bacterial endosymbionts provide the host with an undoubted nutritional advantage, their presence also requires specific adaptations for the transport and storage of sulphide, which is a potent toxin of aerobic respiration. Although different mechanisms such as the reversible binding of sulphide to serum binding proteins or its oxidation to less toxic forms have been described, many questions still remained unanswered. In the last decade, large amounts of thiotaurine, an unusual sulphur-amino acid, have been reported in sulphur-based symbioses from hydrothermal vents and cold seeps. Compounds such as thiotaurine are known to take part in trans-sulphuration reactions, so the involvement of thiotaurine in sulphide metabolism has been suggested. We present here an experimental study on thiotaurine biosynthesis in three sulphur-oxidising symbiont-bearing species from the East Pacific Rise: the vesicomyid Calyptogena magnifica, the mytilid Bathymodiolus thermophilus and the vestimentiferan Riftia pachyptila. In all three species, thiotaurine synthesis is stimulated in vitro by an input of sulphide, as well as by thiosulphate in B. thermophilus.Several distinct metabolic pathways seem to occur, however, since hypotaurine is the only precursor in the bivalves C. magnified and B. thermophilus, whereas thiotaurine is also produced from taurine in R. pachyptila. Hypotaurine (NH2-CH2-CH2-SO 2H) and thiotaurine (NH2-CH2-CH 2-SO2SH) are two free sulphur amino acids whose chemical formulae differ by only one atom of sulphur. It appears that the extent of thiotaurine synthesis is strongly dependent on the initial equilibrium between these two amino acids, since the strongest thiotaurine synthesis rates are found in tissues with the lowest initial thiotaurine concentration. Moreover, the lack of any effect of sulphide in symbiont-free tissues and in gills of the methanotrophic mussel Bathymodiolus childressi reinforces the assumption that thiotaurine synthesis is a specific adaptation to the thiotrophic mode of life. While the precise function (i.e. transport and/or storage of sulphide) of hypotaurine and thiotaurine has yet to be established, our results strongly support a general role for these free amino acids in the metabolism of sulphide in hydrothermal-vent thiotrophic symbioses.