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

Abstract

In contrast to the generally bare aspect of the deep-sea bottom, dense and rich faunistic communities have flourished in the vicinity of hydrothermal vents (Hessler and Kaharl, 1995). The root of these unique ecosystems are chemoautotrophic bacteria, which oxidise the geothermal sulphide released in hydrothermal fluids (Jannasch, 1995). Many of the metazoan species that dominate these extreme habitats live in association with intracellular sulphur-oxidising symbionts. Such endosymbioses are found in mytilid and vesicomyid bivalves, provannid gastropods and vestimentiferan tubeworms (for a list of references, see Fisher, 1995). The host is provided with a regular input of organic matter produced by the symbionts, but also has to transport in its tissues the poisonous compound used by the bacteria as energetic substrate (i.e. sulphide). These symbioses therefore require structural and functional adaptations by the host for the uptake, transport and storage of sulphide (Powell and Somero, 1986). For example, in the vestimentiferan tubeworm Riftia pachyptila, sulphide is taken up from the surrounding seawater across the plume; the sulphide is then reversibly bound in the blood to extracellular haemoglobins and transported to the trophosome, where the bacteria are located. The high affinity of these haemoglobins ensures that internal sulphide can reach very high levels in the body fluids of vestimentiferans (e.g. up 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. magnifica and B. thermophilus, whereas thiotaurine is also produced from taurine in R. pachyptila. Hypotaurine (NH 2-CH2-CH2-SO2H)...

Hypotaurine and sulfhydryl-containing antioxidants reduce H2S toxicity in erythrocytes from a marine invertebrate

“…However, HT can also react with sulfide directly, forming thiotaurine (ThT) in vitro (Cavallini et al, 1963). If this reaction occurs in vivo, it would scavenge free sulfide and might, therefore, reduce sulfide toxicity by acting as a sulfide 'buffer' (Alberic and Boulegue, 1990;Brand et al, 2007;Joyner et al, 2003;Pruski and Fiala-Medioni, 2003;Rosenberg et al, 2006). In sulfide-exposed animals that lack sulfide-oxidizing endosymbionts, the resulting ThT may be enzymatically recycled back to HT, thereby releasing sulfide at a rate that allows detoxification through other mechanisms (Rosenberg et al, 2006).…”

“…In sulfide-exposed animals that lack sulfide-oxidizing endosymbionts, the resulting ThT may be enzymatically recycled back to HT, thereby releasing sulfide at a rate that allows detoxification through other mechanisms (Rosenberg et al, 2006). In sulfide-exposed animals with sulfideoxidizing endosymbiotic bacteria, the conversion of HT to ThT may provide a mechanism to transport sulfide to the endosymbionts, which would then convert ThT back to sulfide and HT (Pranal et al, 1995;Pruski and Fiala-Medioni, 2003;Pruski et al, 1997;Pruski et al, 2001;Pruski et al, 2000b). Accordingly, Pranal and colleagues proposed that the ratio of ThT to HT in tissues represents the extent of that animal's recent sulfide exposure (Pranal et al, 1995).…”

Thiotaurine and hypotaurine contents in hydrothermal‐vent polychaetes without thiotrophic endosymbionts: correlation With sulfide exposure

“…The source of SH could be a free radical, a ligand donated by a protein R as R-SSH, or a moiety donated by glutathione-SSH. Synthesis of thiotaurine from hypotaurine appears to be enzymatic and is reversible (Pruski and Fiala-Médioni, 2003). Thus, thiotaurine might serve to store sulfide nontoxically within cells, and release it as the endosymbionts deplete free sulfide, thus acting as a sulfide ''buffer''.…”

Comparison of taurine related compounds in deep- and shallow-water mussel species

“…The thiotaurine/(hypotaurine+thiotaurine) ratio has been proposed to be an indicator of sulfide exposure (Pruski et al 2003, Brand et al 2007. In this study, the B. septemdierum gill had the highest value, and the B. platifrons gill had a slightly higher value than that of M. galloprovincialis.…”

“…Therefore, the host species can safely store toxic hydrogen sulfide obtained from the environment by converting it to thiotaurine. Furthermore, as the reaction is reversible, the host species are able to provide sulfide to the thiotrophic symbionts by converting thiotaurine back to hypotaurine (Pruski et al 2001(Pruski et al , 2003. Indeed, thiotaurine is mainly found in symbiont-bearing tissues, such as the gill of mussels and clams and the trophosome of tube worms (Brand et al 2007).…”