Thiotaurine is a biomarker of sulfide‐based symbiosis in deep‐sea bivalves

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)...

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

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

Pruski

Fiala-Médioni

2003

“…This led to a proposal that thiotaurine is a marker of symbiosis (Pruski et al, 2000b). Studies in our laboratory suggest the hypotaurine-thiotaurine reaction has a greater, body-wide cytoprotective role against sulfide in some species: we found that two species of vent gastropods without endosymbionts have both hypotaurine and thiotaurine as major osmolytes (Fig.·1, snail vent bar) and that the ratio of thiotaurine to hypotaurine decreases in animals held in the laboratory without sulfide (Rosenberg et al, 2003).…”

Section: Antioxidationmentioning

confidence: 99%

Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses

Yancey

2005

1,561

1,272

SUMMARY Organic osmolytes are small solutes used by cells of numerous water-stressed organisms and tissues to maintain cell volume. Similar compounds are accumulated by some organisms in anhydrobiotic, thermal and possibly pressure stresses. These solutes are amino acids and derivatives,polyols and sugars, methylamines, methylsulfonium compounds and urea. Except for urea, they are often called `compatible solutes', a term indicating lack of perturbing effects on cellular macromolecules and implying interchangeability. However, these features may not always exist, for three reasons. First, some of these solutes may have unique protective metabolic roles, such as acting as antioxidants (e.g. polyols, taurine, hypotaurine),providing redox balance (e.g. glycerol) and detoxifying sulfide (hypotaurine in animals at hydrothermal vents and seeps). Second, some of these solutes stabilize macromolecules and counteract perturbants in non-interchangeable ways. Methylamines [e.g. trimethylamine N-oxide (TMAO)] can enhance protein folding and ligand binding and counteract perturbations by urea (e.g. in elasmobranchs and mammalian kidney), inorganic ions, and hydrostatic pressure in deep-sea animals. Trehalose and proline in overwintering insects stabilize membranes at subzero temperatures. Trehalose in insects and yeast,and anionic polyols in microorganisms around hydrothermal vents, can protect proteins from denaturation by high temperatures. Third, stabilizing solutes appear to be used in nature only to counteract perturbants of macromolecules,perhaps because stabilization is detrimental in the absence of perturbation. Some of these solutes have applications in biotechnology, agriculture and medicine, including in vitro rescue of the misfolded protein of cystic fibrosis. However, caution is warranted if high levels cause overstabilization of proteins.

“…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).…”

Section: Introductionmentioning

confidence: 99%

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

Ortega

Julian

2008

SUMMARYHypotaurine (HT) has been proposed to reduce sulfide toxicity in some deep-sea invertebrates by scavenging free radicals produced from sulfide oxidation or by scavenging sulfide via the reaction of HT with sulfide, forming thiotaurine (ThT). We tested whether HT or several antioxidants could reduce the total dissolved sulfide concentration in buffered seawater exposed to H 2 S, and whether HT, ThT or antioxidants could increase the viability of Glycera dibranchiata erythrocytes exposed to H 2 S in vitro. We found that 5 and 50 mmol l -1 HT reduced the dissolved sulfide in cell-free buffer exposed to H 2 S by up to 80% whereas the antioxidants glutathione ethyl ester (GEE) ), which contain sulfhydryl groups, increased cell viability during H 2 S exposure but to a lesser extent than HT whereas ASC, Tempol and Trolox, which do not contain sulfhydryl groups, decreased viability or had no effect. These data show that HT can protect cells from sulfide in vitro and suggest that sulfide scavenging, rather than free radical scavenging, is the most important mechanism of protection.,