Calvin-Benson cycle and sulphide oxidation enzymes in animals from sulphide-rich habitats

Abstract

The role of sulphide oxidation-driven production of reduced carbon in the nutrition of animals adapted to life in sulphide-rich habitats such as the deep-sea hydrothermal vents and intertidal mudflats has been a topic of recent interest^1–4. Chemoautotrophic sulphide-oxidizing bacteria have been isolated from samples of sulphide-rich vent water^5–8, and it has been suggested that these could provide a food source for filter-feeding animals that live at the vents. The recent discovery of prokaryotic cells⁹ and activities of sulphide-oxidizing enzymes (which generate reducing power and ATP) and Calvin—Benson cycle enzymes¹⁰ within the trophosome tissue of the large vestimentiferan tubeworm of the vents, Riftia pachyptila Jones (Phylum Pogonophora)¹¹ suggests that sulphide-oxidizing chemoauto-trophic bacteria exist in a symbiotic relationship with at least this vent species. This discovery led us to measure enzyme activities associated with sulphide oxidation, the Calvin-Benson cycle and nitrate reduction in a variety of other vestimentiferan tube-worms and bivalve molluscs which occur in sulphide-rich habitats. All the vestimentiferan worms and several of the molluscs were found to contain these enzymatic activities, suggesting that the putative animal-bacterial symbiosis first described in Riftia pachyptila may be of widespread occurrence in species living in environments offering simultaneous access to sulphide and oxygen.