Sulfide acquisition by deep-sea hydrothermal vent tubeworm hemoglobins

by Flores, Jason Francisco.

The reducing environments of deep-sea hydrothermal vents and cold seeps are a stark contrast to the rest of the deep sea. Animals associated with these seafloor oases derive their energy from the oxidation of reduced sulfide and methane. Among the best-studied animals are vestimentiferan tubeworms. Tubeworms are obligate partners with chemoautotrophic endosymbiotic bacteria and must supply their symbionts with oxygen and sulfide from the external environment. The gas exchange organ of vestimentiferan tubeworms has only been studied in one species, Riftia pachyptila. The gill (plume) of this species has a high mass specific surface area and low diffusion distance. Both of these attributes, in concert with gradients of sulfide and oxygen, make a high diffusion rate possible. To offset the influx of oxygen and sulfide, uptake and delivery of these chemical species in vestimentiferans is facilitated by high concentrations of large extracellular hemoglobins (Hbs) circulating in the vascular blood and dissolved in the coelomic fluid. Again, the structure and function of the Hbs from the hydrothermal vent tubeworm R. pachyptila are the most well known. There are at least two Hb types, a 3600-kDa hexagonal bi-layer Hb and a spherical 400-kDa Hb. Both Hbs bind sulfide and oxygen reversibly and can transport both chemical species simultaneously to their endosymbionts. Ligand binding by the Hbs prevents sulfide from poisoning the host’s mitochondria by keeping free sulfide concentrations low while still delivering oxygen to the same organelles and tissues. The information gained from studies on R. pachyptila has served as a basis for general knowledge of the ecology and physiology of all hydrothermal vent tubeworms. iv This dissertation addresses the sulfide uptake properties of vestimentiferan tubeworms by first investigating the mechanism of sulfide binding in the Hbs of R. pachyptila and second comparing the sulfide uptake abilities of R. pachyptila to the sulfide binding abilities of the polymorphic hydrothermal vent tubeworm Ridgeia piscesae from the Juan de Fuca Ridge (JdFR). Because R. piscesae lives around hydrothermal vents with different diffuse flow conditions that apparently induce phenotypic variation, this tubeworm is also a good model for investigating the effects of changes in environment on tubeworm physiology. There are five chapters contained within this dissertation. Chapter I is a review of the literature relevant to this thesis. This includes an overview of animals living in low oxygen and high sulfide environments as well as the biology of vestimentiferan tubeworms, including a review of the current knowledge of vestimentiferan Hbs.