Linking bacterial symbiont physiology to the ecology of hydrothermal vent symbioses

Abstract

Symbioses between prokaryotes and eukaryotes are ubiquitous in our biosphere, nevertheless, the effects of such associations on the partners' ecology and evolution are poorly understood. At hydrothermal vents, dominant invertebrate species typically host bacterial symbionts, which use chemical energy to fix carbon to nourish their hosts and themselves. In this dissertation, I present evidence that symbiont metabolism plays a substantive, if not major, role in habitat use by vent symbioses. A study of nearly 300 individuals of the symbiotic snail Alviniconcha sp. showed specificity between three host species and three specific symbiont phylotypes, as well as a novel lineage of Oceanospirillales. Additionally, this study revealed a structured distribution of each Alviniconcha-symbiont combination across ~300 km of hydrothermal vents that exhibited a gradient in geochemical composition, which is consistent with the physiological tendencies of the specific symbiont phylotypes. I also present a comparison of the in situ gene expression of the symbionts of Alviniconcha across that same geochemical gradient, which further implicates symbiont energy and nitrogen metabolism in governing the habitat partitioning of Alviniconcha. Finally, I present data that allies productivity and sulfur metabolism in three coexisting vent symbioses, demonstrating specific interaction with the environment. Three symbioses, namely the snails Alviniconcha and Ifremeria, and the mussel Bathymodiolus, are found around vents with differing concentrations of sulfide, thiosulfate and polysulfide. Using high-pressure, flow-through incubations and stable isotopic tracers, I quantified symbiont productivity via sulfide and thiosulfate oxidation, and provided the first demonstration of thiosulfate-dependent autotrophy in intact hydrothermal vent symbioses. I further demonstrated that vent symbioses can excrete thiosulfate and/or polysulfides, implicating them in substantively influencing the sulfur chemistry of their habitats. In summary, this dissertation demonstrates the importance of symbiont physiology to the ecology of prokaryote-eukaryote symbioses by revealing that symbiont activity may be critically important to the distribution of symbioses among specific niches, as well as can alter the geochemical environment through uptake and excretion of chemicals.