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Beinart, Roxanne Abra

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Beinart

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Roxanne Abra

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Beinart, Roxanne Abra
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    Linking bacterial symbiont physiology to the ecology of hydrothermal vent symbioses
    (2014-02-25) Beinart, Roxanne Abra; Girguis, Peter R.; Cavanaugh, Colleen; Knoll, Andrew; Marx, Christopher
    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.
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    Evidence for the Role of Endosymbionts in Regional-Scale Habitat Partitioning by Hydrothermal Vent Symbioses
    (Proceedings of the National Academy of Sciences, 2012) Beinart, Roxanne Abra; Sanders, Jon G.; Faure, Baptiste; Sylva, Sean P.; Lee, Raymond W.; Becker, Erin L.; Gartman, Amy; Luther, George W.; Seewald, Jeffrey S.; Fisher, Charles R.; Girguis, Peter
    Deep-sea hydrothermal vents are populated by dense communities of animals that form symbiotic associations with chemolithoautotrophic bacteria. To date, our understanding of which factors govern the distribution of host/symbiont associations (or holobionts) in nature is limited, although host physiology often is invoked. In general, the role that symbionts play in habitat utilization by vent holobionts has not been thoroughly addressed. Here we present evidence for symbiont-influenced, regional-scale niche partitioning among symbiotic gastropods (genus Alviniconcha) in the Lau Basin. We extensively surveyed Alviniconcha holobionts from four vent fields using quantitative molecular approaches, coupled to characterization of high-temperature and diffuse vent-fluid composition using gastight samplers and in situ electrochemical analyses, respectively. Phylogenetic analyses exposed cryptic host and symbiont diversity, revealing three distinct host types and three different symbiont phylotypes (one ε-proteobacteria and two γ-proteobacteria) that formed specific associations with one another. Strikingly, we observed that holobionts with ε-proteobacterial symbionts were dominant at the northern fields, whereas holobionts with γ-proteobacterial symbionts were dominant in the southern fields. This pattern of distribution corresponds to differences in the vent geochemistry that result from deep subsurface geological and geothermal processes. We posit that the symbionts, likely through differences in chemolithoautotrophic metabolism, influence niche utilization among these holobionts. The data presented here represent evidence linking symbiont type to habitat partitioning among the chemosynthetic symbioses at hydrothermal vents and illustrate the coupling between subsurface geothermal processes and niche availability.