Metabolic versatility of the hydrothermal vent worm Riftia pachyptila: Allying transcriptional and metabolic responses to a dynamic environment

Abstract

The hydrothermal vent tubeworm, Riftia pachyptila, having no mouth or gut, rely solely on their intracellular symbiotic chemosynthetic bacteria for nutrition. Incredibly, these organisms can achieve very high growth rates, supported solely by their symbionts’ substantial primary production. These tubeworms are found in areas where hydrothermally influenced fluid mixes with cold oxygenated bottom water, and are subject to rapid, extreme shifts in temperature, pH, oxygen, and sulfide (the latter is used by the symbionts for chemosynthesis). Tubeworms have evolved the physiological capacity to maintain a more stable internal environment, one which optimizes chemoautotrophic primary productivity by their intracellular symbionts. However, environmental variation can and does translate to changes in the availability of substrates to the symbionts, and genomic evidence suggests the symbionts may also have evolved in response to the dynamic vent environment. Here, via a suite of metabolic, biochemical, and transcriptomic analyses, I explore how symbiont metabolism responds to varying environmental conditions, and how these metabolic shifts affect primary production and, ultimately, growth. To this end, I used a high pressure respirometry system to maintain tubeworms at controlled vent-like conditions and conducted a series of experiments to explore the effects of different electron donors and availability, oxygen and nitrate limitation. In chapter 1, I test the hypothesis that the symbiont can utilize different electron donors, specifically hydrogen as well as hydrogen sulfide. The data reveal that hydrogen is not playing a key role as an electron donor, as hydrogen utilization was modest or non-existent and was never sufficient to support the observed rates of dependent processes, e.g. carbon fixation. In chapter 2, I test the hypothesis that the symbionts, which possess two pathways for carbon fixation, bias towards one carbon fixation pathway over another in response to environmental changes. I show that there is a strong metabolic response in these pathways, in which carbon fixation pathways seem to vary in relation to environmental conditions, but not to the exclusion of one over the other. In chapter 3, I explore the ways in which nitrate, a substrate that could serve either as an electron acceptor, a source of nitrogen, or both, is utilized by the association at varying conditions. I show that nitrate assimilation and primary production covary, that nitrate limitation may limit primary production, and that nitrate respiration is likely occurring, but cannot support the association when the external oxygen is limiting. Taken together, this body of work significantly advances our understanding of how the symbionts’ diverse metabolic capabilities interact with the host-symbiont association; in both challenging prior assumptions and providing a framework for how the symbiont supports the association under substrate limitation.