Physiological ecology of hydrocarbon seep tubeworms from the Gulf of Mexico

by Dattagupta, Sharmishtha.

Cold seeps are located worldwide at active and passive continental margins, and are characterized by the seepage of hydrocarbon-rich fluids from deep reservoirs to the seafloor. Chemosynthetic communities comprising tubeworms, clams and mussels thrive at cold seeps and derive nutrition from reduced chemicals such as methane and sulfide. This study focuses on thiotrophic vestimentiferan tubeworms from the upper Louisiana slope of the Gulf of Mexico. These tubeworms, dominated by the species Lamellibrachia luymesi and Seepiophila jonesi, are nutritionally dependent on internal sulfide-oxidizing bacterial symbionts. These tubeworms form large, bush-like aggregations that provide habitat for numerous associated fauna, and can persist for centuries. Individual tubeworms grow posterior root-like structures to mine sulfide from the sediment underlying their aggregations. Microbial communities that oxidize hydrocarbons using sulfate as an electron donor produce sulfide in the sediment. Previous to this study, it was hypothesized that tubeworms could release sulfate, a byproduct of sulfide oxidation by their symbionts, through their roots into the underlying sediment. They could thereby enhance microbial sulfate reduction, and ensure themselves a lifetime supply of sulfide. In this study, I provide the first empirical evidence for this phenomenon. I used a multi-disciplinary approach that included live animal physiology, tissue biochemistry, sediment geochemistry and theoretical modeling, to demonstrate that tubeworms can enhance microbial sulfate reduction through root sulfate release. My experiments with live L. luymesi tubeworms demonstrated that they release 85% of the sulfate produced by sulfide oxidation, and 67% of the protons produced by various metabolic processes across their root. Based on inhibitor experiments, I suggest that they use sulfate- iii bicarbonate exchangers to mediate sulfate transport across their root epithelium. Further, I measured the proton-ATPase activity of their plume and root tissues and surmised that these tubeworms might use passive proton channels for root proton transport. In combination, these results suggest that tubeworms could conserve energy by eliminating sulfate and protons using ATP-independent mechanisms across their roots. In situ geochemical characterization of the tubeworm habitat showed that these tubeworms could exert a significant influence on the chemistry of their environments. Geochemical data, in combination with a theoretical model, suggest that tubeworms release between 70-90% of the sulfate produced by their symbionts across their roots. The combination of root sulfide uptake and sulfate release appears to maintain a steady sulfide-to-sulfate ratio in sediments adjoining tubeworm roots. The model suggests that by releasing sulfate, tubeworms can maintain basal metabolic requirements as well as enhanced growth rates under conditions where sediment sulfate concentrations would otherwise become limiting. iv