Geobiological feedbacks and the evolution of thermophiles in Yellowstone National Park hot springs

Abstract

This dissertation focuses on identifying the geobiological feedbacks that shaped the evolutionary ecology of thermophiles in Yellowstone National Park (YNP) hot springs. Hot springs can generally be grouped as acidic, moderately acidic, and neutral to alkaline. Although the geochemistry and microbiology of YNP hot springs have been studied for over a century, fundamental gaps in the understanding of the feedbacks between them remain. Here, the influence of fluid mixing regime on geochemistry, microbial diversity, and productivity was investigated in three geographically co-localized springs whose communities are supported by chemical energy. The results indicate that a higher degree of disequilibrium in electron donor/acceptor pairs due to mixing of highly reduced volcanic gases and oxidized near surface waters was present in the moderately acidic hot spring, which supported higher biodiversity and primary productivity. In contrast, the acidic hot spring had the lowest biodiversity and productivity. Interestingly, acidic springs are generally dominated by members of the archaeal order Sulfolobales which have been suggested to mediate the acidification of these environments through aerobic elemental sulfur (S 8 0 ) oxidation that produces sulfuric acid (H2 SO4 ). Intriguingly, Sulfolobales encode the protein sulfide:quinone oxidoreductase (SQR), proposed to catalyze the oxidation of sulfide (H2 S). However, this metabolism has yet to be demonstrated. Five novel Sulfolobales strains were isolated under H 2S-oxidizing conditions from YNP. This activity was coupled to growth and H 2SO 4 production, expanding the role of Sulfolobales in the oxidative sulfur cycle. S 8 0 oxidation in these strains was also investigated due to the observation that nearly half of Sulfolobales don't encode sulfur oxidoreductase (SOR), the canonical pathway of S 80 oxidation in Sulfolobales. Two Sulfolobales strains were selected, one of which encoded SOR and the other of which did not. SOR disproportionates S 8 0 , yielding H 2S as a product. Since H 2S can react with S 8 0 , promoting its solubilization, it was hypothesized that the strain encoding SOR could grow via indirect contact to the mineral while the non-SOR encoding would need direct contact. This was confirmed through experiments where S 8 0 was sequestered in dialysis membranes. Interestingly, the non-SOR strain was able to grow via indirect contact when H 2S was added to the culture media to mimic SOR mechanism. The results shown here provide new insight into the geological and biological feedbacks that shaped the evolution, ecology, and physiology of thermophiles.