The Ecology of Aquificales

Abstract

Aquificales are dominant autotrophs in hydrothermal environments which has led to their extensive study over the past 30 years. However, many questions of the physiology and ecology of Aquificales remain unanswered, including aspects of their energy metabolism and how this affects their distribution, abundance, and interactions with other populations in hydrothermal ecosystems. Here, using cultivation-dependent and independent methods on samples from Yellowstone and Iceland, I aim to address several of the gaps in our understanding of Aquificales physiology and ecology. Water samples were collected from Old Faithful Geyser, Yellowstone, to examine the distribution and activity of Aquificales in these ecosystems that have yet to be studied microbially. Cells detected in the samples resembled Aquificales filaments and actively fixed carbon dioxide at temperatures consistent with the geyser vent temperature. The autotroph Thermocrinis, a member of Aquificales, dominated the community alongside ecosystems of the putative heterotroph, Thermus. Metagenomic analyses of 105 hot springs also revealed a strong pattern in the co-distribution of Aquificales and Thermus across Yellowstone and Iceland, especially in alkaline springs. Enrichments targeting an autotrophic, nitrogen-fixing Aquificales produced a co-culture of a yet to be classified Aquificales and Thermus populations. Subsequent experimentation showed that Thermus was dependent on unclassified Aquificales for organic carbon and nitrogen when these sources were not supplied in culture. To further our understanding of hot spring community structure, the planktonic and sediment communities of an alkaline hot spring were compared and showed that the planktonic community was enriched in aerobic, autotrophic organisms, including members of the order Aquificales, while the sediment community was mainly anaerobic and heterotrophic. Together with the co-culture work, these results demonstrated that Aquificales have a key role in provisioning of nutrients to secondary consumers in hot springs. Lastly, a Hydrogenobacter (Aquificales) isolated from suboxic sediments from a dynamic Yellowstone hot spring was shown to simultaneously oxidize hydrogen and elemental sulfur and could simultaneously respire oxygen and elemental sulfur. This flexible and hybrid energy metabolism sheds new light on adaptations that facilitate life in dynamic, low oxygen ecosystems and may provide insight into the transition from anerobic to aerobic metabolism on early Earth.