The Dynamic Influence of Subsurface Geological Processes on the Assembly and Diversification of Thermophilic Microbial Communities in Continental Hydrothermal Systems

An accepted paradigm of hydrothermal systems is the process of phase separation, or boiling, of a deep, homogeneous hydrothermal fluid as it ascends through the subsurface resulting in gas rich and gas poor fluids. While phase separation helps to explain first-order patterns in the chemistry and biology of a hot spring’s surficial expression, we know little about the subsurface architecture beneath “phase-separated” pools and the timescales over which phase separation processes occur. Essentially, we have a two-dimensional understanding of a four-dimensional process. By combining geophysical, geochemical, isotopic, and microbiological measurements of two adjacent phase-separated hot springs in Norris Geyser Basin, Yellowstone National Park, we provide a four-dimensional assessment of phase separation processes and their biological manifestation. We uniquely show that Yellowstone’s hydrothermal waters originate from a deep sedimentary aquifer and that both meteoric recharge and shallow reactive transport processes are required to establish the geobiological feedbacks that drive bimodal distributions in the geochemical and microbial composition of hot springs. Specifically, over periods of tens of years, gas-enriched fluids containing volcanic sulfide mix with meteoric waters resulting in microbially-mediated production of sulfuric acid by thermoacidophilic Archaea in the near subsurface. In contrast, over periods of hundreds of years, anoxic residual liquid rises to the surface where it is infused with atmospheric gas fostering Archaea and Bacteria that are largely dependent on oxygen. As such, our results provide formative insight into the causative links between subsurface geological processes, the development of geochemical fluids, and the assembly and diversification of thermophilic microbial communities in hydrothermal systems.