Soil microbial communities influenced by proximity to Yellowstone phase-separated fluids

The separation of hydrothermal fluids in the subsurface into a vapor-phase and liquid-phase leads to diverging surface features, including hot springs that can have vastly different pH, geochemistry, and microbiology. While these effects have been well-characterized in hot springs themselves, the influence of phase-separation on the microbial communities inhabiting adjacent environments such as soils has not been determined. In this study, we characterized microbial communities inhabiting soils at varying distances from two adjacent, hot springs in Yellowstone National Park, Red Bubbler (RB) that is sourced by a mixture of liquid and vapor phase fluids and Perpetual Spouter (PS) that is sourced by liquid phase fluids. Despite being spatially separated by < 15 meters, the hot springs represent divergent environments largely due to their phase-separated fluids as reflected in their geochemistry and microbial communities. Soils directly adjacent to RB showed minimal phylogenetic or functional overlap with the RB hot spring communities, while PS-adjacent soil communities were nearly identical to those of the PS hot spring, likely due to deposition of microbes from PS waters during recurring eruptions. Metagenome-assembled genomes and experimental net gas oxidation calculations in soils between the springs and adjacent to RB provide evidence of increased microbial high-affinity H2 oxidation as a function of distance from RB. However, this trend was inverted in the PS-adjacent soils. These results indicate that diffuse gas flow and local emissions of the H2-enriched vapor from the RB hot spring select against high-affinity H2 oxidation in the nearby soils, while proximity to the gas-depleted PS hot spring appears to promote high-affinity H2 metabolisms, lending support to the inhibition of gas flow by a hypothesized silica-encased conduit. The study indicates that hot springs can have a broad spatial influence on microbial community composition and function particularly through feedback effects on gas delivery induced by their fluid sourcing.