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Abstract Elemental sulfur (S₈⁰)‐oxidising Sulfolobales (Archaea) dominate high‐temperature acidic hot springs (>80°C, pH <4). However, genomic analyses of S₈⁰‐oxidising members of the Sulfolobales reveal a patchy distribution of genes encoding sulfur oxygenase reductase (SOR), an S₈⁰disproportionating enzyme attributed to S₈⁰oxidation. Here, we report the S₈⁰‐dependent growth of two Sulfolobales strains previously isolated from acidic hot springs in Yellowstone National Park, one of which associated with bulk S₈⁰during growth and one that did not. The genomes of each strain encoded different sulfur metabolism enzymes, with only one encoding SOR. Dialysis membrane experiments showed that direct contact is not required for S₈⁰oxidation in the SOR‐encoding strain. This is attributed to the generation of hydrogen sulfide (H₂S) from S₈⁰disproportionation that can diffuse out of the cell to solubilise bulk S₈⁰to form soluble polysulfides (S_x²⁻) and/or S₈⁰nanoparticles that readily diffuse across dialysis membranes. The Sulfolobales strain lacking SOR required direct contact to oxidise S₈⁰, which could be overcome by the addition of H₂S. High concentrations of S₈⁰inhibited the growth of both strains. These results implicate alternative strategies to acquire and metabolise sulfur in Sulfolobales and have implications for their distribution and ecology in their hot spring habitats. 

Abstract Despite over a century of study, it is unknown if continental hydrothermal fields support high-temperature subsurface biospheres. Cinder Pool is among the deepest hot springs in Yellowstone and is widely studied due to unique sulfur geochemistry that is attributed to hydrolysis of molten elemental sulfur at ∼18 m depth that promotes several chemical reactions that maintain low sulfide, low oxygen, and a moderate pH of ∼4.0. Following ∼100 years of stability, Cinder Pool underwent extreme visual and chemical change (acidification) in 2018. Here, we show that depth-resolved geochemical and metagenomic-based microbial community analyses pre- (2016) and post-acidification (2020) indicate the changes are likely attributable to feedbacks between geological/geochemical processes, sulfur oxidation by subsurface Sulfolobales Archaea, and the disappearance of molten sulfur at depth. These findings underscore the dynamic and rapid feedback between the geosphere and biosphere in continental hydrothermal fields and suggest subsurface biospheres to be more prevalent in these systems than previously recognized. 

Abstract The factors that influence biodiversity and productivity of hydrothermal ecosystems are not well understood. Here we investigate the relationship between fluid mixing, biodiversity, and chemosynthetic primary productivity in three co‐localized hot springs (RSW, RSN, and RSE) in Yellowstone National Park that have different geochemistry. All three springs are sourced by reduced hydrothermal fluid, but RSE and RSN receive input of vapour phase gas and oxidized groundwaters, with input of both being substantially higher in RSN. Metagenomic sequencing revealed that communities in RSN were more biodiverse than those of RSE and RSW in all dimensions evaluated. Microcosm activity assays indicate that rates of dissolved inorganic carbon (DIC) uptake were also higher in RSN than in RSE and RSW. Together, these results suggest that increased mixing of reduced volcanic fluid with oxidized fluids generates additional niche space capable of supporting increasingly biodiverse communities that are more productive. These results provide insight into the factors that generate and maintain chemosynthetic biodiversity in hydrothermal systems and that influence the distribution, abundance, and diversity of microbial life in communities supported by chemosynthesis. These factors may also extend to other ecosystems not supported by photosynthesis, including the vast subterranean biosphere and biospheres beneath ice sheets and glaciers.