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At present, molecular hydrogen (H₂) produced through Fe(II) oxidation during serpentinization of ultramafic rocks represents a small fraction of the global sink for O₂due to limited exposures of ultramafic rocks. In contrast, ultramafic rocks such as komatiites were much more common in the Early Earth and H₂production via serpentinization was a likely factor in maintaining an O₂-free atmosphere throughout most of the Archean. Using thermodynamic simulations, this work quantifies the global O₂consumption attributed to serpentinization during the past 3.5 billion years. Results show that H₂generation is strongly dependent on rock compositions where serpentinization of more magnesian lithologies generated substantially higher amounts of H₂. Consumption of >2 Tmole O₂yr⁻¹via low-temperature serpentinization of Archean continents and seafloor is possible. This O₂sink diminished greatly towards the end of the Archean as ultramafic rocks became less common and helped set the stage for the Great Oxidation Event.

 

ABSTRACT Little is known of how the confluence of subsurface and surface processes influences the assembly and habitability of hydrothermal ecosystems. To address this knowledge gap, the geochemical and microbial composition of a high-temperature, circumneutral hot spring in Yellowstone National Park was examined to identify the sources of solutes and their effect on the ecology of microbial inhabitants. Metagenomic analysis showed that populations comprising planktonic and sediment communities are archaeal dominated, are dependent on chemical energy (chemosynthetic), share little overlap in their taxonomic composition, and are differentiated by their inferred use of/tolerance to oxygen and mode of carbon metabolism. The planktonic community is dominated by putative aerobic/aerotolerant autotrophs, while the taxonomic composition of the sediment community is more evenly distributed and comprised of anaerobic heterotrophs. These observations are interpreted to reflect sourcing of the spring by anoxic, organic carbon-limited subsurface hydrothermal fluids and ingassing of atmospheric oxygen that selects for aerobic/aerotolerant organisms that have autotrophic capabilities in the water column. Autotrophy and consumption of oxygen by the planktonic community may influence the assembly of the anaerobic and heterotrophic sediment community. Support for this inference comes from higher estimated rates of genome replication in planktonic populations than sediment populations, indicating faster growth in planktonic populations. Collectively, these observations provide new insight into how mixing of subsurface waters and atmospheric oxygen create dichotomy in the ecology of hot spring communities and suggest that planktonic and sediment communities may have been less differentiated taxonomically and functionally prior to the rise of oxygen at ∼2.4 billion years ago (Gya). IMPORTANCE Understanding the source and availability of energy capable of supporting life in hydrothermal environments is central to predicting the ecology of microbial life on early Earth when volcanic activity was more widespread. Little is known of the substrates supporting microbial life in circumneutral to alkaline springs, despite their relevance to early Earth habitats. Using metagenomic and informatics approaches, water column and sediment habitats in a representative circumneutral hot spring in Yellowstone were shown to be dichotomous, with the former largely hosting aerobic/aerotolerant autotrophs and the latter primarily hosting anaerobic heterotrophs. This dichotomy is attributed to influx of atmospheric oxygen into anoxic deep hydrothermal spring waters. These results indicate that the ecology of microorganisms in circumneutral alkaline springs sourced by deep hydrothermal fluids was different prior to the rise of atmospheric oxygen ∼2.4 Gya, with planktonic and sediment communities likely to be less differentiated than contemporary circumneutral hot springs. 

Hot springs integrate hydrologic and geologic processes that vary over short‐ and long‐term time scales. However, the influence of temporal hydrologic and geologic change on hot spring biodiversity is unknown. Here, we coordinated near‐weekly, cross‐seasonal (~140 days) geochemical and microbial community analyses of three widely studied hot springs with local precipitation data in Yellowstone National Park. One spring (‘HFS’) exhibited statistically significant, coupled microbial and geochemical variation across seasons that was associated with recent precipitation patterns. Two other spring communities, ‘CP’ and ‘DS’, exhibited minimal to no variation across seasons. Variability in the seasonal response of springs is attributed to differences in the timing and extent of aquifer recharge with oxidized near‐surface water from precipitation. This influx of oxidized water is associated with changes in community composition, and in particular, the abundances of aerobic sulfide‐/sulfur‐oxidizers that can acidify waters. During sampling, a new spring formed after a period of heavy precipitation and its successional dynamics were also influenced by surface water recharge. Collectively, these results indicate that changes in short‐term hydrology associated with precipitation can impact hot spring geochemistry and microbial biodiversity. These results point to potential susceptibility of certain hot springs and their biodiversity to sustained, longer‐term hydrologic changes.