Thermophilic Filamentous Microbial Communities associated with Sulfidic Hydrothermal Vents in Yellowstone Lake

Reduced sulfur in hydrothermal vent systems supports modern thermophilic microbial communities and may have been an important energy source in the origin of life. As part of a collaborative project focused on the hydrothermal dynamics of Yellowstone Lake (HD-YLake), Wyoming, we are characterizing filamentous, microbial 'streamer' communities inhabiting high-temperature (ca. 140°C), sulfur-rich discharge sites on the lake floor. We obtained biomass samples for shotgun metagenome sequencing from a deep (120 m) basin east of Stevenson Island using a remotely operated vehicle (Yogi) aboard R/V Annie. DNA from five vent streamer communities was sequenced by the Census of Deep Life and several high-quality population genomes were reconstructed via nucleotide frequency and coverage-based analyses. Results indicated that the microbial communities from multiple vent sites were dominated by thermophilic, sulfur-cycling archaea and bacteria including taxa within the Crenarchaeota and Aquificales. Functional analyses based on gene content and metabolic predictions provided further evidence for the important role of elemental sulfur in these communities and suggested numerous phylotypes contribute to redox transformations important within the sulfur cycle. Compositional analyses and electron microscopy also revealed elemental sulfur deposits embedded within the streamer fabric. Persistence of active, sulfur-rich hydrothermal vents over geologic time may have sustained thermophilic communities like these with a relatively consistent energy supply compared to the surface of the Earth where changes in redox conditions likely caused changes in microbial community dynamics. We propose that these vents and the complex microbial communities they support can be investigated as analogs of early-earth systems, where autotrophic and sulfur-processing metabolisms were fueled by deep energy sources.