Respiratory processes of early-evolved hyperthermophiles in sulfidic and low-oxygen geothermal microbial communities

Abstract High-temperature microbial communities contain early evolved archaea and bacteria growing under low levels of oxygen and thus may hold important clues regarding mechanisms of oxygen respiration relevant to the evolutionary history of Earth. Conch and Octopus Springs in Yellowstone National Park, WY (YNP) are highly similar alkaline-chloride springs that provide natural laboratories to identify changes in microbial community composition and metabolism due to differences in dissolved oxygen and sulfide. Replicate metagenomic, metatranscriptomic, microscopic and geochemical analyses were conducted in these two contrasting, high-temperature (82–84 oC) filamentous biofilm communities to understand the role of oxygen, sulfur and arsenic in microbial energy conservation and community composition. Highly related populations of Aquificota (Thermocrinis), with average nucleotide identity (ANI) greater than 97%, were abundant in both communities, as well as a deeply rooted bacterium (Caldipriscus) of the Pyropristinus lineage, and Pyrobaculum (Thermoproteota). Genomic sequence of replicate metagenome assembled genomes (MAGs) of these three phylotypes showed that each possess a different mechanism for metabolic shifts due to concentrations of oxygen and sulfide. The high expression of high-affinity bd ubiquinol and CydAA’ oxygen reductases in sulfidic environments revealed the importance of oxygen respiration under conditions often considered anaerobic. Higher oxygen concentrations in Octopus Spring resulted in a greater diversity of microbial populations with lower-affinity Type 1 heme Cu oxidases (HCOs). The fact that members of several early evolved thermophilic lineages express high levels of high-affinity oxygen reductases under suboxic (< 1 µM dissolved O2) conditions suggests that these proteins have played a major role in the early evolution of microbial life, where similar low-oxygen conditions were nevertheless sufficient for exergonic redox coupling.