Cowan, Don A.

Significance Diverse microbial life has been detected in the cold desert soils of Antarctica once thought to be barren. Here, we provide metagenomic, biogeochemical, and culture-based evidence that Antarctic soil microorganisms are phylogenetically and functionally distinct from those in other soils and adopt various metabolic and ecological strategies. The most abundant community members are metabolically versatile aerobes that use ubiquitous atmospheric trace gases to potentially meet energy, carbon, and, through metabolic water production, hydration needs. Lineages capable of harvesting solar energy, oxidizing edaphic inorganic substrates, or adopting symbiotic lifestyles were also identified. Altogether, these findings provide insights into microbial adaptation to extreme water and energy limitation and will inform ongoing efforts to conserve the unique biodiversity on this continent.

AbstractA surprising diversity and abundance of microorganisms resides in the cold desert soils of Antarctica. The metabolic processes that sustain them, however, are poorly understood. In this study, we used metagenomic and biogeochemical approaches to study the microbial communities in 16 physicochemically diverse mountainous and glacial soils from remote sites in South Victoria Land, north of the Mackay Glacier. We assembled 451 metagenome-assembled genomes from 18 bacterial and archaeal phyla, constituting the largest resource of Antarctic soil microbial genomes to date. The most abundant and prevalent microorganisms are metabolically versatile aerobes that use atmospheric hydrogen and carbon monoxide to meet energy, carbon, and, through metabolic water production, hydration needs. Phylogenetic analysis and structural modelling infer that bacteria from nine phyla can scavenge atmospheric hydrogen using a previously unreported enzyme family, the group 1l [NiFe]-hydrogenases. Consistently, gas chromatography measurements confirmed most soils rapidly consume atmospheric hydrogen and carbon monoxide, and provide the first experimental evidence of methane oxidation in non-maritime Antarctica. We also recovered genomes of microorganisms capable of oxidizing other inorganic compounds, including nitrogen, sulfur, and iron compounds, as well as harvesting solar energy via photosystems and novel microbial rhodopsins. Bacterial lineages defined by symbiotic lifestyles, including Patescibacteria, Chlamydiae, and predatory Bdellovibrionota, were also surprisingly abundant. We conclude that the dominant microorganisms in Antarctic soils adopt mixotrophic strategies for energy and sometimes carbon acquisition, though they co-exist with diverse bacteria and archaea that adopt more specialist lifestyles. These unprecedented insights and associated genome compendium will inform efforts to protect biodiversity in this continent.