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Multiple energy sources and metabolic strategies sustain microbial diversity in Antarctic desert soils

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. Numerous diverse microorganisms reside in the cold desert soils of continental Antarctica, though we lack a holistic understanding of the metabolic processes that sustain them. Here, we profile the composition, capabilities, and activities of the microbial communities in 16 physicochemically diverse mountainous and glacial soils. We assembled 451 metagenome-assembled genomes from 18 microbial phyla and inferred through Bayesian divergence analysis that the dominant lineages present are likely native to Antarctica. In support of earlier findings, metagenomic analysis revealed that the most abundant and prevalent microorganisms are metabolically versatile aerobes that use atmospheric hydrogen to support aerobic respiration and sometimes carbon fixation. Surprisingly, however, hydrogen oxidation in this region was catalyzed primarily by a phylogenetically and structurally distinct enzyme, the group 1l [NiFe]-hydrogenase, encoded by nine bacterial phyla. Through gas chromatography, we provide evidence that both Antarctic soil communities and an axenic Bacteroidota isolate (Hymenobacter roseosalivarius) oxidize atmospheric hydrogen using this enzyme. Based on ex situ rates at environmentally representative temperatures, hydrogen oxidation is theoretically sufficient for soil communities to meet energy requirements and, through metabolic water production, sustain hydration. Diverse carbon monoxide oxidizers and abundant methanotrophs were also active in the soils. We also recovered genomes of microorganisms capable of oxidizing edaphic inorganic nitrogen, sulfur, and iron compounds and harvesting solar energy via microbial rhodopsins and conventional photosystems. Obligately symbiotic bacteria, including Patescibacteria, Chlamydiae, and predatory Bdellovibrionota, were also present. We conclude that microbial diversity in Antarctic soils reflects the coexistence of metabolically flexible mixotrophs with metabolically constrained specialists.