Abstract:
Cold desert soil microbiomes thrive despite severe moisture and nutrient limitations. In Eastern Antarctic soils, bacterial primary
production is supported by trace gas oxidation and the light-independent RuBisCO form IE. This study aims to determine if
atmospheric chemosynthesis is widespread within Antarctic, Arctic and Tibetan cold deserts, to identify the breadth of trace gas
chemosynthetic taxa and to further characterize the genetic determinants of this process. H2 oxidation was ubiquitous, far
exceeding rates reported to fulfill the maintenance needs of similarly structured edaphic microbiomes. Atmospheric
chemosynthesis occurred globally, contributing significantly (p < 0.05) to carbon fixation in Antarctica and the high Arctic.
Taxonomic and functional analyses were performed upon 18 cold desert metagenomes, 230 dereplicated medium-to-high-quality
derived metagenome-assembled genomes (MAGs) and an additional 24,080 publicly available genomes. Hydrogenotrophic and
carboxydotrophic growth markers were widespread. RuBisCO IE was discovered to co-occur alongside trace gas oxidation enzymes
in representative Chloroflexota, Firmicutes, Deinococcota and Verrucomicrobiota genomes. We identify a novel group of high-affinity
[NiFe]-hydrogenases, group 1m, through phylogenetics, gene structure analysis and homology modeling, and reveal substantial
genetic diversity within RuBisCO form IE (rbcL1E), and high-affinity 1h and 1l [NiFe]-hydrogenase groups. We conclude that
atmospheric chemosynthesis is a globally-distributed phenomenon, extending throughout cold deserts, with significant
implications for the global carbon cycle and bacterial survival within environmental reservoirs.
