Atmospheric chemosynthesis is phylogenetically and geographically widespread and contributes significantly to carbon fixation throughout cold deserts

Abstract Cold desert soil microbiomes thrive despite severe moisture and nutrient limitations. In Eastern Antarctic soils, hydrogen oxidising bacteria support primary production through a novel carbon fixation process reliant on the chemoautotrophy-associated RuBisCO form IE. Here, biochemical assays show that atmospheric chemosynthesis occurs globally for primary production, contributing significantly to autotrophic carbon fixation throughout arid to hyperarid deserts in Antarctica, the high Arctic, and the Tibetan Plateau. Taxonomic and functional analyses were performed on 230 dereplicated medium-to-high quality metagenome-assembled genomes (MAGs) derived from 18 cold desert metagenomes and an additional 24,080 publicly available genomes. We infer that atmospheric chemosynthetic bacteria are widespread across environmental and clinical samples, increasing our knowledge of the bacterial phyla genetically capable of atmospheric chemosynthesis to seven, with key enzymes co-occurring within MAGs from four previously unidentified phyla; Chloroflexota, Firmicutes, Deinococcota and Verrucomicrobiota. We informatically identify an additional group of high-affinity hydrogenases, group 1m [NiFe]-hydrogenase using phylogenetics, gene structure analysis and homology modelling and reveal substantial new genetic diversity within RuBisCO form IE (rbcL1E), and high-affinity groups 1h and 1l [NiFe]-hydrogenases. Finally, we conclude that atmospheric chemosynthesis is a global phenomenon, extending throughout and beyond cold deserts, with significant implications for the global carbon cycle and bacterial survival within environmental and clinical reservoirs.