Cold desert soils are notoriously scarce in liquid water and nutrients and are exposed to highly variable levels of sunlight. Whilst residing microbiomes are abundant and diverse, photoautotrophs are increasingly reported as scarce. Simultaneously, soil oligotrophy limits geochemical carbon fixation by chemoautotrophs. This reveals a gap in our understanding of the first-order processes that supply carbon and energy to these trophic webs. In 2017, we proposed that the oxidation of atmospheric hydrogen and carbon monoxide by high-affinity enzymes liberates sufficient energy to support primary production in Antarctic deserts through the novel RuBisCO form IE driven Calvin-Benson-Bassham (CBB) cycle in a process since coined “atmospheric chemosynthesis”. It has remained unclear how widely distributed and significant atmospheric chemosynthesis is as a primary production strategy throughout other desert environments, and the process and underlying pathway have not been characterised in pure culture.
Here, we will describe the use of biochemical assays to quantify atmospheric chemosynthesis alongside photosynthesis in soils from six sites that encompass the Antarctic, Arctic and Tibetan Plateau. Trace gas oxidation rates were rapid (H2; 6.3 - 623.9 nmol/mol/h/g, CO; 0 - 2.6 nmol/mol/h/g), exceeding those rates required to support persistence in similarly structure terrestrial microbiomes. In the McMurdo Dry Valleys and in the high Arctic, trace H2 oxidation significantly increased (p < 0.05) microbial carbon fixation and, in the high Arctic, so did light exposure confirming that atmospheric chemosynthesis occurs broadly within cold deserts and can co-occur alongside photosynthesis. Through analysis of 18 metagenomes, 230 dereplicated metagenome-assembled-genomes and 24,080 publicly available genomes, we will describe the immense diversity within RuBisCO form I and high-affinity hydrogenases, including our identification of a novel form; 1m. We identify an additional four phyla (Chloroflexota, Firmicutes, Deinococcota and Verrucomicrobiota) and 92 bacterial isolates that are genetically capable of atmospheric chemosynthesis. Finally, we use pure culture studies, biochemical assays and transcriptomics to investigate the atmospheric chemosynthesis pathway for the first time within a facultatively autotrophic bacteria.