Desert soils harbor diverse communities of heterotrophic bacteria despite lacking organic carbon inputs from vegetation. A major question is therefore how these communities maintain biodiversity and biomass in such resource-limited soils. We addressed this question by investigating desert topsoils and biological soil crusts collected along an aridity gradient traversing four climatic regions (sub-humid, semi-arid, arid and hyper-arid). Metagenomic analysis showed that these communities harbored a variable potential to utilize sunlight, organic compounds, and inorganic compounds as energy sources. Thermoleophilia and Actinobacteria were the most abundant and prevalent classes across the aridity gradient; genome-resolved analysis suggested these taxa are metabolically flexible, capable of mediating aerobic organoheterotrophic growth, as well as conserving energy and fixing carbon using atmospheric H2 as an energy source. In contrast, the abundance of Cyanobacteria was variable and often low across the aridity gradient. We subsequently performed biogeochemical measurements to measure how two key metabolic processes interact with aridity: (i) chemosynthetic H2 oxidation and (ii) photosynthetic CO2 fixation. Gas chromatography analysis revealed biomass-normalized rates of H2 consumption increased 500-fold along the aridity gradient, correlating with increased abundance of high-affinity hydrogenases. Radiolabelled carbon fixation assays confirmed that photosynthetic processes exhibited the inverse relationship, with reduced photosynthetic capacity in arid and hyper-arid soils. Altogether, this suggests that the dominant bacterial lineages inhabiting hot deserts use different strategies for energy and carbon acquisition depending on resource availability. Moreover, these findings suggest trace gases are critical energy sources supporting the productivity and resilience of desert biocrust and topsoil communities.
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