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Organoheterotrophs are the dominant bacteria in most soils worldwide. While many of these bacteria can subsist on atmospheric hydrogen (H 2 ), levels of this gas are generally insufficient to sustain hydrogenotrophic growth. In contrast, bacteria residing within soil-derived termite mounds are exposed to high fluxes of H 2 due to fermentative production within termite guts. Here, we show through community, metagenomic, and biogeochemical profiling that termite emissions select for a community dominated by diverse hydrogenotrophic Actinobacteriota and Dormibacterota. Based on metagenomic short reads and derived genomes, uptake hydrogenase and chemosynthetic RuBisCO genes were significantly enriched in mounds compared to surrounding soils. In situ and ex situ measurements confirmed that high- and low-affinity H 2 -oxidizing bacteria were highly active in the mounds, such that they efficiently consumed all termite-derived H 2 emissions and served as net sinks of atmospheric H 2 Concordant findings were observed across the mounds of three different Australian termite species, with termite activity strongly predicting H 2 oxidation rates ( R 2 = 0.82). Cell-specific power calculations confirmed the potential for hydrogenotrophic growth in the mounds with most termite activity. In contrast, while methane is produced at similar rates to H 2 by termites, mounds contained few methanotrophs and were net sources of methane. Altogether, these findings provide further evidence of a highly responsive terrestrial sink for H 2 availability shapes composition and activity of microbial communities. They also reveal a unique arthropod-bacteria interaction dependent on H 2 availability shapes composition and activity of microbial communities. They also reveal a unique arthropod-bacteria interaction dependent on H 2 transfer between host-associated and free-living microbial communities., Competing Interests: The authors declare no competing interest.

Soil microorganisms globally are thought to be sustained primarily by organic carbon sources. Certain bacteria also consume inorganic energy sources such as trace gases, but they are presumed to be rare community members, except within some oligotrophic soils. Here we combined metagenomic, biogeochemical and modelling approaches to determine how soil microbial communities meet energy and carbon needs. Analysis of 40 metagenomes and 757 derived genomes indicated that over 70% of soil bacterial taxa encode enzymes to consume inorganic energy sources. Bacteria from 19 phyla encoded enzymes to use the trace gases hydrogen and carbon monoxide as supplemental electron donors for aerobic respiration. In addition, we identified a fourth phylum (Gemmatimonadota) potentially capable of aerobic methanotrophy. Consistent with the metagenomic profiling, communities within soil profiles from diverse habitats rapidly oxidized hydrogen, carbon monoxide and to a lesser extent methane below atmospheric concentrations. Thermodynamic modelling indicated that the power generated by oxidation of these three gases is sufficient to meet the maintenance needs of the bacterial cells capable of consuming them. Diverse bacteria also encode enzymes to use trace gases as electron donors to support carbon fixation. Altogether, these findings indicate that trace gas oxidation confers a major selective advantage in soil ecosystems, where availability of preferred organic substrates limits microbial growth. The observation that inorganic energy sources may sustain most soil bacteria also has broad implications for understanding atmospheric chemistry and microbial biodiversity in a changing world.