Microbial aerotrophy enables continuous primary production in diverse cave ecosystems

Aerated caves receive minimal light energy, yet host diverse microbial communities and the strategies allowing them to meet energy and carbon needs remain unclear. We determined the processes and mediators of primary production in aerated limestone and basalt caves through paired metagenomic and biogeochemical profiling. Four caves were sampled, including sediments and biofilms, yielding 94 metagenomes. Based on 1458 metagenome-assembled genomes, over half of microbial cells encode enzymes to use atmospheric trace gases as energy and carbon sources. The most abundant microbes are chemosynthetic primary producers, notably the gammaproteobacterial methanotrophic order Ca. Methylocavales and two uncultivated actinobacterial genera predicted to grow on atmospheric hydrogen, carbon dioxide, and carbon monoxide. Biogeochemical and isotopic measurements confirmed that these gases are rapidly consumed at rates likely sustaining a substantial fraction of the community and potentially driving primary production. Conventional chemolithoautotrophs, using ammonium and sulfide, are also enriched and active. Altogether, these results indicate that caves are unique in microbial biodiversity and the biogeochemical processes sustaining them. Consumption of atmospheric trace gases likely has a dual role in caves, providing energy for microbial survival and potentially supporting chemosynthetic growth, thereby introducing organic carbon. This process, defined as 'aerotrophy', operates alongside organic and inorganic inputs.