The natural combustion of underground coal seams leads to the formation of gas, which contains molecular hydrogen and carbon monoxide. In places where hot coal gases are released to the surface, specific thermal ecosystems are formed. Here, 16S rRNA gene profiling and shotgun metagenome sequencing were employed to characterize the taxonomic diversity and genetic potential of prokaryotic communities of the near-surface ground layer near hot gas vents in an open quarry heated by a subsurface coal fire. The communities were dominated by only a few groups of spore-forming Firmicutes, namely the aerobic heterotroph Candidatus Carbobacillus altaicus, the aerobic chemolitoautotrophs Kyrpidia tusciae and Hydrogenibacillus schlegelii, and the anaerobic chemolithoautotroph Brockia lithotrophica. Genome analysis predicted that these species can obtain energy from the oxidation of hydrogen and/or carbon monoxide in coal gases. We assembled the first complete closed genome of a member of uncultured class-level division DTU015 in the phylum Firmicutes. This bacterium, ‘Candidatus Fermentithermobacillus carboniphilus’ Bu02, was predicted to be rod-shaped and capable of flagellar motility and sporulation. Genome analysis showed the absence of aerobic and anaerobic respiration and suggested chemoheterotrophic lifestyle with the ability to ferment peptides, amino acids, N-acetylglucosamine, and tricarboxylic acid cycle intermediates. Bu02 bacterium probably plays the role of a scavenger, performing the fermentation of organics formed by autotrophic Firmicutes supported by coal gases. A comparative genome analysis of the DTU015 division revealed that most of its members have a similar lifestyle.