The genome of Hydrogenophaga taeniospiralis 2K1T, the type and only strain of the species, was analysed. The genes encoding elements involved in autotrophic and chemolithotrophic growth that oxidize H2 in addition to other metabolic traits, such as potential nitrogen fixation capability, are described. A phylogenomic analysis of the taxonomy of members of the genus reveals a high number of species not yet described in the genus, especially if the numerous metagenomes obtained from environmental samples are included. The differences from the closest related genera, Malikia and Serpentinimonas, are highlighted and the delineation of the genus Hydrogenophaga is discussed based on phylogenomic analysis. Furthermore, a survey of metagenomes available in public databases demonstrates the wide environmental and geographic distribution of Hydrogenophaga strains. H. taeniospiralis 2K1T is the first free-living bacterium described for its ability to synthesize R- bodies, which are intracytoplasmic extendable protein ribbons associated mainly with toxic effects. The genetic determinants of R-body synthesis are analysed and compared with those found in other Hydrogenophaga genomes and strains from other genera.