The phylum Thermodesulfobiota was described in 2023 as a result of reclassification of the family Thermodesulfobiaceae (Frolov et al., 2023a), and currently comprises only two species with validly published names: Thermodesulfobium narugense (Mori et al., 2003; Euzeby, 2004) and Thermodesulfobium acidiphilum (Frolov et al., 2017). T. narugense Na82T was isolated from a terrestrial hot spring in Japan (Mori et al., 2003), while T. acidiphilum 3127-1T was obtained from geothermally heated soil of Uzon Caldera in Russia (Frolov et al., 2017). Both organisms are moderately thermoacidophilic, strictly anaerobic, non-sporulating, rod-shaped, Gram-negative bacteria capable of growing chemolithoautotrophically by the oxidation of H2 or formate with sulfate or thiosulfate (Mori et al., 2003; Frolov et al., 2017). T. narugense Na82T can also use nitrate and nitrite as the terminal electron acceptors (Mori et al., 2003). Heterotrophic growth of T. narugense Na82T and T. acidiphilum 3127-1T has not been demonstrated.

In addition to these two species, a mesophilic strain 3baa was isolated from sediments of an acidic mine pit lake of the Lusatian lignite mining district of Germany (Rüffel et al., 2018). This strain has not been described as a taxon with validly published name, although it most probably represents a new species of the genus Thermodesulfobium. The strain 3baa was described as an acidophile growing in artificial pore water medium in the range of pH 2.6–6.6 at 25 °C and capable of forming biofilms triggered by mineral precipitation. Like T. narugense Na82T and T. acidiphilum 3127-1T, strain 3baa grows chemolithoautotrophically by the oxidation of H2 with sulfate (Rüffel et al., 2018).

The genomes of T. narugense Na82T and T. acidiphilum 3127-1T, but not of strain 3baa, were sequenced, assembled, and deposited in public databases. However, to date, none of these genomes has been analyzed in detail.

Molecular signatures of representatives of the phylum Thermodesulfobiota have been detected in acidic hot springs (Brito et al., 2014; Burgess et al., 2012; Frolov et al., 2016; Frolov et al., 2021) and anaerobic sediments (Sánchez-Andrea et al., 2011; Zelenina et al., 2022).

The autotrophic growth of representatives of the genus Thermodesulfobium was studied in detail, and a new form III RubisCO-mediated transaldolase variant of the Calvin cycle was discovered and described in these microorganisms (Frolov et al., 2019). Subsequently, this pathway of CO2 fixation was predicted for bacteria of the genera Ammonifex and Thermodesulfitimonas of the phylum Bacillota (Frolov et al., 2019), as well as for some representatives of the genus Thermodesulfovibrio of the phylum Nitrospirota (Maltseva et al., 2024). Horizontal gene transfer of transaldolase variant of the Calvin cycle between Thermodesulfobium, Thermodesulfovibrio and Ammonifex-Thermodesulfitimonas lineages has been suggested (Frolov et al., 2019; Maltseva et al., 2024). However, the direction of this horizontal gene transfer, the origin of the Calvin cycle and the initial metabolism in Thermodesulfobium lineage remain unclear. The description of new representatives of the phylum Thermodesulfobiota followed by detailed analysis of their genomes should help answering the questions posed.

In this paper, we report the isolation and characterization of the third species of the genus Thermodesulfobium from an acidic thermal spring of the Uzon Caldera (Kamchatka, Russia), which is capable not only of autotrophic but also of heterotrophic growth and has other new metabolic properties. The comparative genome analysis of this isolate and the two known species with validly published names revealed genetic determinants of the dissimilatory sulfate reduction, oxidation of hydrogen, formate and fumarate, as well as CO2 fixation and central carbon metabolism pathways.