Autotrophic growth of Thermus sp. PS18 and its genomic determinants shed light on the autotrophic lifestyle and its evolution in the Thermaceae family

A thermophilic bacterial strain PS18 was isolated from a hot spring on Kunashir Island under aerobic autotrophic conditions and identified as Thermus brevis . Autotrophy has never been demonstrated in representatives of the Thermaceae family or the entire Deinococcota phylum. T. brevis PS18, in addition to the capacity for heterotrophic growth, showed sustainable autotrophic growth on thiosulfate in aerobic conditions. It could also grow anaerobically with formate and nitrate. Autotrophic growth of T. brevis PS18 was characterized in growth experiments, as well as by radioisotopic, genomic and proteomic analyses, and the leading role of the CBB cycle was demonstrated. Analysis of Deinococcota genomes available in GenBank revealed CBB cycle determinants in 24 species of the Thermaceae family. We further demonstrated autotrophic growth of T. caldilimi YIM 78456 T , one of the carriers of CBB cycle determinants, and isolated two more autotrophically growing Thermus strains, T. oshimai Uz8 and T. scotoductus Uz79, from hot spring samples. These results indicate widespread occurrence of autotrophic CO 2 assimilation in representatives of the Thermaceae family, and suggest that they may be among primary producers in microbial communities of natural and anthropogenic thermal environments. Bioinformatic insight into the evolution of the autotrophic capacity in Thermaceae revealed remarkable lateral mobility of autotrophy key determinants in this family, which we explain in terms of our hypothesis of inheritance of facultative characters by gene loss and reacquisition from the pangenome. We also present bioinformatic evidence that in Thermaceae the (re)acquisition mechanism may involve heterozygous stage sustainable over generations.