Abstract
The evolution of phototrophy and carbon fixation in the phylum Chloroflexota remains incompletely understood, largely due to the scarcity of cultured mesophilic representatives. Here, we report the isolation and genomic characterization of a novel filamentous anoxygenic phototrophic bacterium from a microbial mat in the mesothermal Lake Umkhey (Southern Siberia). Although the original culture was lost, its genome was recovered via metagenome-assembled genome reconstruction from environmental samples, enabling a detailed phylogenomic and metabolic analysis. The genome of umkhey_bin13 (proposed as ‘Candidatus Viridifilum namsaraevi’ gen. nov., sp. nov.) encodes a complete 3-hydroxypropionate bicycle for autotrophic CO₂ fixation, a type II sulfide:quinone oxidoreductase, but lacks nitrogenase and chemolithotrophic markers. Comparative genomics across 18 Chloroflexota genomes reveals that this new lineage occupies an intermediate phylogenetic position, with distinct gene content for sulfur, nitrogen, and hydrogen metabolism, and highlights a complex evolutionary history within the group. Our findings provide new insights into the evolutionary transitions of photosynthetic and carbon-fixation pathways, and underscore the value of integrating cultivation-independent genomics with classical microbiology. The proposed novel genus and species contribute to a revised framework of Chloroflexota evolution and offer a genomic reference for studying metabolic adaptation in alkaline, sulfide-influenced microbial mats.