New insights into the evolution and metabolism of the bacterial phylum Candidatus Acidulodesulfobacteriota through metagenomics.

Candidatus Acidulodesulfobacterales, a formerly proposed bacterial order within the Deltaproteobacteria lineage, represents an ecologically significant group in sulfur-rich environments. Their diversity and functional potential in artificial acid mine drainage (AMD) ecosystems have been well studied; however, their distribution and ecological role in marine hydrothermal sulfides remain poorly understood. Here we integrated publicly available metagenome-assembled genomes (MAGs) with a newly reconstructed MAG from hydrothermal sulfides to perform comprehensive phylogenetic, metabolic, and host-virus interaction analyses. Phylogenomic and 16S rRNA gene analyses indicated that this lineage represents a distinct phylum-level clade, leading us to propose the designation Ca. Acidulodesulfobacteriota. Metabolic reconstructions indicated a versatile lifestyle, encompassing pathways for carbon fixation, nitrogen fixation, sulfur metabolism, iron oxidation, and hydrogen oxidation. Notably, the concatenated DsrAB protein phylogeny and the mixed enzyme types involved in Dsr-dependent dissimilatory sulfur metabolism suggest that Ca. Acidulodesulfobacteriota may represent a transitional lineage in the evolutionary shift from reductive to oxidative Dsr metabolism. Viral auxiliary metabolic genes (AMGs) associated with this phylum were predicted to modulate host metabolic pathways, including folate biosynthesis and sulfur metabolism, highlighting intricate host-virus interactions. These findings advance our understanding of the evolution, metabolic potential, and ecological roles of Ca. Acidulodesulfobacteriota in biogeochemical cycling.