Bulleidia extructa PP_925: Genome Reduction, Minimalist Metabolism, and Evolutionary Insights into Firmicutes Diversification

<i>Bulleidia extructa</i> strain PP_925, isolated from the periodontal pocket of a patient with periodontitis, is a Gram-positive <i>Bacillota</i> with an unusually compact genome of 1.38 Mb. Phylogenomic analyses place PP_925 within <i>Erysipelotrichales</i> and show close relatedness of <i>Bulleidia</i> to <i>Solobacterium</i> and <i>Lactimicrobium,</i> as well as the existence of previously undescribed related clades. The metabolic repertoire of PP_925 is strongly reduced: it retains glycolysis, the phosphotransacetylase-acetate kinase pathway, and arginine catabolism but lacks the tricarboxylic acid cycle and most de novo biosynthetic pathways for amino acids, nucleotides, fatty acids, cofactors, and vitamins, implying reliance on salvage and cross-feeding. Phylogenetic inference indicates independent peptidoglycan losses in multiple mycoplasma <i>Erysipelotrichia</i>-related lineages, while PP_925 has retained an ancestral Gram-positive cell wall despite extensive genomic reduction. The genome preserves systems crucial for host interaction and adaptability, including a horizontally acquired <i>tad</i> locus encoding type IV pili, a <i>comG</i> competence system, and several adherence-associated virulence factors. Defense mechanisms are diverse and include a CRISPR-Cas II-A system, a type II restriction-modification module adjacent to Gao_Qat-like genes, and the Wadjet system in a genome without prophages; CRISPR spacers indicate repeated encounters with <i>Bacillota</i> phages. Comparative genomics of PP_925 and related strains reveals a small core genome with lineage-specific adhesion and defense modules, indicating recent shared ancestry combined with adaptive flexibility under substantial genome reduction.