Gardnerella vaginalis is described as a common anaerobic vaginal bacterium whose presence may correlate with vaginal dysbiotic conditions. In the current study, we performed phylogenomic analyses of 72 G. vaginalis genome sequences, revealing noteworthy genome differences underlying a polyphyletic organization of this taxon. Particularly, the genomic survey revealed that this species may actually include nine distinct genotypes (GGtype1 to GGtype9). Furthermore, the observed link between sialidase and phylogenomic grouping provided clues of a connection between virulence potential and the evolutionary history of this microbial taxon. Specifically, based on the outcomes of these in silico analyses, GGtype3, GGtype7, GGtype8, and GGtype9 appear to have virulence potential since they exhibited the sialidase gene in their genomes. Notably, the analysis of 34 publicly available vaginal metagenomic samples allowed us to trace the distribution of the nine G. vaginalis genotypes identified in this study among the human population, highlighting how differences in genetic makeup could be related to specific ecological properties. Furthermore, comparative genomic analyses provided details about the G. vaginalis pan- and core genome contents, including putative genetic elements involved in the adaptation to the ecological niche as well as many putative virulence factors. Among these putative virulence factors, particularly noteworthy genes identified were the gene encoding cholesterol dependent cytolysin (CDC) toxin vaginolysin and genes related to microbial biofilm formation, iron uptake, adhesion to the vaginal epithelium, as well as macrolide antibiotic resistance. IMPORTANCE The identification of nine different genotypes among members of G. vaginalis allowed us to distinguish an uneven distribution of virulence-associated genetic traits within this taxon and thus suggest the potential occurrence of putative pathogen and commensal G. vaginalis strains. These findings, coupled with metagenomics microbial profiling of human vaginal microbiota, permitted us to get insights into the distribution of the genotypes among the human population, highlighting the presence of different structural communities in terms of G. vaginalis genotypes.
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