Site-tropism of streptococci in the oral microbiome

A detailed understanding of where bacteria localize is necessary to advance microbial ecology and microbiome-based therapeutics. The site-specialist hypothesis predicts that most microbes in the human oral cavity have a primary habitat type within the mouth where they are most abundant. We asked whether this hypothesis accurately describes the distribution of the members of the genus Streptococcus, a clinically relevant taxon that dominates most oral sites. Prior analysis of 16S rRNA gene sequencing data indicated that some oral Streptococcus clades are site-specialists while others may be generalists. However, within complex microbial populations composed of numerous closely related species and strains, such as the oral streptococci, genome-scale analysis is necessary to provide the resolution to discriminate closely related taxa with distinct functional roles. Here, we assess whether individual species within this genus are specialists using publicly available genomic sequence data that provide species-level resolution. We chose a set of high-quality representative genomes for human oral Streptococcus species. Onto these genomes, we mapped shotgun metagenomic sequencing reads from supragingival plaque, tongue dorsum, and other sites in the oral cavity. We found that every abundant Streptococcus species in the healthy human oral cavity showed strong site-tropism and that even closely related species such as S. mitis, S. oralis, and S. infantis specialized in different sites. These findings indicate that closely related bacteria can have distinct habitat distributions in the absence of dispersal limitation and under similar environmental conditions and immune regimes. Substantial overlap between the core genes of these three species suggests that site-specialization is determined by subtle differences in genomic content.