Ecology and Evolution Within the Oral Microbiome

Bacteria inhabit every known ecosystem, from deep-sea hydrothermal vents to plant surfaces. The human body represents one such microbially-dominated ecosystem with the identity and function of human-associated microbiota being intimately connected with human health. However, few specifics are known about the processes governing the distribution and composition of host-associated microbial communities, challenging efforts to alter or maintain certain host-associated bacterial communities. Thus, studying the ecology and evolution of human-associated bacteria is critical both for improving human health and more broadly for better understanding microbial community organization and function. In this dissertation, I use the healthy human oral microbiome as a model system to investigate the processes shaping bacterial populations from an ecological and evolutionary perspective. Altogether, these investigations reveal genomic signatures indicative of fine-scale adaptation to diverse oral niches. In my first chapter, I employ a metapangenomic approach to combine Human Microbiome Project (HMP) metagenomes with pangenomes from public genomes to study the diversity of microbial residents of three oral habitats: tongue dorsum, buccal mucosa, and supragingival plaque. For two exemplar taxa, Haemophilus parainfluenzae and the genus Rothia, metapangenomes revealed distinct genomic groups based on shared genome content. H. parainfluenzae genomes separated into three distinct subgroups with differential abundance between oral habitats. Functional enrichment analyses identified genes encoding oxaloacetate decarboxylase as diagnostic for the tongue-abundant subgroup, suggesting a metabolic adaptation to the tongue habitat. For the genus Rothia, while most R. mucilaginosa were restricted to the tongue as expected, two genomes represented a cryptic population of R. mucilaginosa in many buccal mucosa samples. For both H. parainfluenzae and the genus Rothia, I identified not only limitations in the ability of cultivated organisms to represent populations in their native environment, but also specifically which cultivar gene sequences were absent or ubiquitous. These findings provide insights into population structure and biogeography in the mouth and form specific hypotheses about habitat adaptation. These results also illustrate the power of combining metagenomes and pangenomes to investigate the ecology and evolution of bacteria across analytical scales. In my second chapter, I