Genome-Centric Dynamics Shape the Diversity of Oral Bacterial Populations

Two major viewpoints have been put forward for how microbial populations change, differing in whether adaptation is driven principally by gene-centric or genome-centric processes. Longitudinal sampling at microbially relevant timescales, i.e., days to weeks, is critical for distinguishing these mechanisms. Because of its significance for both microbial ecology and human health and its accessibility and high level of curation, we used the oral microbiota to study bacterial intrapopulation genome dynamics. Metagenomes were generated by shotgun sequencing of total community DNA from the healthy tongues of 17 volunteers at four to seven time points obtained over intervals of days to weeks. We obtained 390 high-quality metagenome-assembled genomes (MAGs) defining population genomes from 55 genera. The vast majority of genes in each MAG were tightly linked over the 2-week sampling window, indicating that the majority of the population's genomes were temporally stable at the MAG level. MAG-defined populations were composed of up to 5 strains, as determined by single-nucleotide-variant frequencies. Although most were stable over time, individual strains carrying over 100 distinct genes that rose from low abundance to dominance in a population over a period of days were detected. These results indicate a genome-wide as opposed to a gene-level process of population change. We infer that genome-wide selection of ecotypes is the dominant mode of adaptation in the oral populations over short timescales. IMPORTANCE The oral microbiome represents a microbial community of critical relevance to human health. Recent studies have documented the diversity and dynamics of different bacteria to reveal a rich, stable ecosystem characterized by strain-level dynamics. However, bacterial populations and their genomes are neither monolithic nor static; their genomes are constantly evolving to lose, gain, or alter their functional potential. To better understand how microbial genomes change in complex communities, we used culture-independent approaches to reconstruct the genomes (MAGs) for bacterial populations that approximated different species, in 17 healthy donors' mouths over a 2-week window. Our results underscored the importance of strain-level dynamics, which agrees with and expands on the conclusions of previous research. Altogether, these observations reveal patterns of genomic dynamics among strains of oral bacteria occurring over a matter of days.