Ancient genomes from Bronze Age remains reveal deep diversity and recent adaptive episodes for human oral pathobionts

Ancient microbial genomes can illuminate pathobiont evolution, with teeth providing a particularly rich substrate. However, very few prehistoric genomes from oral species have been retrieved, limiting the scope of inference. Here, we report well-preserved microbiomes from two 4,000 year old human teeth from an Irish limestone cave. These contained bacterial species implicated in periodontal disease, as well as Streptococcus mutans, the major cause of caries and rare in the ancient genomic record. Despite deriving from the same individual, these teeth produced divergent Tannerella forsythia genomes, indicating higher levels of diversity in prehistoric populations of this species. We also find evidence of microbiome dysbiosis, with a disproportionate quantity of S. mutans sequences relative to other oral streptococci observed. This high abundance allowed for metagenomic assembly, resulting in its first reported ancient genome. Phylogenetic analysis indicates major post-medieval population expansions for both species, highlighting the inordinate impact of recent dietary changes on these species' ecology. In T. forsythia, this expansion is associated with the replacement of older lineages, possibly reflecting a genome-wide selective sweep. Accordingly, we see dramatic changes in T. forsythia's virulence repertoire across this period. S. mutans shows a contrasting pattern, with deeply divergent lineages (pre-6000 BP) persisting in modern populations. This may be due to its highly recombining nature, allowing for maintenance of diversity through selective episodes. Nonetheless, an explosion in recent coalescences and significantly shorter branch lengths separating bacteriocin-carrying strains indicate major changes in S. mutans demography and function coinciding with sugar popularisation during the industrial period.