Ancient Genomes From Bronze Age Remains Reveal Deep Diversity and Recent Adaptive Episodes for Human Oral Pathobionts

• Published in: Molecular biology and evolution Vol. 41; no. 3
• Main Authors: Jackson, Iseult, Woodman, Peter, Dowd, Marion, Fibiger, Linda, Cassidy, Lara M
• Format: Journal Article
• Language: English
• Published: US Oxford University Press 01.03.2024
• Subjects: Analysis; Archaeology; Bacteriocins; Demography; Dental caries; Discoveries; Dysbacteriosis; Ethylenediaminetetraacetic acid; Genetic aspects; Genomes; Genomic analysis; Genomics; Humans; Limestone; Metagenome; Metagenomics; Microbiomes; Microbiota; Microorganisms; Periodontitis; Phylogenetics; Phylogeny; Populations; Prehistoric era; Streptococcus mutans - genetics; Teeth; Virulence; Ireland; oral microbiome; microbial evolution; ancient pathogen genomics; Tannerella forsythia; Streptococcus mutans
• ISSN: 0737-4038; 1537-1719; 1537-1719
• DOI: 10.1093/molbev/msae017

Abstract Ancient microbial genomes can illuminate pathobiont evolution across millenia, with teeth providing a rich substrate. However, the characterization of prehistoric oral pathobiont diversity is limited. In Europe, only preagricultural genomes have been subject to phylogenetic analysis, with none compared to more recent archaeological periods. Here, we report well-preserved microbiomes from two 4,000-year-old teeth from an Irish limestone cave. These contained bacteria implicated in periodontitis, 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 strain diversity in prehistoric populations. We find evidence of microbiome dysbiosis, with a disproportionate quantity of S. mutans sequences relative to other oral streptococci. This high abundance allowed for metagenomic assembly, resulting in its first reported ancient genome. Phylogenetic analysis indicates major postmedieval population expansions for both species, highlighting the inordinate impact of recent dietary changes. 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 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 popularization during the industrial period.