Impact of Host Diet and Lifestyle on Oral Microbial Ecologies Across Temporal and Geographic Scales

Abstract

Microbiomes are complex host-associated microbial networks that play important roles in maintaining systemic health. These microbial communities are influenced by host behavior and environmental factors, while host health can be reciprocally affected by shifts in microbial composition and functioning. This dissertation investigates how the oral microbiome is impacted by factors such as host behavior, diet, geography, and time. This work uses calcified dental plaque, or dental calculus, which forms on the surfaces of the teeth throughout an individual’s life and traps microbes and their genetic information. Leveraging advances in shotgun metagenomic sequencing and ancient DNA techniques, oral microbiomes were recovered from a total of 91 individuals from diverse ancestral populations. Chapter one provides the framework of the dissertation and discusses the current state of the field of ancient metagenomics, including the findings from other studies on how oral microbiomes impact health and are shaped by human bioculture. Chapter two investigates how the adoption of maize as a dietary staple by ancestral Maya populations in Belize led to changes in their oral microbiome over a nearly 10,000-year time period. Here, it is revealed that an increase in the availability of fermentable carbohydrates was accompanied by an increased necessity for acid tolerance among oral microbes, leading to differential abundance of key microbes. Chapter three investigates whether intensive acorn consumption impacted the oral microbiome of ancient Muwekma Ohlone peoples from California, U.S. in comparison to those of other populations of varying subsistence patterns. This chapter also includes an analysis of metagenomically assembled genomes (MAGs) from ancient American oral microbiomes, providing a snapshot of oral microbial strain diversity in pre-European contact populations. The functional potential of metagenomes from those with this unique diet revealed a composition similar to agricultural groups, but without enrichment of specific organisms that mark the agricultural diet. Chapter four presents methods for extracting and interpreting non-human herbivorous oral metagenomes by examining dental calculus from ancient and modern bison in Oklahoma. This is the first investigation into oral microbiomes from bison dental calculus, and among the first to explore modern non-human dental calculus. This approach not only revealed prokaryotic organisms that mark bison oral microbiomes but also exhibited ecologically significant eukaryotic plant and fungal genomes accessible through bison dental calculus. Each project employed molecular techniques designated for ancient and modern DNA extraction and shotgun library preparation. Additionally, innovative computational methods for taxonomic and functional assessment, phylogenetic analysis, and de novo metagenome assembly expanded the breadth of knowledge that could be obtained from metagenomic data. By examining the interplay between diet and oral microbial composition and function, this dissertation summarizes the mechanisms driving the existence and prominence of oral microbes, especially some associated with oral disease. By reconstructing metagenomically assembled genomes, we uncover hidden strain diversity irrespective of host or clinical relevance. Finally, by expanding into non-human hosts, we demonstrate the acquisition of environmental eukaryotic DNA from dental calculus of a keystone mammalian species.