Ecology in the dentist's chair [electronic resource] : patterns of biogeography and stability in human subgingival microbial communities

Recent work on the human microbiome represents the essence of community ecology: "What makes assemblages of species more or less similar to each other at different places and times?" (Vellend 2010; Anderson et al. 2011). The complex microbial communities of the human subgingival crevice are particularly relevant since multiple, spatially distinct but ecologically similar sites are found in a single subject. Healthy sites and sites affected by periodontitis (gum disease) can coexist in the same mouth simultaneously; periodontal disease may reflect community processes since it is thought to have a polymicrobial etiology rather than a single species etiology in the tradition of Koch's postulates. Subgingival communities therefore provide a unique, clinically relevant context to apply ecological concepts. The goal of this work was to advance our ecological understanding of the human subgingival microbiota, drawing on two fields of ecological research: biogeography and the stability of complex communities. The first half of this work explored oral biogeography and treating subgingival sites as isolated, island-like patches of similar habitat distributed within a mouth. A survey of twenty-three to thirty subgingival sites per mouth within five periodontally healthy subjects uncovered non-random, spatially relevant patterns of community distributions. Specifically, a left-right symmetric pattern of community similarity and a positive correlation between physical distance between sites and the dissimilarity of their respective communities were observed. However, these patterns were only discernable among deeply sequenced communities. Additional applications of co-occurrence analysis and neutral theory models to the data indicated that both competitive interactions and stochastic, demographic processes influence distributions of subgingival taxa. The second half of this work assessed the temporal stability of health and periodontitis-associated subgingival and salivary microbial communities before and after a single disturbance event of professional teeth cleaning. Communities were surveyed in 8 subjects (4 healthy, 4 with moderate chronic periodontitis), at 4 sites per subject, and at four sampling times ranging from 2 weeks to 1 day before the cleaning to assess baseline spatial and temporal variation. Samples collected at seven time points ranging from 1 hour to 3 months after the cleaning were also examined in order to monitor the compositional response to the perturbation. The results of this work demonstrated that healthy and periodontitis-associated subgingival communities are resilient to a teeth-cleaning perturbation, but the displacement of community composition immediately after cleaning was greater in periodontitis than in health. Periodontitis-associated subgingival communities more closely resembled a health-like composition as they recovered from the cleaning, although this change was transient. Salivary communities were also shown to be resilient to a teeth cleaning perturbation, but the impact of the cleaning on community composition is less pronounced in saliva. The results further suggest that post-cleaning residual subgingival communities contribute more to subgingival recolonization than salivary communities. The results of this work generated testable hypotheses about the ecological mechanisms governing observed spatial and temporal patterns. I hope these findings will contribute to the development of novel, ecologically informed approaches to the clinical treatment of the subgingival environment.

Keywords: Biology.
Advisor: Relman David A. primary advisor. Thesis advisor
Field Christopher B.
Armitage G. E.
Spormann Alfred M. advisor. Thesis advisor