Microbial biogeography and ecology of the mouth and implications for periodontal diseases

Abstract

In humans, the composition of microbial communities differs among body sites and between habitats within a single site. Patterns of variation in the distribution of organisms across time and space are referred to as "biogeography." The human oral cavity is a critical observatory for exploring microbial biogeography because it is spatially structured, easily accessible, and its microbiota has been linked to the promotion of both health and disease. The biogeographic features of microbial communities residing in spatially distinct, but ecologically similar, environments on the human body, including the subgingival crevice, have not yet been adequately explored. The purpose of this paper is twofold. First, we seek to provide the dental community with a primer on biogeographic theory, highlighting its relevance to the study of the human oral cavity. We summarize what is known about the biogeographic variation of dental caries and periodontitis and postulate that disease occurrence reflects spatial patterning in the composition and structure of oral microbial communities. Second, we present a number of methods that investigators can use to test specific hypotheses using biogeographic theory. To anchor our discussion, we apply each method to a case study and examine the spatial variation of the human subgingival microbiota in 2 individuals. Our case study suggests that the composition of subgingival communities may conform to an anterior-to-posterior gradient within the oral cavity. The gradient appears to be structured by both deterministic and nondeterministic processes, although additional work is needed to confirm these findings. A better understanding of biogeographic patterns and processes will lead to improved efficacy of dental interventions targeting the oral microbiota.

Keywords: biogeography; oral microbiome; oral microbiota; spatial pattern; subgingival; supragingival.

Figure 1:. Exploratory analysis of 4 genera.

a) The absolute abundance (x-axis) of Prevotella and Fusobacterium is plotted (y-axis) for each of 2 individuals. Each bar is shaded by the Phylum to which the taxon belongs. b) the site-specific abundance of each Genus was visualized for each site for Subject 1 (Left) and Subject 2 (Right). Similar colors represent similar abundance values: red indicates low; pink intermediate; and blue high abundance values for each taxon at that site. Numbers within each circle correspond to universal tooth number.

Figure 2:. Subgingival communities, like supragingival communities, may conform to an ecological gradient.

a) Trend surface analysis was used to examine spatial patterning at subgingival sites. Scores from the first principal component (y-axis) is plotted against universal tooth number (x-axis). Each point represents a sample that is colored according to tooth class (canine, incisor, molar, premolar). The blue line is a loess smoothened curve surrounded by 95% confidence intervals in grey. b) MEM was used to evaluate spatial patterning in subgingival samples from the same subjects. Each point represents a tooth plotted against the x- and y- geographic coordinates of sample sites. Points are shaded with a heatmap scale according the first RDA axis. The trend surface and MEM models both suggest communities vary along an ecological gradient that distinguishes between sites across the anterior-to-posterior dimension.

Figure 3:. Elements of community structure suggests subgingival communities conform to a nested subset gradient with clumped species loss.

a) coherence was less than the simulated mean for both subjects (p < 0.001). b) turnover was less than the simulated mean for both subjects (p < 0.001), and c) boundary clumping exceeded 1 for both subjects. Taken together, these data suggest that the gradient fits a nested subset with clumped species loss.

Figure 4:. Frequency-abundance distributions of subgingival taxa conform to a neutral community model (NCM).

Subject-specific comparisons of the NCM to observed frequency and mean relative abundance of subgingival OTUs. Each circle represents an individual OTU. Dashed lines represent the least-squares best fit. OTUs that lie to the right of the curve indicate taxa that may be at a selective disadvantage.