The Structure of Dental Plaque Microbial Communities in the Transition from Health to Dental Caries and Periodontal Disease

Abstract

The human oral cavity harbors diverse communities of microbes that live as biofilms: highly ordered, surface-associated assemblages of microbes embedded in an extracellular matrix. Oral microbial communities contribute to human health by fine-tuning immune responses and reducing dietary nitrate. Dental caries and periodontal disease are together the most prevalent microbially mediated human diseases worldwide. Both of these oral diseases are known to be caused not by the introduction of exogenous pathogens to the oral environment, but rather by a homeostasis breakdown that leads to changes in the structure of the microbial communities present in states of health. Both dental caries and periodontal disease are mediated by synergistic interactions within communities, and both diseases are further driven by specific host inputs: diet and behavior in the case of dental caries and immune system interactions in the case of periodontal disease. Changes in community structure (taxonomic identity and abundance) are well documented during the transition from health to disease. In this review, changes in biofilm physical structure during the transition from oral health to disease and the concomitant relationship between structure and community function will be emphasized.

Keywords: dental caries; oral microbiome; periodontal disease; plaque structure; subgingival biofilm.

Figure 1. Observed changes in dental plaque structure between states of health and sites of active caries.

DNA sequencing provides a description of community structure in the form of taxonomic membership and abundance. Supragingival plaque communities from patients with dental caries experience shifts in community composition, marked by a general decrease in community diversity. The shift in microbial community structure is mediated by frequent dietary consumption of fermentable carbohydrates and synergistic interactions between increasingly abundant acidogenic and aciduric organisms. (See refs. [13],[106] and [29]). The spatial structure of caries-associated communities also undergoes specific developmental changes during the transition to dysbiosis. The structure of caries associated biofilms is mediated by the increased production of extrapolymeric substances (EPS) by Mutans Streptococci, including on the surface of C. albicans hyphae as seen in early childhood caries and by synergistic interactions among bacteria that create a highly localized low pH microenvironment mediated by secretion of lactic acid and its sequestration within dense EPS meshworks. Unknown bacterium and Other acidogenic/aciduric organisms represent species that have been identified in molecular surveys but which have not been identified with taxonomic resolution in biofilm images. Small question marks in the diagram reflect recommended caution in drawing conclusions about inter-taxon associations because caries-associated supragingival biofilms have yet to be imaged after labeling with more than a few probes simultaneously. (See refs. [107], [29] and [80]).

Figure 2. Observed changes in dental plaque structure between states of health and periodontal disease.

Subgingival plaque communities from patients with periodontal disease have increased bacterial load and shifts in community composition that reflect a process of ecological succession. Importantly, the shift in community structure involves the expansion of a subset of organisms that are present in states of health without the displacement of other health-associated taxa. (See refs. [16] and [5]). The highly ordered physical structure of dental plaque communities has been probed with taxonomic resolution using FISH. In states of health, supragingival plaque biofilms have taxonomic distributions that reflect host and environmental inputs including oxygen concentration and salivary components as well as within-community interactions such as H₂O₂ production and oxygen sequestration to create anaerobic niches. Cells of the genus Corynebacterium were observed to play a central role in structuring the system. The spatial structure of subgingival plaque biofilms in states of health is not well studied due to the inaccessibility of these biofilms for imaging and is reflected in the graphic as a large question mark. FISH on extracted teeth from patients with periodontal disease revealed the spatial distribution of organisms with respect to the basal (tooth-associated) and apical (facing the gingival pocket) surfaces. Gingivitis is a reversible form of periodontal disease that is mediated by increased bacterial load at the gingival margin, characterized by a unique community structure not shown in this diagram. In susceptible hosts, gingivitis may progress to chronic periodontitis. Small question marks in the diagram reflect recommended caution in drawing conclusions about inter-taxon associations because subgingival biofilms have yet to be imaged after labeling with more than a few probes simultaneously. GCF = gingivo crevicular fluid. (See refs. [29], [95] and [108]).