Biogeography of the Oral Microbiome: The Site-Specialist Hypothesis

Abstract

Microbial communities are complex and dynamic, composed of hundreds of taxa interacting across multiple spatial scales. Advances in sequencing and imaging technology have led to great strides in understanding both the composition and the spatial organization of these complex communities. In the human mouth, sequencing results indicate that distinct sites host microbial communities that not only are distinguishable but to a meaningful degree are composed of entirely different microbes. Imaging suggests that the spatial organization of these communities is also distinct. Together, the literature supports the idea that most oral microbes are site specialists. A clear understanding of microbiota structure at different sites in the mouth enables mechanistic studies, informs the generation of hypotheses, and strengthens the position of oral microbiology as a model system for microbial ecology in general.

Keywords: biofilm; fluorescence microscopy; human microbiome; imaging; metagenomics; microbial ecology.

Figure 1.. Site specificity in the oral microbiome.

The position of each species represents its relative abundance in three distinct oral sites: supragingival plaque, tongue dorsum, and keratinized gingiva. The y-axis shows the ratio of the taxon’s normalized abundance in supragingival plaque to its normalized abundance in tongue dorsum; the x-axis shows the ratio of normalized abundance in keratinized gingiva to the mean of the supragingival plaque and tongue dorsum normalized abundance. The area of points is proportional to the mean abundance of the taxon in its site of greatest normalized abundance. Color indicates the genus; species are as follows: An, Actinomyces naeslundii group; Ao, Actinomyces odontolyticus group; Ag, Actinomyces graevenitzii; Cm, Corynebacterium matruchotii; Fn, Fusobacterium nucleatum; Fp, Fusobacterium periodonticum; F. sp. 248, Fusobacterium sp. HMT 248; Gh, Gemella haemolysans; Gs, Gemella sanguinis; Ga, Granulicatella adiacens; Ge, Granulicatella elegans; Hh, Haemophilus haemolyticus group; Hp, Haemophilus parainfluenzae; Lm, Lautropia mirabilis; Lb, Leptotrichia buccalis group; L. sp. 221, Leptotrichia sp. HMT 221; Nf, Neisseria flavescens group; Nm, Neisseria mucosa group; Pp, Porphyromonas pasteri; P. sp. 930, Porphyromonas sp. HMT 930; Pm, Prevotella melaninogenica; A. sp. 473, Alloprevotella sp. HMT 473; Rd, Rothia dentocariosa; Rm, Rothia mucilaginosa; Sg, Streptococcus gordonii; Ssan, Streptococcus sanguinis; Sm, Streptococcus mitis; Ssal; Streptococcus salivarius; Sp, Streptococcus parasanguinis group; Va, Veillonella atypica; Vp1, Veillonella parvula/dispar group 1; Vp2, Veillonella parvula/dispar group 2; Vr, Veillonella rogosae; V. sp. 780 Veillonella sp. HMT 780. Data is from the Human Microbiome Project analyzed with oligotyping (26) and mapped to eHOMD version15.1 (www.homd.org).

Figure 2.. Imaging reveals dense and highly organized communities in the human oral microbiome.

(A): a “hedgehog” structure from dental plaque. Corynebacterium (magenta filaments) radiate outward from a central point forming a spatially structured habitat inhabited by other taxa at characteristic positions. Cocci (Streptococcus, green; Porphyromonas, blue, Haemophilus/Aggregatibacter, orange) occupy an outer shell; microaerophilic taxa (Fusobacterium, yellow; Leptotrichia, cyan) occupy a presumably low-oxygen zone inside the outer shell. See Mark Welch et al 2016. (B): a biofilm scraped from the surface of the tongue and imaged using CLASI-FISH. Human epithelial tissue forms a central core (gray). Actinomyces (red) occupy a region close to the core; Streptococcus (green) is localized in an exterior crust and in stripes in the interior. Other taxa (Rothia, cyan; Neisseria, yellow; Veillonella, magenta) are present in clusters and stripes that suggest growth of the community outward from the central core. S. Wilbert et al., manuscript in preparation.