Biogeography of a human oral microbiome at the micron scale

Abstract

The spatial organization of complex natural microbiomes is critical to understanding the interactions of the individual taxa that comprise a community. Although the revolution in DNA sequencing has provided an abundance of genomic-level information, the biogeography of microbiomes is almost entirely uncharted at the micron scale. Using spectral imaging fluorescence in situ hybridization as guided by metagenomic sequence analysis, we have discovered a distinctive, multigenus consortium in the microbiome of supragingival dental plaque. The consortium consists of a radially arranged, nine-taxon structure organized around cells of filamentous corynebacteria. The consortium ranges in size from a few tens to a few hundreds of microns in radius and is spatially differentiated. Within the structure, individual taxa are localized at the micron scale in ways suggestive of their functional niche in the consortium. For example, anaerobic taxa tend to be in the interior, whereas facultative or obligate aerobes tend to be at the periphery of the consortium. Consumers and producers of certain metabolites, such as lactate, tend to be near each other. Based on our observations and the literature, we propose a model for plaque microbiome development and maintenance consistent with known metabolic, adherence, and environmental considerations. The consortium illustrates how complex structural organization can emerge from the micron-scale interactions of its constituent organisms. The understanding that plaque community organization is an emergent phenomenon offers a perspective that is general in nature and applicable to other microbiomes.biofilm | imaging | microscopy | microbial ecology B iogeography-the study of the distribution of organisms across the globe-seeks to recognize patterns in the spatial distribution of organisms and discover the forces that underlie those patterns. Bacteria are micron-sized, and many of the forces and factors that underlie their distributional patterns operate at micron scales and are qualitatively different from the large-scale factors, such as climate, that drive traditional biogeography. To frame the analysis of microbial distribution patterns at the scale that microbes themselves experience, we introduce the concept of micron-scale biogeography: the study of the distribution of microbes relative to micron-scale features of their environment. These features include the host or inanimate surfaces on which the microbes reside as well as local gradients of nutrients and oxygen. Key components of the micron-scale environment, particularly in biofilms and other densely populated habitats, are the microbes themselves, serving as substrates for attachment of other microbes, creating spatial structure, and acting as point sources for diffusible metabolites.Micron-scale biogeography is critical to understanding the physiology and ecology of the community as well as its systems biology and its effects on human health and disease. Close proximity or physical contact between two microbes can substantially a...

Two-component signal transduction systems in oral bacteria

“…According to the predicted model of oral biofilm formation, streptococci are substrate-adhering pioneer bacteria, fusobacteria are bridging organisms, and P. gingivalis is a late colonizer that was shown by direct imaging to bind to both Streptococcus and Fusobacterium [32]. A series of studies examined proteomic and gene expression of P. gingivalis , Streptococcus gordonii , and F. nucleatum in a simulated biofilm in which resting cocultures were incubated for 18 h under anaerobic conditions [33–35].…”

Organization of supragingival plaque at the micron scale

“…Although the revolution in bacterial sequencing has left us with an unprecedented abundance of data regarding the diversity and abundance of bacteria in caries and periodontal diseases, detailed information on the organization of dental biofilms in man in micrometre scale is lacking. By using spectral imaging fluorescence in situ hybridization guided by metagenomic sequence analysis, Mark Welch et al [1] described a multigenus, highly organized microbial consortium in human supragingival plaque. Their unique methodology (CLASI-FISH) (see reference [2] for additional details) was developed by Gary Borisy at the Forsyth Institute, Cambridge, MA, USA.…”

“…CLASI-FISH is clearly different from nucleic acid methods where the structure of plaque is destroyed. Mark Welch et al [1] applied spectral fluorescence imaging to examine the structures produced by nine key bacterial taxa of supragingival plaque. By using sequencing data from the HMP [4], major bacterial taxa thought to be prevalent and abundant in the overall structure and function of supragingival plaque were selected and by imaging the spatial organization of these taxa, a complex, spatially organized, multigenus consortium of bacteria was detected.…”

“…Mark Welch et al [1] reported that supragingival biofilm from 22 healthy volunteers consisted of a radially arranged, nine-taxon structure that was established around cells of filamentous corynebacteria. This bacterial consortium had a radius ranging from a few tens to a few hundreds of microns and was spatially differentiated.…”

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Figure 1.Schematic drawing of the hypothesis for interpreting hedgehog structures in supragingival plaque (from ref. [1]).Permission has been granted from PNAS.

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