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Review
. 2023 Sep 14;91(9):e0012423.
doi: 10.1128/iai.00124-23. Epub 2023 Aug 18.

Social networking at the microbiome-host interface

Richard J Lamont #  1 , George Hajishengallis #  2 , Hyun Koo #  3   4
Affiliations
Review

Social networking at the microbiome-host interface

Richard J Lamont et al. Infect Immun. .

Abstract

Microbial species colonizing host ecosystems in health or disease rarely do so alone. Organisms conglomerate into dynamic heterotypic communities or biofilms in which interspecies and interkingdom interactions drive functional specialization of constituent species and shape community properties, including nososymbiocity or pathogenic potential. Cell-to-cell binding, exchange of signaling molecules, and nutritional codependencies can all contribute to the emergent properties of these communities. Spatial constraints defined by community architecture also determine overall community function. Multilayered interactions thus occur between individual pairs of organisms, and the relative impact can be determined by contextual cues. Host responses to heterotypic communities and impact on host surfaces are also driven by the collective action of the community. Additionally, the range of interspecies interactions can be extended by bacteria utilizing host cells or host diet to indirectly or directly influence the properties of other organisms and the community microenvironment. In contexts where communities transition to a dysbiotic state, their quasi-organismal nature imparts adaptability to nutritional availability and facilitates resistance to immune effectors and, moreover, exploits inflammatory and acidic microenvironments for their persistence.

Keywords: dental caries; periodontal disease; polymicrobial community.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig 1
Fig 1
Interbacterial and interkingdom interactions in oral polymicrobial communities. (A) The oral microbiota harbors a multitude of different microbes, including bacteria, fungi, viruses, and ultra-small organisms. These diverse microbial populations engage in complex interspecies or cross-kingdom interactions which drive cooperative, competitive, or both outcomes among community members. Certain species, such as Streptococcus mutans, form highly clustered communities with precise spatial structure at the infection site (supragingival) which promotes a disease-causing state (dental caries). (B) Complex physical and chemical interactions with different species promote a multilayered, corona-like spatial arrangement formed by an inner core composed almost exclusively of S. mutans and outer layers of other oral microbes, physically separated by extracellular polymeric substances. This spatial structure enhances bacterial fitness and protection, and creates a highly acidic microenvironment, leading to the localized onset of disease. Precise positioning and spatial arrangement combined with polymicrobial interactions can coordinate pathogenesis in situ to create virulence hotspots impacting the host tissues. [Adapted from reference (12) with permission from Elsevier.]
Fig 2
Fig 2
The P. gingivalis interactome. (A) Overview (not to scale) of interactions of P. gingivalis with other bacteria, bacterial communities, and with gingival epithelial cells. Green arrows represent a synergistic relationship which increases the colonization, growth, or pathogenicity of P. gingivalis, or an increase in an epithelial cell signaling pathway. Red flat arrows represent an antagonistic relationship. (B) The streptococcal metabolite para-amino benzoic acid (pABA) and physical attachment between P. gingivalis and S. gordonii have opposing effects on pathogenicity, although both funnel through activation/inactivation of the Ptk1 tyrosine kinase signaling pathway. (C) Indirect communication between S. gordonii and P. gingivalis involving the epithelial cell as an intermediary. S. gordonii can activate the TAK1-NLK pathway, which mitigates P. gingivalis stimulation of FOXO1-Zeb2 signaling. P. gingivalis, however, can enhance Zeb2 activity through pathways that are insulated from S. gordonii.
Fig 3
Fig 3
Interspecies and microbe-host interactions that promote dysbiosis and inflammatory disease. Whereas communities of predominantly eubiotic commensals induce balanced immune responses that contribute to homeostatic immunity and a healthy periodontal tissue, dysbiotic communities induce dysregulated inflammatory responses that are detrimental for the host and ineffective in controlling the bacteria. In polymicrobial communities associated with periodontitis, keystone pathogens are aided by accessory pathogens in terms of metabolic and/or colonization support and, once established, can subvert host immunity in a manner that contributes to the outgrowth of inflammophilic pathobionts. Community members engage in complex interspecies communication that elevates the expression of virulence factors and the pathogenicity of the entire community. A key environmental factor that aggravates dysbiosis and pathobiont expansion is destructive inflammation, which not only drives bone loss but also generates tissue breakdown products that can be used as nutrients by the dysbiotic community. These mutually reinforcing interactions between dysbiosis and inflammation represent a self-sustained feed-forward loop that constitutes the actual driver of periodontitis and can explain, in great part, its chronic nature.
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