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Oral multispecies biofilm development and the key role of cell–cell distance

Key Points

  • Human oral biofilms are multispecies microbial communities that attach to the surfaces of hard and soft tissues in the mouth. The ease with which these communities can be accessed has enabled detailed investigations into their composition, structure and physiology.

  • Specific adhesive interactions between genetically distinct cell types (coaggregation) contribute to the spatial and temporal development of dental plaque biofilms.

  • Microcommunities that contain coaggregation partners juxtaposed on the enamel surface can be identified and micromanipulated. The partner organisms in one of these communities were grown and analyzed in the laboratory and reconstituted as a multispecies biofilm growing on saliva.

  • In open, flowing systems an important consequence of cell–cell proximity is an ability of the cells to communicate.

  • Many oral bacteria produce autoinducer 2, which is a key signal for intercellular communication in biofilms. The presence of autoinducer 2 in two-species communities containing Streptococcus oralis and Actinomyces oris enables mutualistic growth of both organisms.

  • Oral biofilms contain vast networks of intermicrobial interactions, most of which have yet to be identified. In this respect, oral microbial communities are similar to many other biofilm systems, and studies on oral biofilms have produced a paradigm for many aspects of biofilm biology.

Abstract

Growth of oral bacteria in situ requires adhesion to a surface because the constant flow of host secretions thwarts the ability of planktonic cells to grow before they are swallowed. Therefore, oral bacteria evolved to form biofilms on hard tooth surfaces and on soft epithelial tissues, which often contain multiple bacterial species. Because these biofilms are easy to study, they have become the paradigm of multispecies biofilms. In this Review we describe the factors involved in the formation of these biofilms, including the initial adherence to the oral tissues and teeth, cooperation between bacterial species in the biofilm, signalling between the bacteria and its role in pathogenesis, and the transfer of DNA between bacteria. In all these aspects distance between cells of different species is integral for oral biofilm growth.

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Figure 1: Oral bacterial colonization.
Figure 2: Relationship between succession of oral communities and autoinducer 2.
Figure 3: Mutualistic Fusobacterium nucleatumAggregatibacter actinomycetemcomitansVeillonella sp. biofilm.

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Acknowledgements

This work was improved by the comments of three anonymous reviewers and was supported in part by the Intramural Research Program of the National Institute of Dental and Craniofacial Research, National Institutes of Health.

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Correspondence to Paul E. Kolenbrander.

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Glossary

Phylotype

A taxonomic unit typically defined by 99% similar 16S rRNA gene sequences; this is the molecular equivalent of a species and it allows inclusion of yet-to-be cultured organisms in a taxonomic framework.

Gingival crevicular fluid

Host-derived exudate into the sulcus.

Salivary pellicle

A layer of proteins and glycoproteins of salivary origin that permanently coats the surfaces of oral tissues.

Desquamating surface

A surface that sheds the outer layers.

Coadhesion

The adherence of a planktonic microorganism to a genetically distinct microbial cell that is immobilized on a surface.

Coaggregation

The binding of two genetically distinct microorganisms suspended in the fluid phase that occurs by means of highly specific interactions between components on the respective cell surfaces.

Supragingival dental plaque

Dental plaque that occurs on areas of the teeth that are not covered by gum tissue.

Subgingival dental plaque

Dental plaque on tooth surfaces below the level of the gums.

Periodontitis

Inflammatory gum disease involving the destruction of the tissues surrounding the teeth, loss of attachment of the gums and the creation of a 'pocket' between the teeth and gums.

Gingivitis

Minor and reversible inflammation of the gum tissue.

Competent

State of bacteria in which they can take up extracellular DNA from the environment.

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Kolenbrander, P., Palmer, R., Periasamy, S. et al. Oral multispecies biofilm development and the key role of cell–cell distance. Nat Rev Microbiol 8, 471–480 (2010). https://doi.org/10.1038/nrmicro2381

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