How biogeography of the oral microbiome affects dental caries

A US study in PNAS shows how the spatial structure affects the progression of localised dental caries.
How biogeography of the oral microbiome affects dental caries

A new paper out in PNAS has identified a specific spatial organisation of bacteria associated with dental caries in toddlers. The study examined microbial communities on clinical samples of dental caries and identified a number of different spatial structures, one of which was far more prevalent than the others. The team were then able to recreate this structure in the lab and show that it had the demineralising properties of a caries biofilm.

While examining the structure of caries biofilms from clinical samples, the research team led by Marvin Whiteley from Georgia Tech and Hyun Koo from the University of Pennsylvania found that the biofilm architectures fit into one of four types, corncob, hedgehog, seaweed or rotund. While all of these structures were found on caries tooth samples, the rotund shape was present much more often, seen in 21 out of 30 samples.

The research team then set out to see if they could recreate this “rotund” structure in the lab and to see if it would produce demineralisation and increased pH associated with caries. To produce the rotund structure, the researchers had to produce an inner core of Streptococcus mutans with an outer core of protective non-mutans streptococci.

They achieved this and indeed saw that the structure produced a localised acidic pH as well as demineralisation of the enamel in the lab. In other words, they had produced a representative model for the clinical observations on the teeth.

They then used this model to look at treatment options. They saw that the outer coat of non-mutans streptococci had a protective effect when treating the biofilm with chlorohexadine. This effect disappeared when the biofilm’s protective non-mutans streptococci corona was disrupted.

"It's clear that identifying the constituents of the human microbiome is not enough to understand their impact on human health. We also have to know how they are spatially organized. This is largely under studied as obtaining intact samples that maintain spatial structure is difficult,” - explained co-lead author Marvin Whiteley.

The findings in this paper are interesting for a number of reasons, not least of which the antagonism previously described between S. oralis and S. mutans. This work suggests that given a specific spatial arrangement, S. oralis could actually protect S. mutans. The authors of the paper stopped short of claiming this, citing that animal models were needed to fully validate this finding in vivo

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Spatial mapping of polymicrobial communities reveals a precise biogeography associated with human dental caries

Dongyeop Kim, Juan P. Barraza, Rodrigo A. Arthur, Anderson Hara, Karl Lewis, Yuan Liu, Elizabeth L. Scisci, Evlambia Hajishengallis, Marvin Whiteley, Hyun Koo

Proceedings of the National Academy of Sciences May 2020, 201919099; DOI: 10.1073/pnas.1919099117


Tooth decay (dental caries) is a widespread human disease caused by microbial biofilms. Streptococcus mutans, a biofilm-former, has been consistently associated with severe childhood caries; however, how this bacterium is spatially organized with other microorganisms in the oral cavity to promote disease remains unknown. Using intact biofilms formed on teeth of toddlers affected by caries, we discovered a unique 3D rotund-shaped architecture composed of multiple species precisely arranged in a corona-like structure with an inner core of S. mutans encompassed by outer layers of other bacteria. This architecture creates localized regions of acidic pH and acute enamel demineralization (caries) in a mixed-species biofilm model on human teeth, suggesting this highly ordered community as the causative agent. Notably, the construction of this architecture was found to be an active process initiated by production of an extracellular scaffold by S. mutans that assembles the corona cell arrangement, encapsulating the pathogen core. In addition, this spatial patterning creates a protective barrier against antimicrobials while increasing bacterial acid fitness associated with the disease-causing state. Our data reveal a precise biogeography in a polymicrobial community associated with human caries that can modulate the pathogen positioning and virulence potential in situ, indicating that micron-scale spatial structure of the microbiome may mediate the function and outcome of host–pathogen interactions.

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