Abstract
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.
Highlights
Dental caries is one of the most common human infectious diseases, affecting 2.3 billion people globally, with high prevalence (60 to 90%) among underprivileged children [1, 2]
Using intact dental biofilms formed on the teeth of toddlers affected by caries, we discovered a unique 3D rotund-shaped architecture composed of multiple species arranged in a corona-like structure with an inner core of S. mutans surrounded by outer layers of non-mutans streptococci
We developed a methodology to quantify the spatial structure of microbial communities at the micron scale and found a precise spatial patterning of bacteria associated with localized caries onset
Summary
Dental caries is one of the most common human infectious diseases, affecting 2.3 billion people globally, with high prevalence (60 to 90%) among underprivileged children [1, 2]. Once these teeth were collected, we analyzed the spatial and structural organization of naturally formed biofilms on the noncavitated tooth surfaces using confocal laser scanning microscopy and computational analyses after fluorescent labeling of bacteria via taxonomic ranks (domain-genus-species) (Fig. 1A and SI Appendix, Fig. S1).
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