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


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.

SUBMITTER: Kim D 

PROVIDER: S-EPMC7275741 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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

Kim Dongyeop D   Barraza Juan P JP   Arthur Rodrigo A RA   Hara Anderson A   Lewis Karl K   Liu Yuan Y   Scisci Elizabeth L EL   Hajishengallis Evlambia E   Whiteley Marvin M   Koo Hyun H  

Proceedings of the National Academy of Sciences of the United States of America 20200518 22


Tooth decay (dental caries) is a widespread human disease caused by microbial biofilms. <i>Streptococcus mutans</i>, 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  ...[more]

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