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

Research output: Contribution to journalArticle

1 Scopus citations

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 mixedspecies 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.

Original languageEnglish (US)
Article number12375
JournalProceedings of the National Academy of Sciences of the United States of America
Volume117
Issue number22
DOIs
StatePublished - Jun 2 2020

Keywords

  • Biofilm
  • Biogeography
  • Dental caries
  • Polymicrobial
  • Streptococcus mutans

ASJC Scopus subject areas

  • General

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