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 ofS. mutansencompassed 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 byS. mutansthat 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.

Isolation and Identification of Potentially Pathogenic Microorganisms Associated with Dental Caries in Human Teeth Biofilms

“…The cariogenic biofilm of human teeth is a unique 3D circular structure made up of multiple species, with S. mutans at its core and other acidogenic microorganisms on its periphery, this community is the causative factor [ 24 ]. Cariogenic microorganisms are symbiotic in the biofilm.…”

Priority effects dictate community structure and alter virulence of fungal-bacterial biofilms

“…For example, the Gram-negative bacterium Pseudomonas aeruginosa can have both synergistic and antagonistic effects on C. albicans, even resulting in fungal death [29,[46][47][48][49][50], signifying the complicated and dynamic interactions occurring within microbial communities. Furthermore, the physical orientation of fungal-bacterial biofilms suggests that their assembly and growth likely involves a temporal component [51][52][53][54][55].…”

Droplet printing reveals the importance of micron-scale structure for bacterial ecology

“…However, natural spatial structure often occurs at much finer scales, with data from the mammalian microbiome suggesting that the micron-to-millimetre scale is particularly important 6,11,28 . For example, while there appears to be significant genotypic mixing in the gut microbiome 29 , the dental and tongue microbiome is more structured, with patches of bacteria dominated by one genotype reaching tens to hundreds of microns in scale 8,9,30 . Moreover, there is evidence that solute gradients within bacterial communities can limit the distance at which cells affect each other to micron scales [31][32][33] , raising the possibility that differences in the arrangement of genotypes at these scales will have impacts.…”