Selenomonas sputigena acts as a pathobiont mediating spatial structure and biofilm virulence in early childhood caries

Hunyong Cho, Zhi Ren, Kimon Divaris (), Jeffrey Roach, Bridget M. Lin, Chuwen Liu, M. Andrea Azcarate-Peril, Miguel A. Simancas-Pallares, Poojan Shrestha, Alena Orlenko, Jeannie Ginnis, Kari E. North, Andrea G. Ferreira Zandona, Apoena Aguiar Ribeiro, Di Wu () and Hyun Koo ()
Additional contact information
Hunyong Cho: University of North Carolina at Chapel Hill
Zhi Ren: University of Pennsylvania
Kimon Divaris: University of North Carolina at Chapel Hill
Jeffrey Roach: University of North Carolina at Chapel Hill
Bridget M. Lin: University of North Carolina at Chapel Hill
Chuwen Liu: University of North Carolina at Chapel Hill
M. Andrea Azcarate-Peril: University of North Carolina at Chapel Hill
Miguel A. Simancas-Pallares: University of North Carolina at Chapel Hill
Poojan Shrestha: University of North Carolina at Chapel Hill
Alena Orlenko: Cedars-Sinai Medical Center
Jeannie Ginnis: University of North Carolina at Chapel Hill
Kari E. North: University of North Carolina at Chapel Hill
Andrea G. Ferreira Zandona: Tufts University
Apoena Aguiar Ribeiro: University of North Carolina at Chapel Hill
Di Wu: University of North Carolina at Chapel Hill
Hyun Koo: University of Pennsylvania

Nature Communications, 2023, vol. 14, issue 1, 1-19

Abstract: Abstract Streptococcus mutans has been implicated as the primary pathogen in childhood caries (tooth decay). While the role of polymicrobial communities is appreciated, it remains unclear whether other microorganisms are active contributors or interact with pathogens. Here, we integrate multi-omics of supragingival biofilm (dental plaque) from 416 preschool-age children (208 males and 208 females) in a discovery-validation pipeline to identify disease-relevant inter-species interactions. Sixteen taxa associate with childhood caries in metagenomics-metatranscriptomics analyses. Using multiscale/computational imaging and virulence assays, we examine biofilm formation dynamics, spatial arrangement, and metabolic activity of Selenomonas sputigena, Prevotella salivae and Leptotrichia wadei, either individually or with S. mutans. We show that S. sputigena, a flagellated anaerobe with previously unknown role in supragingival biofilm, becomes trapped in streptococcal exoglucans, loses motility but actively proliferates to build a honeycomb-like multicellular-superstructure encapsulating S. mutans, enhancing acidogenesis. Rodent model experiments reveal an unrecognized ability of S. sputigena to colonize supragingival tooth surfaces. While incapable of causing caries on its own, when co-infected with S. mutans, S. sputigena causes extensive tooth enamel lesions and exacerbates disease severity in vivo. In summary, we discover a pathobiont cooperating with a known pathogen to build a unique spatial structure and heighten biofilm virulence in a prevalent human disease.

Date: 2023
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DOI: 10.1038/s41467-023-38346-3

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