Antagonistic interactions by a high H2O2-producing commensal streptococcus modulate caries development by Streptococcus mutans

Dongyeop Kim, Tatsuro Ito, Anderson Hara, Yong Li, Jens Kreth, Hyun Koo

Research output: Contribution to journalArticlepeer-review

Abstract

Dental caries (tooth-decay) is caused by biofilms harboring polymicrobial communities on teeth that leads to the onset of localized areas of enamel demineralization. Streptococcus mutans has been clinically associated with severe caries in childhood. Although commensal bacteria can combat S. mutans using self-generated antimicrobials such as hydrogen peroxide (H2O2), constant sugar-rich diet consumption disrupts microbial homeostasis shifting toward cariogenic community. Recently, Streptococcus oralis subsp. tigurinus strain J22, an oral isolate, was identified as a uniquely potent H2O2 producer. Here, we assess whether a high H2O2-producing commensal streptococcus can modulate the spatial organization and virulence of S. mutans within biofilms. Using an experimental biofilm model, we find that the presence of S. oralis J22 can effectively inhibit the clustering, accumulation, and spatial organization of S. mutans on ex vivo human tooth surface, resulting in significant reduction of enamel demineralization. Notably, the generation of H2O2 via pyruvate oxidase (SpxB) from S. oralis J22 is not repressed by sugars (a common repressor in other mitis group streptococci), resulting in enhanced inhibition of S. mutans growth (vs. Streptococcus gordonii). We further investigate its impact on biofilm virulence using an in vivo rodent caries model under sugar-rich diet. Coinfection of S. mutans with S. oralis results in reduced caries development compared to either species infected alone, whereas coinfection with S. gordonii has negligible effects, suggesting that the presence of an efficient, high H2O2-producer can disrupt S. mutans virulence. This work demonstrates that oral isolates with unusual high H2O2 production may be capable of modulating biofilm cariogenicity in vivo. The findings also highlight the importance of bacterial antagonistic interactions within polymicrobial communities in health and in disease-causing state.

Original languageEnglish (US)
Pages (from-to)244-255
Number of pages12
JournalMolecular Oral Microbiology
Volume37
Issue number6
DOIs
StatePublished - Dec 2022

Keywords

  • Streptococcus oralis J22
  • caries model
  • microbial interaction
  • oral biofilm
  • synchronized biofilm-surface analysis

ASJC Scopus subject areas

  • Microbiology
  • Immunology
  • Dentistry(all)
  • Microbiology (medical)

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