Quorum sensing of Streptococcus mutans is activated by Aggregatibacter actinomycetemcomitans and by the periodontal microbiome

Abstract

BackgroundThe oral cavity is inhabited by complex microbial communities forming biofilms that can cause caries and periodontitis. Cell-cell communication might play an important role in modulating the physiologies of individual species, but evidence so far is limited.ResultsHere we demonstrate that a pathogen of the oral cavity, Aggregatibacter actinomycetemcomitans (A. act.), triggers expression of the quorum sensing (QS) regulon of Streptococcus mutans, a well-studied model organism for cariogenic streptococci, in dual-species biofilms grown on artificial saliva. The gene for the synthesis of the QS signal XIP is essential for this interaction. Transcriptome sequencing of biofilms revealed that S. mutans up-regulated the complete QS regulon (transformasome and mutacins) in the presence of A. act. and down-regulated oxidative stress related genes. A.act. required the presence of S. mutans for growth. Fimbriae and toxins were its most highly expressed genes and up-regulation of anaerobic metabolism, chaperones and iron acquisition genes was observed in co-culture. Metatranscriptomes from periodontal pockets showed highly variable levels of S. mutans and low levels of A. act.. Transcripts of the alternative sigma-factor SigX, the key regulator of QS in S. mutans, were significantly enriched in periodontal pockets compared to single cultures (log2 4.159, FDR ≤0.001, and expression of mutacin related genes and transformasome components could be detected.ConclusionThe data show that the complete QS regulon of S. mutans can be induced by an unrelated oral pathogen and S. mutans may be competent in oral biofilms in vivo.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-017-3618-5) contains supplementary material, which is available to authorized users.

Commensal and pathogenic biofilms differently modulate peri‐implant oral mucosa in an organotypic model

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“…There have been greater than 50 articles published over the last two decades with an emphasis on understanding cell‐cell communication in S mutans . These papers have covered a diverse array of topics including the linkage and impact of biofilm formation on this process, role in microbial interactions, overlap with stress tolerance, and single‐cell behaviors . Genetic competence is regulated by 2 signaling peptides in S mutans , competence stimulating peptide (CSP, also known as mutacin‐inducing peptide, MIP) and comX ‐inducing peptide (XIP) .…”