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

Szymon P Szafrański,Helena Sztajer,Irene Wagner-Döbler,Michael Jarek,Manfred Rohde,Zhi-Luo Deng,Jürgen Tomasch,Sabin Bhuju

doi:10.1186/s12864-017-3618-5

Szymon P Szafrański, Helena Sztajer + Show 6 more

Open Access

https://doi.org/10.1186/s12864-017-3618-5

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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.

Highlights

The oral cavity is inhabited by complex microbial communities forming biofilms that can cause caries and periodontitis
Induction of the alternative sigma-factor SigX of S. mutans by A. act To determine if A.act. is able to induce quorum sensing (QS) in S. mutans we co-cultured it with a reporter strain
The complete quorum sensing regulon of S. mutans was induced by A. act. by an unknown mechanism which required the presence of Autoinducer synthase for the sigX-inducing peptide (XIP) prepeptide (ComS), the synthase for the XIP prepeptide

Summary

Introduction

The oral cavity is inhabited by complex microbial communities forming biofilms that can cause caries and periodontitis. Cultivation independent studies, metagenome and metatranscriptome analyses, have completely revolutionized our understanding of oral diseases like caries and periodontitis. They clearly show that S. mutans is only a tiny component of the active oral microbiome. The etiology of caries is one of the prime examples for the paradigm shift from Kochs postulates towards the concept of a polymicrobial origin of disease caused by a shift in the composition and metabolic activity of a complex community towards dysbiosis [6]. Modifying the interaction pattern could potentially have complex downstream effects on the community [7]

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