A Novel Pheromone Quorum-Sensing System Controls the Development of Natural Competence in Streptococcus thermophilus and Streptococcus salivarius

• DOI: 10.1128/jb.01251-09
• Publication Date: 2009-12-19T02:41:52Z
• Authors: Laetitia Fontaine; Céline Boutry; Marie Henry de Fr...; Brigitte Delplace; Christophe Fremaux; Philippe Horvath; Patrick Boyaval; Pascal Hols
• Keywords: 0301 basic medicine; Gene Expression Profiling; Quorum Sensing; Gene Expression Regulation, Bacterial; Pheromones; 03 medical and health sciences; Transformation, Genetic; Bacterial Proteins; Operon; Streptococcus thermophilus; Peptides; Sequence Deletion; Signal Transduction; Transcription Factors

ABSTRACT

In streptococcal species, the key step of competence development is the transcriptional induction of comX , which encodes the alternative sigma factor σ X , which positively regulates genes necessary for DNA transformation. In Streptococcus species belonging to the mitis and mutans groups, induction of comX relies on the activation of a three-component system consisting of a secreted pheromone, a histidine kinase, and a response regulator. In Streptococcus thermophilus , a species belonging to the salivarius group, the oligopeptide transporter Ami is essential for comX expression under competence-inducing conditions. This suggests a different regulation pathway of competence based on the production and reimportation of a signal peptide. The objective of our work was to identify the main actors involved in the early steps of comX induction in S. thermophilus LMD-9. Using a transcriptomic approach, four highly induced early competence operons were identified. Among them, we found a Rgg-like regulator (Ster_0316) associated with a nonannotated gene encoding a 24-amino-acid hydrophobic peptide (Shp0316). Through genetic deletions, we showed that these two genes are essential for comX induction. Moreover, addition to the medium of synthetic peptides derived from the C-terminal part of Shp0316 restored comX induction and transformation of a Shp0316-deficient strain. These peptides also induced competence in S. thermophilus and Streptococcus salivarius strains that are poorly transformable or not transformable. Altogether, our results show that Ster_0316 and Shp0316, renamed ComRS, are the two members of a novel quorum-sensing system responsible for comX induction in species from the salivarius group, which differs from the classical phosphorelay three-component system identified previously in streptococci.