Cryptic Competence Pathway in Streptococcus pyogenes Is Controlled by a Peptide Pheromone

• Published in: Journal of Bacteriology 2012-09, Vol.194 (17), p.4589-4600
• Main Authors: Mashburn-Warren, Lauren, Morrison, Donald A, Federle, Michael J
• Format: Article
• Language: English
• Subjects: bacteria; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; Bacteriology; Biological and medical sciences; Cytoplasm; Deoxyribonucleic acid; DNA; DNA Transformation Competence; Endopeptidase Clp; evolution; Fundamental and applied biological sciences. Psychology; Gene expression; Gene Expression Regulation, Bacterial; Gene Transfer, Horizontal; genetic transformation; Genetics; horizontal gene transfer; Microbiology; pathogens; Peptides; Peptides - genetics; Peptides - metabolism; Pheromones; Pheromones - genetics; Pheromones - metabolism; proteinases; Quorum Sensing; radiolabeling; regulon; Serine Endopeptidases - genetics; Serine Endopeptidases - metabolism; Sigma Factor - genetics; Sigma Factor - metabolism; Streptococcus bovis; Streptococcus infections; Streptococcus mutans; Streptococcus pyogenes; Streptococcus pyogenes - genetics; Streptococcus pyogenes - metabolism; Trans-Activators - genetics; Trans-Activators - metabolism; transcription factors; Transformation, Bacterial
• ISSN: 0021-9193; 1098-5530; 1067-8832
• DOI: 10.1128/JB.00830-12

Horizontal gene transfer is an important means of bacterial evolution that is facilitated by transduction, conjugation, and natural genetic transformation. Transformation occurs after bacterial cells enter a state of competence, where naked DNA is acquired from the extracellular environment. Induction of the competent state relies on signals that activate master regulators, causing the expression of genes involved in DNA uptake, processing, and recombination. All streptococcal species contain the master regulator SigX and SigX-dependent effector genes required for natural genetic transformation; however, not all streptococcal species have been shown to be naturally competent. We recently demonstrated that competence development in Streptococcus mutans requires the type II ComRS quorum-sensing circuit, comprising an Rgg transcriptional activator and a novel peptide pheromone (L. Mashburn-Warren, D. A. Morrison, and M. J. Federle, Mol. Microbiol. 78:589–606, 2010). The type II ComRS system is shared by the pyogenic, mutans, and bovis streptococci, including the clinically relevant pathogen Streptococcus pyogenes. Here, we describe the activation of sigX by a small-peptide pheromone and an Rgg regulator of the type II ComRS class. We confirm previous reports that SigX is functional and able to activate sigX-dependent gene expression within the competence regulon, and that SigX stability is influenced by the cytoplasmic protease ClpP. Genomic analyses of available S. pyogenes genomes revealed the presence of intact genes within the competence regulon. While this is the first report to show natural induction of sigX, S. pyogenes remained nontransformable under laboratory conditions. Using radiolabeled DNA, we demonstrate that transformation is blocked at the stage of DNA uptake.