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The rgg gene of Streptococcus pyogenes NZ131 positively influences extracellular SPE B production.

ABSTRACT: Streptococcus pyogenes produces several extracellular proteins, including streptococcal erythrogenic toxin B (SPE B), also known as streptococcal pyrogenic exotoxin B and streptococcal proteinase. Several reports suggest that SPE B contributes to the virulence associated with S. pyogenes; however, little is known about its regulation. Nucleotide sequence data revealed the presence, upstream of the speB gene, of a gene, designated rgg, that was predicted to encode a polypeptide similar to previously described positive regulatory factors. The putative Rgg polypeptide of S. pyogenes NZ131 consisted of 280 amino acids and had a predicted molecular weight of 33,246. To assess the potential role of Rgg in the production of SPE B, the rgg gene was insertionally inactivated in S. pyogenes NZ131, which resulted in markedly decreased SPE B production, as determined both by immunoblotting and caseinolytic activity on agar plates. However, the production of other extracellular products, including streptolysin O, streptokinase, and DNase, was not affected. Complementation of the rgg mutant with an intact rgg gene copy in S. pyogenes NZ131 could restore SPE B production and confirmed that the rgg gene product is involved in the production of SPE B.

SUBMITTER: Chaussee MS

PROVIDER: S-EPMC96519 | biostudies-literature | 1999 Apr

REPOSITORIES: biostudies-literature

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The rgg gene of Streptococcus pyogenes NZ131 positively influences extracellular SPE B production.

Chaussee M S MS Ajdic D D Ferretti J J JJ

Infection and immunity 19990401 4

Streptococcus pyogenes produces several extracellular proteins, including streptococcal erythrogenic toxin B (SPE B), also known as streptococcal pyrogenic exotoxin B and streptococcal proteinase. Several reports suggest that SPE B contributes to the virulence associated with S. pyogenes; however, little is known about its regulation. Nucleotide sequence data revealed the presence, upstream of the speB gene, of a gene, designated rgg, that was predicted to encode a polypeptide similar to previou ...[more]

PMID: 10085009

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Project description:Recent studies have established the fact that multiple members of the Rgg family of transcriptional regulators serve as key components of quorum sensing (QS) pathways that utilize peptides as intercellular signaling molecules. We previously described a novel QS system in Streptococcus pyogenes which utilizes two Rgg-family regulators (Rgg2 and Rgg3) that respond to neighboring signaling peptides (SHP2 and SHP3) to control gene expression and biofilm formation. We have shown that Rgg2 is a transcriptional activator of target genes, whereas Rgg3 represses expression of these genes, and that SHPs function to activate the QS system. The mechanisms by which Rgg proteins regulate both QS-dependent and QS-independent processes remain poorly defined; thus, we sought to further elucidate how Rgg2 and Rgg3 mediate gene regulation. Here we provide evidence that S. pyogenes employs a unique mechanism of direct competition between the antagonistic, peptide-responsive proteins Rgg2 and Rgg3 for binding at target promoters. The highly conserved, shared binding sites for Rgg2 and Rgg3 are located proximal to the -35 nucleotide in the target promoters, and the direct competition between the two regulators results in concentration-dependent, exclusive occupation of the target promoters that can be skewed in favor of Rgg2 in vitro by the presence of SHP. These results suggest that exclusionary binding of target promoters by Rgg3 may prevent Rgg2 binding under SHP-limiting conditions, thereby preventing premature induction of the quorum sensing circuit. Rgg-family transcriptional regulators are widespread among low-G+C Gram-positive bacteria and in many cases contribute to bacterial physiology and virulence. Only recently was it discovered that several Rgg proteins function in cell-to-cell communication (quorum sensing [QS]) via direct interaction with signaling peptides. The mechanism(s) by which Rgg proteins mediate regulation is poorly understood, and further insight into Rgg function is anticipated to be of great importance for the understanding of both regulatory-network architecture and intercellular communication in Rgg-containing species. The results of this study on the Rgg2/3 QS circuit of S. pyogenes demonstrate that DNA binding of target promoters by the activator Rgg2 is directly inhibited by competitive binding by the repressor Rgg3, thereby preventing transcriptional activation of the target genes and premature induction of the QS circuit. This is a unique regulatory mechanism among Rgg proteins and other peptide-responsive QS regulators.

Dataset Information

The rgg gene of Streptococcus pyogenes NZ131 positively influences extracellular SPE B production.

Publications

The rgg gene of Streptococcus pyogenes NZ131 positively influences extracellular SPE B production.

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