Competence in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Is Regulated by the Rate of Ribosomal Decoding Errors

ABSTRACT Competence for genetic transformation in Streptococcus pneumoniae develops in response to accumulation of a secreted peptide pheromone and was one of the initial examples of bacterial quorum sensing. Activation of this signaling system induces not only expression of the proteins required fo...

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Autores principales:	Kathleen E. Stevens, Diana Chang, Erin E. Zwack, Michael E. Sebert
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2011
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/2dfc9b2d5e9c42e09be8d857f8539922
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spelling	oai:doaj.org-article:2dfc9b2d5e9c42e09be8d857f85399222021-11-15T15:38:58ZCompetence in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Is Regulated by the Rate of Ribosomal Decoding Errors10.1128/mBio.00071-112150-7511https://doaj.org/article/2dfc9b2d5e9c42e09be8d857f85399222011-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00071-11https://doaj.org/toc/2150-7511ABSTRACT Competence for genetic transformation in Streptococcus pneumoniae develops in response to accumulation of a secreted peptide pheromone and was one of the initial examples of bacterial quorum sensing. Activation of this signaling system induces not only expression of the proteins required for transformation but also the production of cellular chaperones and proteases. We have shown here that activity of this pathway is sensitively responsive to changes in the accuracy of protein synthesis that are triggered by either mutations in ribosomal proteins or exposure to antibiotics. Increasing the error rate during ribosomal decoding promoted competence, while reducing the error rate below the baseline level repressed the development of both spontaneous and antibiotic-induced competence. This pattern of regulation was promoted by the bacterial HtrA serine protease. Analysis of strains with the htrA (S234A) catalytic site mutation showed that the proteolytic activity of HtrA selectively repressed competence when translational fidelity was high but not when accuracy was low. These findings redefine the pneumococcal competence pathway as a response to errors during protein synthesis. This response has the capacity to address the immediate challenge of misfolded proteins through production of chaperones and proteases and may also be able to address, through genetic exchange, upstream coding errors that cause intrinsic protein folding defects. The competence pathway may thereby represent a strategy for dealing with lesions that impair proper protein coding and for maintaining the coding integrity of the genome. IMPORTANCE The signaling pathway that governs competence in the human respiratory tract pathogen Streptococcus pneumoniae regulates both genetic transformation and the production of cellular chaperones and proteases. The current study shows that this pathway is sensitively controlled in response to changes in the accuracy of protein synthesis. Increasing the error rate during ribosomal decoding induced competence, while decreasing the error rate repressed competence. This pattern of regulation was promoted by the HtrA protease, which selectively repressed competence when translational fidelity was high but not when accuracy was low. Our findings demonstrate that this organism is able to monitor the accuracy of information used for protein biosynthesis and suggest that errors trigger a response addressing both the immediate challenge of misfolded proteins and, through genetic exchange, upstream coding errors that may underlie protein folding defects. This pathway may represent an evolutionary strategy for maintaining the coding integrity of the genome.Kathleen E. StevensDiana ChangErin E. ZwackMichael E. SebertAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 2, Iss 5 (2011)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Kathleen E. Stevens Diana Chang Erin E. Zwack Michael E. Sebert Competence in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Is Regulated by the Rate of Ribosomal Decoding Errors
description	ABSTRACT Competence for genetic transformation in Streptococcus pneumoniae develops in response to accumulation of a secreted peptide pheromone and was one of the initial examples of bacterial quorum sensing. Activation of this signaling system induces not only expression of the proteins required for transformation but also the production of cellular chaperones and proteases. We have shown here that activity of this pathway is sensitively responsive to changes in the accuracy of protein synthesis that are triggered by either mutations in ribosomal proteins or exposure to antibiotics. Increasing the error rate during ribosomal decoding promoted competence, while reducing the error rate below the baseline level repressed the development of both spontaneous and antibiotic-induced competence. This pattern of regulation was promoted by the bacterial HtrA serine protease. Analysis of strains with the htrA (S234A) catalytic site mutation showed that the proteolytic activity of HtrA selectively repressed competence when translational fidelity was high but not when accuracy was low. These findings redefine the pneumococcal competence pathway as a response to errors during protein synthesis. This response has the capacity to address the immediate challenge of misfolded proteins through production of chaperones and proteases and may also be able to address, through genetic exchange, upstream coding errors that cause intrinsic protein folding defects. The competence pathway may thereby represent a strategy for dealing with lesions that impair proper protein coding and for maintaining the coding integrity of the genome. IMPORTANCE The signaling pathway that governs competence in the human respiratory tract pathogen Streptococcus pneumoniae regulates both genetic transformation and the production of cellular chaperones and proteases. The current study shows that this pathway is sensitively controlled in response to changes in the accuracy of protein synthesis. Increasing the error rate during ribosomal decoding induced competence, while decreasing the error rate repressed competence. This pattern of regulation was promoted by the HtrA protease, which selectively repressed competence when translational fidelity was high but not when accuracy was low. Our findings demonstrate that this organism is able to monitor the accuracy of information used for protein biosynthesis and suggest that errors trigger a response addressing both the immediate challenge of misfolded proteins and, through genetic exchange, upstream coding errors that may underlie protein folding defects. This pathway may represent an evolutionary strategy for maintaining the coding integrity of the genome.
format	article
author	Kathleen E. Stevens Diana Chang Erin E. Zwack Michael E. Sebert
author_facet	Kathleen E. Stevens Diana Chang Erin E. Zwack Michael E. Sebert
author_sort	Kathleen E. Stevens
title	Competence in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Is Regulated by the Rate of Ribosomal Decoding Errors
title_short	Competence in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Is Regulated by the Rate of Ribosomal Decoding Errors
title_full	Competence in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Is Regulated by the Rate of Ribosomal Decoding Errors
title_fullStr	Competence in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Is Regulated by the Rate of Ribosomal Decoding Errors
title_full_unstemmed	Competence in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Is Regulated by the Rate of Ribosomal Decoding Errors
title_sort	competence in <named-content content-type="genus-species">streptococcus pneumoniae</named-content> is regulated by the rate of ribosomal decoding errors
publisher	American Society for Microbiology
publishDate	2011
url	https://doaj.org/article/2dfc9b2d5e9c42e09be8d857f8539922
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Competence in <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Is Regulated by the Rate of Ribosomal Decoding Errors

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