Expression of a cryptic secondary sigma factor gene unveils natural competence for DNA transformation in Staphylococcus aureus.

It has long been a question whether Staphylococcus aureus, a major human pathogen, is able to develop natural competence for transformation by DNA. We previously showed that a novel staphylococcal secondary sigma factor, SigH, was a likely key component for competence development, but the correspond...

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Autores principales: Kazuya Morikawa, Aya J Takemura, Yumiko Inose, Melody Tsai, Le Thuy Nguyen Thi, Toshiko Ohta, Tarek Msadek
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Publicado: Public Library of Science (PLoS) 2012
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Acceso en línea:https://doaj.org/article/f4ca0375bb6947148941ab15ace826d7
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spelling oai:doaj.org-article:f4ca0375bb6947148941ab15ace826d72021-11-18T06:06:24ZExpression of a cryptic secondary sigma factor gene unveils natural competence for DNA transformation in Staphylococcus aureus.1553-73661553-737410.1371/journal.ppat.1003003https://doaj.org/article/f4ca0375bb6947148941ab15ace826d72012-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23133387/pdf/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374It has long been a question whether Staphylococcus aureus, a major human pathogen, is able to develop natural competence for transformation by DNA. We previously showed that a novel staphylococcal secondary sigma factor, SigH, was a likely key component for competence development, but the corresponding gene appeared to be cryptic as its expression could not be detected during growth under standard laboratory conditions. Here, we have uncovered two distinct mechanisms allowing activation of SigH production in a minor fraction of the bacterial cell population. The first is a chromosomal gene duplication rearrangement occurring spontaneously at a low frequency [≤10(-5)], generating expression of a new chimeric sigH gene. The second involves post-transcriptional regulation through an upstream inverted repeat sequence, effectively suppressing expression of the sigH gene. Importantly, we have demonstrated for the first time that S. aureus cells producing active SigH become competent for transformation by plasmid or chromosomal DNA, which requires the expression of SigH-controlled competence genes. Additionally, using DNA from the N315 MRSA strain, we successfully transferred the full length SCCmecII element through natural transformation to a methicillin-sensitive strain, conferring methicillin resistance to the resulting S. aureus transformants. Taken together, we propose a unique model for staphylococcal competence regulation by SigH that could help explain the acquisition of antibiotic resistance genes through horizontal gene transfer in this important pathogen.Kazuya MorikawaAya J TakemuraYumiko InoseMelody TsaiLe Thuy Nguyen ThiToshiko OhtaTarek MsadekPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 8, Iss 11, p e1003003 (2012)
institution DOAJ
collection DOAJ
language EN
topic Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
spellingShingle Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
Kazuya Morikawa
Aya J Takemura
Yumiko Inose
Melody Tsai
Le Thuy Nguyen Thi
Toshiko Ohta
Tarek Msadek
Expression of a cryptic secondary sigma factor gene unveils natural competence for DNA transformation in Staphylococcus aureus.
description It has long been a question whether Staphylococcus aureus, a major human pathogen, is able to develop natural competence for transformation by DNA. We previously showed that a novel staphylococcal secondary sigma factor, SigH, was a likely key component for competence development, but the corresponding gene appeared to be cryptic as its expression could not be detected during growth under standard laboratory conditions. Here, we have uncovered two distinct mechanisms allowing activation of SigH production in a minor fraction of the bacterial cell population. The first is a chromosomal gene duplication rearrangement occurring spontaneously at a low frequency [≤10(-5)], generating expression of a new chimeric sigH gene. The second involves post-transcriptional regulation through an upstream inverted repeat sequence, effectively suppressing expression of the sigH gene. Importantly, we have demonstrated for the first time that S. aureus cells producing active SigH become competent for transformation by plasmid or chromosomal DNA, which requires the expression of SigH-controlled competence genes. Additionally, using DNA from the N315 MRSA strain, we successfully transferred the full length SCCmecII element through natural transformation to a methicillin-sensitive strain, conferring methicillin resistance to the resulting S. aureus transformants. Taken together, we propose a unique model for staphylococcal competence regulation by SigH that could help explain the acquisition of antibiotic resistance genes through horizontal gene transfer in this important pathogen.
format article
author Kazuya Morikawa
Aya J Takemura
Yumiko Inose
Melody Tsai
Le Thuy Nguyen Thi
Toshiko Ohta
Tarek Msadek
author_facet Kazuya Morikawa
Aya J Takemura
Yumiko Inose
Melody Tsai
Le Thuy Nguyen Thi
Toshiko Ohta
Tarek Msadek
author_sort Kazuya Morikawa
title Expression of a cryptic secondary sigma factor gene unveils natural competence for DNA transformation in Staphylococcus aureus.
title_short Expression of a cryptic secondary sigma factor gene unveils natural competence for DNA transformation in Staphylococcus aureus.
title_full Expression of a cryptic secondary sigma factor gene unveils natural competence for DNA transformation in Staphylococcus aureus.
title_fullStr Expression of a cryptic secondary sigma factor gene unveils natural competence for DNA transformation in Staphylococcus aureus.
title_full_unstemmed Expression of a cryptic secondary sigma factor gene unveils natural competence for DNA transformation in Staphylococcus aureus.
title_sort expression of a cryptic secondary sigma factor gene unveils natural competence for dna transformation in staphylococcus aureus.
publisher Public Library of Science (PLoS)
publishDate 2012
url https://doaj.org/article/f4ca0375bb6947148941ab15ace826d7
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