The <italic toggle="yes">Pseudomonas aeruginosa</italic> Orphan Quorum Sensing Signal Receptor QscR Regulates Global Quorum Sensing Gene Expression by Activating a Single Linked Operon

ABSTRACT Pseudomonas aeruginosa uses two acyl-homoserine lactone signals and two quorum sensing (QS) transcription factors, LasR and RhlR, to activate dozens of genes. LasR responds to N-3-oxo-dodecanoyl-homoserine lactone (3OC12-HSL) and RhlR to N-butanoyl-homoserine lactone (C4-HSL). There is a th...

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Autores principales: Fengming Ding, Ken-Ichi Oinuma, Nicole E. Smalley, Amy L. Schaefer, Omar Hamwy, E. Peter Greenberg, Ajai A. Dandekar
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:f016d0f86c5649e79c71d6012e0b0a2a2021-11-15T16:00:16ZThe <italic toggle="yes">Pseudomonas aeruginosa</italic> Orphan Quorum Sensing Signal Receptor QscR Regulates Global Quorum Sensing Gene Expression by Activating a Single Linked Operon10.1128/mBio.01274-182150-7511https://doaj.org/article/f016d0f86c5649e79c71d6012e0b0a2a2018-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01274-18https://doaj.org/toc/2150-7511ABSTRACT Pseudomonas aeruginosa uses two acyl-homoserine lactone signals and two quorum sensing (QS) transcription factors, LasR and RhlR, to activate dozens of genes. LasR responds to N-3-oxo-dodecanoyl-homoserine lactone (3OC12-HSL) and RhlR to N-butanoyl-homoserine lactone (C4-HSL). There is a third P. aeruginosa acyl-homoserine-lactone-responsive transcription factor, QscR, which acts to dampen or delay activation of genes by LasR and RhlR by an unknown mechanism. To better understand the role of QscR in P. aeruginosa QS, we performed a chromatin immunoprecipitation analysis, which showed this transcription factor bound the promoter of only a single operon of three genes linked to qscR, PA1895 to PA1897. Other genes that appear to be regulated by QscR in transcriptome studies were not direct targets of QscR. Deletion of PA1897 recapitulates the early QS activation phenotype of a QscR-null mutant, and the phenotype of a QscR-null mutant was complemented by PA1895-1897 but not by PA1897 alone. We conclude that QscR acts to modulate quorum sensing through regulation of a single operon, apparently raising the QS threshold of the population and providing a “brake” on QS autoinduction. IMPORTANCE Quorum sensing, a cell-cell communication system, is broadly distributed among bacteria and is commonly used to regulate the production of shared products. An important consequence of quorum sensing is a delay in production of certain products until the population density is high. The bacterium Pseudomonas aeruginosa has a particularly complicated quorum sensing system involving multiple signals and receptors. One of these receptors, QscR, downregulates gene expression, unlike the other receptors in P. aeruginosa. QscR does so by inducing the expression of a single operon whose function provides an element of resistance to a population reaching a quorum. This finding has importance for design of quorum sensing inhibitory strategies and can also inform design of synthetic biological circuits that use quorum sensing receptors to regulate gene expression.Fengming DingKen-Ichi OinumaNicole E. SmalleyAmy L. SchaeferOmar HamwyE. Peter GreenbergAjai A. DandekarAmerican Society for Microbiologyarticleacyl-homoserine lactoneantiactivationsociomicrobiologyMicrobiologyQR1-502ENmBio, Vol 9, Iss 4 (2018)
institution DOAJ
collection DOAJ
language EN
topic acyl-homoserine lactone
antiactivation
sociomicrobiology
Microbiology
QR1-502
spellingShingle acyl-homoserine lactone
antiactivation
sociomicrobiology
Microbiology
QR1-502
Fengming Ding
Ken-Ichi Oinuma
Nicole E. Smalley
Amy L. Schaefer
Omar Hamwy
E. Peter Greenberg
Ajai A. Dandekar
The <italic toggle="yes">Pseudomonas aeruginosa</italic> Orphan Quorum Sensing Signal Receptor QscR Regulates Global Quorum Sensing Gene Expression by Activating a Single Linked Operon
description ABSTRACT Pseudomonas aeruginosa uses two acyl-homoserine lactone signals and two quorum sensing (QS) transcription factors, LasR and RhlR, to activate dozens of genes. LasR responds to N-3-oxo-dodecanoyl-homoserine lactone (3OC12-HSL) and RhlR to N-butanoyl-homoserine lactone (C4-HSL). There is a third P. aeruginosa acyl-homoserine-lactone-responsive transcription factor, QscR, which acts to dampen or delay activation of genes by LasR and RhlR by an unknown mechanism. To better understand the role of QscR in P. aeruginosa QS, we performed a chromatin immunoprecipitation analysis, which showed this transcription factor bound the promoter of only a single operon of three genes linked to qscR, PA1895 to PA1897. Other genes that appear to be regulated by QscR in transcriptome studies were not direct targets of QscR. Deletion of PA1897 recapitulates the early QS activation phenotype of a QscR-null mutant, and the phenotype of a QscR-null mutant was complemented by PA1895-1897 but not by PA1897 alone. We conclude that QscR acts to modulate quorum sensing through regulation of a single operon, apparently raising the QS threshold of the population and providing a “brake” on QS autoinduction. IMPORTANCE Quorum sensing, a cell-cell communication system, is broadly distributed among bacteria and is commonly used to regulate the production of shared products. An important consequence of quorum sensing is a delay in production of certain products until the population density is high. The bacterium Pseudomonas aeruginosa has a particularly complicated quorum sensing system involving multiple signals and receptors. One of these receptors, QscR, downregulates gene expression, unlike the other receptors in P. aeruginosa. QscR does so by inducing the expression of a single operon whose function provides an element of resistance to a population reaching a quorum. This finding has importance for design of quorum sensing inhibitory strategies and can also inform design of synthetic biological circuits that use quorum sensing receptors to regulate gene expression.
format article
author Fengming Ding
Ken-Ichi Oinuma
Nicole E. Smalley
Amy L. Schaefer
Omar Hamwy
E. Peter Greenberg
Ajai A. Dandekar
author_facet Fengming Ding
Ken-Ichi Oinuma
Nicole E. Smalley
Amy L. Schaefer
Omar Hamwy
E. Peter Greenberg
Ajai A. Dandekar
author_sort Fengming Ding
title The <italic toggle="yes">Pseudomonas aeruginosa</italic> Orphan Quorum Sensing Signal Receptor QscR Regulates Global Quorum Sensing Gene Expression by Activating a Single Linked Operon
title_short The <italic toggle="yes">Pseudomonas aeruginosa</italic> Orphan Quorum Sensing Signal Receptor QscR Regulates Global Quorum Sensing Gene Expression by Activating a Single Linked Operon
title_full The <italic toggle="yes">Pseudomonas aeruginosa</italic> Orphan Quorum Sensing Signal Receptor QscR Regulates Global Quorum Sensing Gene Expression by Activating a Single Linked Operon
title_fullStr The <italic toggle="yes">Pseudomonas aeruginosa</italic> Orphan Quorum Sensing Signal Receptor QscR Regulates Global Quorum Sensing Gene Expression by Activating a Single Linked Operon
title_full_unstemmed The <italic toggle="yes">Pseudomonas aeruginosa</italic> Orphan Quorum Sensing Signal Receptor QscR Regulates Global Quorum Sensing Gene Expression by Activating a Single Linked Operon
title_sort <italic toggle="yes">pseudomonas aeruginosa</italic> orphan quorum sensing signal receptor qscr regulates global quorum sensing gene expression by activating a single linked operon
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/f016d0f86c5649e79c71d6012e0b0a2a
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