A <italic toggle="yes">rhlI</italic> 5′ UTR-Derived sRNA Regulates RhlR-Dependent Quorum Sensing in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>

ABSTRACT N-Acyl homoserine lactone (AHL) quorum sensing (QS) controls expression of over 200 genes in Pseudomonas aeruginosa. There are two AHL regulatory systems: the LasR-LasI circuit and the RhlR-RhlI system. We mapped transcription termination sites affected by AHL QS in P. aeruginosa, and in do...

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Autores principales: Maureen K. Thomason, Maya Voichek, Daniel Dar, Victoria Addis, David Fitzgerald, Susan Gottesman, Rotem Sorek, E. Peter Greenberg
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Publicado: American Society for Microbiology 2019
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spelling oai:doaj.org-article:e0f5909112bb4c20a576f27cc43373562021-11-15T15:59:42ZA <italic toggle="yes">rhlI</italic> 5′ UTR-Derived sRNA Regulates RhlR-Dependent Quorum Sensing in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>10.1128/mBio.02253-192150-7511https://doaj.org/article/e0f5909112bb4c20a576f27cc43373562019-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02253-19https://doaj.org/toc/2150-7511ABSTRACT N-Acyl homoserine lactone (AHL) quorum sensing (QS) controls expression of over 200 genes in Pseudomonas aeruginosa. There are two AHL regulatory systems: the LasR-LasI circuit and the RhlR-RhlI system. We mapped transcription termination sites affected by AHL QS in P. aeruginosa, and in doing so we identified AHL-regulated small RNAs (sRNAs). Of interest, we noted that one particular sRNA was located within the rhlI locus. We found that rhlI, which encodes the enzyme that produces the AHL N-butanoyl-homoserine lactone (C4-HSL), is controlled by a 5′ untranslated region (UTR)-derived sRNA we name RhlS. We also identified an antisense RNA encoded opposite the beginning of the rhlI open reading frame, which we name asRhlS. RhlS accumulates as wild-type cells enter stationary phase and is required for the production of normal levels of C4-HSL through activation of rhlI translation. RhlS also directly posttranscriptionally regulates at least one other unlinked gene, fpvA. The asRhlS appears to be expressed at maximal levels during logarithmic growth, and we suggest RhlS may act antagonistically to the asRhlS to regulate rhlI translation. The rhlI-encoded sRNAs represent a novel aspect of RNA-mediated tuning of P. aeruginosa QS. IMPORTANCE The opportunistic human pathogen Pseudomonas aeruginosa possesses multiple quorum sensing systems that regulate and coordinate production of virulence factors and adaptation to different environments. Despite extensive research, the regulatory elements that play a role in this complex network are still not fully understood. By using several RNA sequencing techniques, we were able to identify a small regulatory RNA we named RhlS. RhlS increases translation of RhlI, a key enzyme in the quorum sensing pathway, and represses the fpvA mRNA encoding one of the siderophore pyoverdine receptors. Our results highlight a new regulatory layer of P. aeruginosa quorum sensing and contribute to the growing understanding of the role regulatory RNAs play in bacterial physiology.Maureen K. ThomasonMaya VoichekDaniel DarVictoria AddisDavid FitzgeraldSusan GottesmanRotem SorekE. Peter GreenbergAmerican Society for Microbiologyarticleterm-seqtranscriptomesmall RNAHfqpyoverdineMicrobiologyQR1-502ENmBio, Vol 10, Iss 5 (2019)
institution DOAJ
collection DOAJ
language EN
topic term-seq
transcriptome
small RNA
Hfq
pyoverdine
Microbiology
QR1-502
spellingShingle term-seq
transcriptome
small RNA
Hfq
pyoverdine
Microbiology
QR1-502
Maureen K. Thomason
Maya Voichek
Daniel Dar
Victoria Addis
David Fitzgerald
Susan Gottesman
Rotem Sorek
E. Peter Greenberg
A <italic toggle="yes">rhlI</italic> 5′ UTR-Derived sRNA Regulates RhlR-Dependent Quorum Sensing in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
description ABSTRACT N-Acyl homoserine lactone (AHL) quorum sensing (QS) controls expression of over 200 genes in Pseudomonas aeruginosa. There are two AHL regulatory systems: the LasR-LasI circuit and the RhlR-RhlI system. We mapped transcription termination sites affected by AHL QS in P. aeruginosa, and in doing so we identified AHL-regulated small RNAs (sRNAs). Of interest, we noted that one particular sRNA was located within the rhlI locus. We found that rhlI, which encodes the enzyme that produces the AHL N-butanoyl-homoserine lactone (C4-HSL), is controlled by a 5′ untranslated region (UTR)-derived sRNA we name RhlS. We also identified an antisense RNA encoded opposite the beginning of the rhlI open reading frame, which we name asRhlS. RhlS accumulates as wild-type cells enter stationary phase and is required for the production of normal levels of C4-HSL through activation of rhlI translation. RhlS also directly posttranscriptionally regulates at least one other unlinked gene, fpvA. The asRhlS appears to be expressed at maximal levels during logarithmic growth, and we suggest RhlS may act antagonistically to the asRhlS to regulate rhlI translation. The rhlI-encoded sRNAs represent a novel aspect of RNA-mediated tuning of P. aeruginosa QS. IMPORTANCE The opportunistic human pathogen Pseudomonas aeruginosa possesses multiple quorum sensing systems that regulate and coordinate production of virulence factors and adaptation to different environments. Despite extensive research, the regulatory elements that play a role in this complex network are still not fully understood. By using several RNA sequencing techniques, we were able to identify a small regulatory RNA we named RhlS. RhlS increases translation of RhlI, a key enzyme in the quorum sensing pathway, and represses the fpvA mRNA encoding one of the siderophore pyoverdine receptors. Our results highlight a new regulatory layer of P. aeruginosa quorum sensing and contribute to the growing understanding of the role regulatory RNAs play in bacterial physiology.
format article
author Maureen K. Thomason
Maya Voichek
Daniel Dar
Victoria Addis
David Fitzgerald
Susan Gottesman
Rotem Sorek
E. Peter Greenberg
author_facet Maureen K. Thomason
Maya Voichek
Daniel Dar
Victoria Addis
David Fitzgerald
Susan Gottesman
Rotem Sorek
E. Peter Greenberg
author_sort Maureen K. Thomason
title A <italic toggle="yes">rhlI</italic> 5′ UTR-Derived sRNA Regulates RhlR-Dependent Quorum Sensing in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
title_short A <italic toggle="yes">rhlI</italic> 5′ UTR-Derived sRNA Regulates RhlR-Dependent Quorum Sensing in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
title_full A <italic toggle="yes">rhlI</italic> 5′ UTR-Derived sRNA Regulates RhlR-Dependent Quorum Sensing in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
title_fullStr A <italic toggle="yes">rhlI</italic> 5′ UTR-Derived sRNA Regulates RhlR-Dependent Quorum Sensing in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
title_full_unstemmed A <italic toggle="yes">rhlI</italic> 5′ UTR-Derived sRNA Regulates RhlR-Dependent Quorum Sensing in <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content>
title_sort <italic toggle="yes">rhli</italic> 5′ utr-derived srna regulates rhlr-dependent quorum sensing in <named-content content-type="genus-species">pseudomonas aeruginosa</named-content>
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/e0f5909112bb4c20a576f27cc4337356
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