The <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> PilSR Two-Component System Regulates Both Twitching and Swimming Motilities

ABSTRACT Motility is an important virulence trait for many bacterial pathogens, allowing them to position themselves in appropriate locations at appropriate times. The motility structures type IV pili and flagella are also involved in sensing surface contact, which modulates pathogenicity. In Pseudo...

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Autores principales:	Sara L. N. Kilmury, Lori L. Burrows
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	cell surface cystic fibrosis flagellar gene regulation two-component regulatory systems type IV pili Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/927caeb4c6384a5397ecb381df511209
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spelling	oai:doaj.org-article:927caeb4c6384a5397ecb381df5112092021-11-15T16:00:16ZThe <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> PilSR Two-Component System Regulates Both Twitching and Swimming Motilities10.1128/mBio.01310-182150-7511https://doaj.org/article/927caeb4c6384a5397ecb381df5112092018-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01310-18https://doaj.org/toc/2150-7511ABSTRACT Motility is an important virulence trait for many bacterial pathogens, allowing them to position themselves in appropriate locations at appropriate times. The motility structures type IV pili and flagella are also involved in sensing surface contact, which modulates pathogenicity. In Pseudomonas aeruginosa, the PilS-PilR two-component system (TCS) regulates expression of the type IV pilus (T4P) major subunit PilA, while biosynthesis of the single polar flagellum is regulated by a hierarchical system that includes the FleSR TCS. Previous studies of Geobacter sulfurreducens and Dichelobacter nodosus implicated PilR in regulation of non-T4P-related genes, including some involved in flagellar biosynthesis. Here we used transcriptome sequencing (RNA-seq) analysis to identify genes in addition to pilA with changes in expression in the absence of pilR. Among the genes identified were 10 genes whose transcription increased in the pilA mutant but decreased in the pilR mutant, despite both mutants lacking T4P and pilus-related phenotypes. The products of these inversely dysregulated genes, many of which were hypothetical, may be important for virulence and surface-associated behaviors, as mutants had altered swarming motility, biofilm formation, type VI secretion system expression, and pathogenicity in a nematode model. Further, the PilSR TCS positively regulated transcription of fleSR, and thus many genes in the FleSR regulon. As a result, pilSR deletion mutants had defects in swimming motility that were independent of the loss of PilA. Together, these data suggest that in addition to controlling T4P expression, PilSR could have a broader role in the regulation of P. aeruginosa motility and surface sensing behaviors. IMPORTANCE Surface appendages such as type IV pili and flagella are important for establishing surface attachment and infection in a host in response to appropriate cues. The PilSR regulatory system that controls type IV pilus expression in Pseudomonas aeruginosa has an established role in expression of the major pilin PilA. Here we provide evidence supporting a new role for PilSR in regulating flagellum-dependent swimming motility in addition to pilus-dependent twitching motility. Further, even though both pilA and pilR mutants lack PilA and pili, we identified sets of genes downregulated in the pilR mutant and upregulated in a pilA mutant as well as genes downregulated only in a pilR mutant, independent of pilus expression. This finding suggests that change in the inner membrane levels of PilA is only one of the cues to which PilR responds to modulate gene expression. Identification of PilR as a regulator of multiple motility pathways may make it an interesting therapeutic target for antivirulence compounds.Sara L. N. KilmuryLori L. BurrowsAmerican Society for Microbiologyarticlecell surfacecystic fibrosisflagellar gene regulationtwo-component regulatory systemstype IV piliMicrobiologyQR1-502ENmBio, Vol 9, Iss 4 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	cell surface cystic fibrosis flagellar gene regulation two-component regulatory systems type IV pili Microbiology QR1-502
spellingShingle	cell surface cystic fibrosis flagellar gene regulation two-component regulatory systems type IV pili Microbiology QR1-502 Sara L. N. Kilmury Lori L. Burrows The <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> PilSR Two-Component System Regulates Both Twitching and Swimming Motilities
description	ABSTRACT Motility is an important virulence trait for many bacterial pathogens, allowing them to position themselves in appropriate locations at appropriate times. The motility structures type IV pili and flagella are also involved in sensing surface contact, which modulates pathogenicity. In Pseudomonas aeruginosa, the PilS-PilR two-component system (TCS) regulates expression of the type IV pilus (T4P) major subunit PilA, while biosynthesis of the single polar flagellum is regulated by a hierarchical system that includes the FleSR TCS. Previous studies of Geobacter sulfurreducens and Dichelobacter nodosus implicated PilR in regulation of non-T4P-related genes, including some involved in flagellar biosynthesis. Here we used transcriptome sequencing (RNA-seq) analysis to identify genes in addition to pilA with changes in expression in the absence of pilR. Among the genes identified were 10 genes whose transcription increased in the pilA mutant but decreased in the pilR mutant, despite both mutants lacking T4P and pilus-related phenotypes. The products of these inversely dysregulated genes, many of which were hypothetical, may be important for virulence and surface-associated behaviors, as mutants had altered swarming motility, biofilm formation, type VI secretion system expression, and pathogenicity in a nematode model. Further, the PilSR TCS positively regulated transcription of fleSR, and thus many genes in the FleSR regulon. As a result, pilSR deletion mutants had defects in swimming motility that were independent of the loss of PilA. Together, these data suggest that in addition to controlling T4P expression, PilSR could have a broader role in the regulation of P. aeruginosa motility and surface sensing behaviors. IMPORTANCE Surface appendages such as type IV pili and flagella are important for establishing surface attachment and infection in a host in response to appropriate cues. The PilSR regulatory system that controls type IV pilus expression in Pseudomonas aeruginosa has an established role in expression of the major pilin PilA. Here we provide evidence supporting a new role for PilSR in regulating flagellum-dependent swimming motility in addition to pilus-dependent twitching motility. Further, even though both pilA and pilR mutants lack PilA and pili, we identified sets of genes downregulated in the pilR mutant and upregulated in a pilA mutant as well as genes downregulated only in a pilR mutant, independent of pilus expression. This finding suggests that change in the inner membrane levels of PilA is only one of the cues to which PilR responds to modulate gene expression. Identification of PilR as a regulator of multiple motility pathways may make it an interesting therapeutic target for antivirulence compounds.
format	article
author	Sara L. N. Kilmury Lori L. Burrows
author_facet	Sara L. N. Kilmury Lori L. Burrows
author_sort	Sara L. N. Kilmury
title	The <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> PilSR Two-Component System Regulates Both Twitching and Swimming Motilities
title_short	The <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> PilSR Two-Component System Regulates Both Twitching and Swimming Motilities
title_full	The <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> PilSR Two-Component System Regulates Both Twitching and Swimming Motilities
title_fullStr	The <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> PilSR Two-Component System Regulates Both Twitching and Swimming Motilities
title_full_unstemmed	The <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> PilSR Two-Component System Regulates Both Twitching and Swimming Motilities
title_sort	<named-content content-type="genus-species">pseudomonas aeruginosa</named-content> pilsr two-component system regulates both twitching and swimming motilities
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/927caeb4c6384a5397ecb381df511209
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The <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> PilSR Two-Component System Regulates Both Twitching and Swimming Motilities

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