<named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Contact-Dependent Growth Inhibition Plays Dual Role in Host-Pathogen Interactions

ABSTRACT Microorganisms exist in a diverse ecosystem and have evolved many different mechanisms for sensing and influencing the polymicrobial environment around them, utilizing both diffusible and contact-dependent signals. Contact-dependent growth inhibition (CDI) is one such communication system e...

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Autores principales:	Jeffrey A. Melvin, Jordan R. Gaston, Shawn N. Phillips, Michael J. Springer, Christopher W. Marshall, Robert M. Q. Shanks, Jennifer M. Bomberger
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	Pseudomonas aeruginosa contact-dependent growth inhibition toxin/antitoxin systems virulence determinants Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/665f0074282246ea9272cfe4007bc250
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spelling	oai:doaj.org-article:665f0074282246ea9272cfe4007bc2502021-11-15T15:21:53Z<named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Contact-Dependent Growth Inhibition Plays Dual Role in Host-Pathogen Interactions10.1128/mSphere.00336-172379-5042https://doaj.org/article/665f0074282246ea9272cfe4007bc2502017-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00336-17https://doaj.org/toc/2379-5042ABSTRACT Microorganisms exist in a diverse ecosystem and have evolved many different mechanisms for sensing and influencing the polymicrobial environment around them, utilizing both diffusible and contact-dependent signals. Contact-dependent growth inhibition (CDI) is one such communication system employed by Gram-negative bacteria. In addition to CDI mediation of growth inhibition, recent studies have demonstrated CDI-mediated control of communal behaviors such as biofilm formation. We postulated that CDI may therefore play an active role in host-pathogen interactions, allowing invading strains to establish themselves at polymicrobial mucosal interfaces through competitive interactions while simultaneously facilitating pathogenic capabilities via CDI-mediated signaling. Here, we show that Pseudomonas aeruginosa produces two CDI systems capable of mediating competition under conditions of growth on a surface or in liquid. Furthermore, we demonstrated a novel role for these systems in contributing to virulence in acute infection models, likely via posttranscriptional regulation of beneficial behaviors. While we did not observe any role for the P. aeruginosa CDI systems in biofilm biogenesis, we did identify for the first time robust CDI-mediated competition during interaction with a mammalian host using a model of chronic respiratory tract infection, as well as evidence that CDI expression is maintained in chronic lung infections. These findings reveal a previously unappreciated role for CDI in host-pathogen interactions and emphasize their importance during infection. IMPORTANCE How bacteria compete and communicate with each other is an increasingly recognized aspect of microbial pathogenesis with a major impact on disease outcomes. Gram-negative bacteria have recently been shown to employ a contact-dependent toxin-antitoxin system to achieve both competition and regulation of their physiology. Here, we show that this system is vital for virulence in acute infection as well as for establishment of chronic infection in the multidrug-resistant pathogen Pseudomonas aeruginosa. Greater understanding of the mechanisms underlying bacterial virulence and infection is important for the development of effective therapeutics in the era of increasing antimicrobial resistance.Jeffrey A. MelvinJordan R. GastonShawn N. PhillipsMichael J. SpringerChristopher W. MarshallRobert M. Q. ShanksJennifer M. BombergerAmerican Society for MicrobiologyarticlePseudomonas aeruginosacontact-dependent growth inhibitiontoxin/antitoxin systemsvirulence determinantsMicrobiologyQR1-502ENmSphere, Vol 2, Iss 6 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Pseudomonas aeruginosa contact-dependent growth inhibition toxin/antitoxin systems virulence determinants Microbiology QR1-502
spellingShingle	Pseudomonas aeruginosa contact-dependent growth inhibition toxin/antitoxin systems virulence determinants Microbiology QR1-502 Jeffrey A. Melvin Jordan R. Gaston Shawn N. Phillips Michael J. Springer Christopher W. Marshall Robert M. Q. Shanks Jennifer M. Bomberger <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Contact-Dependent Growth Inhibition Plays Dual Role in Host-Pathogen Interactions
description	ABSTRACT Microorganisms exist in a diverse ecosystem and have evolved many different mechanisms for sensing and influencing the polymicrobial environment around them, utilizing both diffusible and contact-dependent signals. Contact-dependent growth inhibition (CDI) is one such communication system employed by Gram-negative bacteria. In addition to CDI mediation of growth inhibition, recent studies have demonstrated CDI-mediated control of communal behaviors such as biofilm formation. We postulated that CDI may therefore play an active role in host-pathogen interactions, allowing invading strains to establish themselves at polymicrobial mucosal interfaces through competitive interactions while simultaneously facilitating pathogenic capabilities via CDI-mediated signaling. Here, we show that Pseudomonas aeruginosa produces two CDI systems capable of mediating competition under conditions of growth on a surface or in liquid. Furthermore, we demonstrated a novel role for these systems in contributing to virulence in acute infection models, likely via posttranscriptional regulation of beneficial behaviors. While we did not observe any role for the P. aeruginosa CDI systems in biofilm biogenesis, we did identify for the first time robust CDI-mediated competition during interaction with a mammalian host using a model of chronic respiratory tract infection, as well as evidence that CDI expression is maintained in chronic lung infections. These findings reveal a previously unappreciated role for CDI in host-pathogen interactions and emphasize their importance during infection. IMPORTANCE How bacteria compete and communicate with each other is an increasingly recognized aspect of microbial pathogenesis with a major impact on disease outcomes. Gram-negative bacteria have recently been shown to employ a contact-dependent toxin-antitoxin system to achieve both competition and regulation of their physiology. Here, we show that this system is vital for virulence in acute infection as well as for establishment of chronic infection in the multidrug-resistant pathogen Pseudomonas aeruginosa. Greater understanding of the mechanisms underlying bacterial virulence and infection is important for the development of effective therapeutics in the era of increasing antimicrobial resistance.
format	article
author	Jeffrey A. Melvin Jordan R. Gaston Shawn N. Phillips Michael J. Springer Christopher W. Marshall Robert M. Q. Shanks Jennifer M. Bomberger
author_facet	Jeffrey A. Melvin Jordan R. Gaston Shawn N. Phillips Michael J. Springer Christopher W. Marshall Robert M. Q. Shanks Jennifer M. Bomberger
author_sort	Jeffrey A. Melvin
title	<named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Contact-Dependent Growth Inhibition Plays Dual Role in Host-Pathogen Interactions
title_short	<named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Contact-Dependent Growth Inhibition Plays Dual Role in Host-Pathogen Interactions
title_full	<named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Contact-Dependent Growth Inhibition Plays Dual Role in Host-Pathogen Interactions
title_fullStr	<named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Contact-Dependent Growth Inhibition Plays Dual Role in Host-Pathogen Interactions
title_full_unstemmed	<named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Contact-Dependent Growth Inhibition Plays Dual Role in Host-Pathogen Interactions
title_sort	<named-content content-type="genus-species">pseudomonas aeruginosa</named-content> contact-dependent growth inhibition plays dual role in host-pathogen interactions
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/665f0074282246ea9272cfe4007bc250
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<named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Contact-Dependent Growth Inhibition Plays Dual Role in Host-Pathogen Interactions

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