Cooperation and Cheating through a Secreted Aminopeptidase in the <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> RpoS Response

ABSTRACT The global stress response controlled by the alternative sigma factor RpoS protects enteric bacteria from a variety of environmental stressors. The role of RpoS in other, nonenteric bacteria, such as the opportunistic pathogen Pseudomonas aeruginosa, is less well understood. Here, we employ...

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Autores principales:	Tanner Robinson, Parker Smith, Erin R. Alberts, Mariana Colussi-Pelaez, Martin Schuster
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	stress response RpoS quorum sensing proteolysis Pseudomonas aeruginosa cooperation Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/9c7fc0c57b254091b277c84ece30336e
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spelling	oai:doaj.org-article:9c7fc0c57b254091b277c84ece30336e2021-11-15T15:57:02ZCooperation and Cheating through a Secreted Aminopeptidase in the <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> RpoS Response10.1128/mBio.03090-192150-7511https://doaj.org/article/9c7fc0c57b254091b277c84ece30336e2020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.03090-19https://doaj.org/toc/2150-7511ABSTRACT The global stress response controlled by the alternative sigma factor RpoS protects enteric bacteria from a variety of environmental stressors. The role of RpoS in other, nonenteric bacteria, such as the opportunistic pathogen Pseudomonas aeruginosa, is less well understood. Here, we employed experimental social evolution to reveal that cooperative behavior via secreted public goods is an important function in the RpoS response of P. aeruginosa. Using whole-genome sequencing, we identified rpoS loss-of-function mutants among isolates evolved in a protein growth medium that requires extracellular proteolysis. We found that rpoS mutants comprise up to 25% of the evolved population and that they behave as social cheaters, with low fitness in isolation but high fitness in mixed culture with the cooperating wild type. We conclude that rpoS mutants cheat because they exploit an RpoS-controlled public good produced by the wild type, the secreted aminopeptidase PaAP, and because they do not carry the metabolic costs of expressing PaAP and many other gene products in the large RpoS regulon. Our results suggest that PaAP is an integral part of a proteolytic sequence in P. aeruginosa that permits the utilization of protein as a nutrient source. Our work broadens the scope of stress response functions in bacteria. IMPORTANCE Bacterial stress responses are generally considered protective measures taken by individual cells. Enabled by an experimental evolution approach, we describe a contrasting property, collective nutrient acquisition, in the RpoS-dependent stress response of the opportunistic human pathogen P. aeruginosa. Specifically, we identify the secreted P. aeruginosa aminopeptidase (PaAP) as an essential RpoS-controlled function in extracellular proteolysis. As a secreted “public good,” PaAP permits cheating by rpoS mutants that save the metabolic costs of expressing RpoS-controlled genes dispensable under the given growth conditions. Proteolytic enzymes are important virulence factors in P. aeruginosa pathogenesis and constitute a potential target for antimicrobial therapy. More broadly, our work contributes to recent findings in higher organisms that stress affects not only individual fitness and competitiveness but also cooperative behavior.Tanner RobinsonParker SmithErin R. AlbertsMariana Colussi-PelaezMartin SchusterAmerican Society for Microbiologyarticlestress responseRpoSquorum sensingproteolysisPseudomonas aeruginosacooperationMicrobiologyQR1-502ENmBio, Vol 11, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	stress response RpoS quorum sensing proteolysis Pseudomonas aeruginosa cooperation Microbiology QR1-502
spellingShingle	stress response RpoS quorum sensing proteolysis Pseudomonas aeruginosa cooperation Microbiology QR1-502 Tanner Robinson Parker Smith Erin R. Alberts Mariana Colussi-Pelaez Martin Schuster Cooperation and Cheating through a Secreted Aminopeptidase in the <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> RpoS Response
description	ABSTRACT The global stress response controlled by the alternative sigma factor RpoS protects enteric bacteria from a variety of environmental stressors. The role of RpoS in other, nonenteric bacteria, such as the opportunistic pathogen Pseudomonas aeruginosa, is less well understood. Here, we employed experimental social evolution to reveal that cooperative behavior via secreted public goods is an important function in the RpoS response of P. aeruginosa. Using whole-genome sequencing, we identified rpoS loss-of-function mutants among isolates evolved in a protein growth medium that requires extracellular proteolysis. We found that rpoS mutants comprise up to 25% of the evolved population and that they behave as social cheaters, with low fitness in isolation but high fitness in mixed culture with the cooperating wild type. We conclude that rpoS mutants cheat because they exploit an RpoS-controlled public good produced by the wild type, the secreted aminopeptidase PaAP, and because they do not carry the metabolic costs of expressing PaAP and many other gene products in the large RpoS regulon. Our results suggest that PaAP is an integral part of a proteolytic sequence in P. aeruginosa that permits the utilization of protein as a nutrient source. Our work broadens the scope of stress response functions in bacteria. IMPORTANCE Bacterial stress responses are generally considered protective measures taken by individual cells. Enabled by an experimental evolution approach, we describe a contrasting property, collective nutrient acquisition, in the RpoS-dependent stress response of the opportunistic human pathogen P. aeruginosa. Specifically, we identify the secreted P. aeruginosa aminopeptidase (PaAP) as an essential RpoS-controlled function in extracellular proteolysis. As a secreted “public good,” PaAP permits cheating by rpoS mutants that save the metabolic costs of expressing RpoS-controlled genes dispensable under the given growth conditions. Proteolytic enzymes are important virulence factors in P. aeruginosa pathogenesis and constitute a potential target for antimicrobial therapy. More broadly, our work contributes to recent findings in higher organisms that stress affects not only individual fitness and competitiveness but also cooperative behavior.
format	article
author	Tanner Robinson Parker Smith Erin R. Alberts Mariana Colussi-Pelaez Martin Schuster
author_facet	Tanner Robinson Parker Smith Erin R. Alberts Mariana Colussi-Pelaez Martin Schuster
author_sort	Tanner Robinson
title	Cooperation and Cheating through a Secreted Aminopeptidase in the <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> RpoS Response
title_short	Cooperation and Cheating through a Secreted Aminopeptidase in the <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> RpoS Response
title_full	Cooperation and Cheating through a Secreted Aminopeptidase in the <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> RpoS Response
title_fullStr	Cooperation and Cheating through a Secreted Aminopeptidase in the <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> RpoS Response
title_full_unstemmed	Cooperation and Cheating through a Secreted Aminopeptidase in the <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> RpoS Response
title_sort	cooperation and cheating through a secreted aminopeptidase in the <named-content content-type="genus-species">pseudomonas aeruginosa</named-content> rpos response
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/9c7fc0c57b254091b277c84ece30336e
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Cooperation and Cheating through a Secreted Aminopeptidase in the <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> RpoS Response

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