Membrane Distribution of the <italic toggle="yes">Pseudomonas</italic> Quinolone Signal Modulates Outer Membrane Vesicle Production in <italic toggle="yes">Pseudomonas aeruginosa</italic>

ABSTRACT The Pseudomonas quinolone signal (PQS) is an important quorum-sensing molecule in Pseudomonas aeruginosa that also mediates its own packaging and transport by stimulating outer membrane vesicle (OMV) formation. Because OMVs have been implicated in many virulence-associated behaviors, it is...

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Autores principales:	Catalina Florez, Julie E. Raab, Adam C. Cooke, Jeffrey W. Schertzer
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	outer membrane vesicles PQS Pseudomonas aeruginosa quorum sensing secretion systems Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/276a83d8fe0f4287bd78bf167c6d2b50
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spelling	oai:doaj.org-article:276a83d8fe0f4287bd78bf167c6d2b502021-11-15T15:51:44ZMembrane Distribution of the <italic toggle="yes">Pseudomonas</italic> Quinolone Signal Modulates Outer Membrane Vesicle Production in <italic toggle="yes">Pseudomonas aeruginosa</italic>10.1128/mBio.01034-172150-7511https://doaj.org/article/276a83d8fe0f4287bd78bf167c6d2b502017-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01034-17https://doaj.org/toc/2150-7511ABSTRACT The Pseudomonas quinolone signal (PQS) is an important quorum-sensing molecule in Pseudomonas aeruginosa that also mediates its own packaging and transport by stimulating outer membrane vesicle (OMV) formation. Because OMVs have been implicated in many virulence-associated behaviors, it is critical that we understand how they are formed. Our group proposed the bilayer-couple model for OMV biogenesis, where PQS intercalates into the outer membrane, causing expansion of the outer leaflet and consequently inducing curvature. In accordance with the model, we hypothesized that PQS must be transported from the cytoplasm to the outer membrane before it can initiate OMV formation. We initially examined two laboratory strains of P. aeruginosa and found significant strain-dependent differences. PQS export correlated strongly with OMV production, even though equivalent amounts of total PQS were produced by both strains. Interestingly, we discovered that poor OMV producers sequestered the majority of PQS in the inner membrane, which appeared to be the result of early saturation of the export pathway. Further analysis showed that strain-specific PQS export and OMV biogenesis patterns were stable once established but could be significantly altered by changing the growth medium. Finally, we demonstrated that the associations described for laboratory strains also held for three clinical strains. These results suggest that factors controlling the export of PQS dictate OMV biogenesis. This work provides new insight into PQS-controlled virulence in P. aeruginosa and provides important tools to further study signal export and OMV biogenesis. IMPORTANCE Bacterial secretion has been recognized as an essential facet of microbial pathogenesis and human disease. Numerous virulence factors have been found to be transported within outer membrane vesicles (OMVs), and delivery using these biological nanoparticles often results in increased potency. OMV biogenesis is an important but poorly understood process that is ubiquitous among Gram-negative organisms. Our group seeks to understand the biochemical mechanisms behind the formation of OMVs and has developed a model of small-molecule-induced membrane curvature as an important driver of this process. With this work, we demonstrate that PQS, a known small-molecule OMV inducer, must be exported to promote OMV biogenesis in both lab-adapted and clinical strains of Pseudomonas aeruginosa. In supporting and expanding the bilayer-couple model of OMV biogenesis, the current work lays the groundwork for studying environmental and genetic factors that modulate OMV production and, consequently, the packaging and delivery of many bacterial factors.Catalina FlorezJulie E. RaabAdam C. CookeJeffrey W. SchertzerAmerican Society for Microbiologyarticleouter membrane vesiclesPQSPseudomonas aeruginosaquorum sensingsecretion systemsMicrobiologyQR1-502ENmBio, Vol 8, Iss 4 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	outer membrane vesicles PQS Pseudomonas aeruginosa quorum sensing secretion systems Microbiology QR1-502
spellingShingle	outer membrane vesicles PQS Pseudomonas aeruginosa quorum sensing secretion systems Microbiology QR1-502 Catalina Florez Julie E. Raab Adam C. Cooke Jeffrey W. Schertzer Membrane Distribution of the <italic toggle="yes">Pseudomonas</italic> Quinolone Signal Modulates Outer Membrane Vesicle Production in <italic toggle="yes">Pseudomonas aeruginosa</italic>
description	ABSTRACT The Pseudomonas quinolone signal (PQS) is an important quorum-sensing molecule in Pseudomonas aeruginosa that also mediates its own packaging and transport by stimulating outer membrane vesicle (OMV) formation. Because OMVs have been implicated in many virulence-associated behaviors, it is critical that we understand how they are formed. Our group proposed the bilayer-couple model for OMV biogenesis, where PQS intercalates into the outer membrane, causing expansion of the outer leaflet and consequently inducing curvature. In accordance with the model, we hypothesized that PQS must be transported from the cytoplasm to the outer membrane before it can initiate OMV formation. We initially examined two laboratory strains of P. aeruginosa and found significant strain-dependent differences. PQS export correlated strongly with OMV production, even though equivalent amounts of total PQS were produced by both strains. Interestingly, we discovered that poor OMV producers sequestered the majority of PQS in the inner membrane, which appeared to be the result of early saturation of the export pathway. Further analysis showed that strain-specific PQS export and OMV biogenesis patterns were stable once established but could be significantly altered by changing the growth medium. Finally, we demonstrated that the associations described for laboratory strains also held for three clinical strains. These results suggest that factors controlling the export of PQS dictate OMV biogenesis. This work provides new insight into PQS-controlled virulence in P. aeruginosa and provides important tools to further study signal export and OMV biogenesis. IMPORTANCE Bacterial secretion has been recognized as an essential facet of microbial pathogenesis and human disease. Numerous virulence factors have been found to be transported within outer membrane vesicles (OMVs), and delivery using these biological nanoparticles often results in increased potency. OMV biogenesis is an important but poorly understood process that is ubiquitous among Gram-negative organisms. Our group seeks to understand the biochemical mechanisms behind the formation of OMVs and has developed a model of small-molecule-induced membrane curvature as an important driver of this process. With this work, we demonstrate that PQS, a known small-molecule OMV inducer, must be exported to promote OMV biogenesis in both lab-adapted and clinical strains of Pseudomonas aeruginosa. In supporting and expanding the bilayer-couple model of OMV biogenesis, the current work lays the groundwork for studying environmental and genetic factors that modulate OMV production and, consequently, the packaging and delivery of many bacterial factors.
format	article
author	Catalina Florez Julie E. Raab Adam C. Cooke Jeffrey W. Schertzer
author_facet	Catalina Florez Julie E. Raab Adam C. Cooke Jeffrey W. Schertzer
author_sort	Catalina Florez
title	Membrane Distribution of the <italic toggle="yes">Pseudomonas</italic> Quinolone Signal Modulates Outer Membrane Vesicle Production in <italic toggle="yes">Pseudomonas aeruginosa</italic>
title_short	Membrane Distribution of the <italic toggle="yes">Pseudomonas</italic> Quinolone Signal Modulates Outer Membrane Vesicle Production in <italic toggle="yes">Pseudomonas aeruginosa</italic>
title_full	Membrane Distribution of the <italic toggle="yes">Pseudomonas</italic> Quinolone Signal Modulates Outer Membrane Vesicle Production in <italic toggle="yes">Pseudomonas aeruginosa</italic>
title_fullStr	Membrane Distribution of the <italic toggle="yes">Pseudomonas</italic> Quinolone Signal Modulates Outer Membrane Vesicle Production in <italic toggle="yes">Pseudomonas aeruginosa</italic>
title_full_unstemmed	Membrane Distribution of the <italic toggle="yes">Pseudomonas</italic> Quinolone Signal Modulates Outer Membrane Vesicle Production in <italic toggle="yes">Pseudomonas aeruginosa</italic>
title_sort	membrane distribution of the <italic toggle="yes">pseudomonas</italic> quinolone signal modulates outer membrane vesicle production in <italic toggle="yes">pseudomonas aeruginosa</italic>
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/276a83d8fe0f4287bd78bf167c6d2b50
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Membrane Distribution of the <italic toggle="yes">Pseudomonas</italic> Quinolone Signal Modulates Outer Membrane Vesicle Production in <italic toggle="yes">Pseudomonas aeruginosa</italic>

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