A Hierarchical Cascade of Second Messengers Regulates <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Surface Behaviors

ABSTRACT Biofilms are surface-attached multicellular communities. Using single-cell tracking microscopy, we showed that a pilY1 mutant of Pseudomonas aeruginosa is defective in early biofilm formation. We leveraged the observation that PilY1 protein levels increase on a surface to perform a genetic...

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Autores principales:	Yun Luo, Kun Zhao, Amy E. Baker, Sherry L. Kuchma, Kimberly A. Coggan, Matthew C. Wolfgang, Gerard C. L. Wong, George A. O’Toole
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/be6bd3d3d44c4a6bb7990dda35c5e3af
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spelling	oai:doaj.org-article:be6bd3d3d44c4a6bb7990dda35c5e3af2021-11-15T15:41:19ZA Hierarchical Cascade of Second Messengers Regulates <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Surface Behaviors10.1128/mBio.02456-142150-7511https://doaj.org/article/be6bd3d3d44c4a6bb7990dda35c5e3af2015-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02456-14https://doaj.org/toc/2150-7511ABSTRACT Biofilms are surface-attached multicellular communities. Using single-cell tracking microscopy, we showed that a pilY1 mutant of Pseudomonas aeruginosa is defective in early biofilm formation. We leveraged the observation that PilY1 protein levels increase on a surface to perform a genetic screen to identify mutants altered in surface-grown expression of this protein. Based on our genetic studies, we found that soon after initiating surface growth, cyclic AMP (cAMP) levels increase, dependent on PilJ, a chemoreceptor-like protein of the Pil-Chp complex, and the type IV pilus (TFP). cAMP and its receptor protein Vfr, together with the FimS-AlgR two-component system (TCS), upregulate the expression of PilY1 upon surface growth. FimS and PilJ interact, suggesting a mechanism by which Pil-Chp can regulate FimS function. The subsequent secretion of PilY1 is dependent on the TFP assembly system; thus, PilY1 is not deployed until the pilus is assembled, allowing an ordered signaling cascade. Cell surface-associated PilY1 in turn signals through the TFP alignment complex PilMNOP and the diguanylate cyclase SadC to activate downstream cyclic di-GMP (c-di-GMP) production, thereby repressing swarming motility. Overall, our data support a model whereby P. aeruginosa senses the surface through the Pil-Chp chemotaxis-like complex, TFP, and PilY1 to regulate cAMP and c-di-GMP production, thereby employing a hierarchical regulatory cascade of second messengers to coordinate its program of surface behaviors. IMPORTANCE Biofilms are surface-attached multicellular communities. Here, we show that a stepwise regulatory circuit, involving ordered signaling via two different second messengers, is required for Pseudomonas aeruginosa to control early events in cell-surface interactions. We propose that our studies have uncovered a multilayered “surface-sensing” system that allows P. aeruginosa to effectively coordinate its surface-associated behaviors. Understanding how cells transition into the biofilm state on a surface may provide new approaches to prevent formation of these communities.Yun LuoKun ZhaoAmy E. BakerSherry L. KuchmaKimberly A. CogganMatthew C. WolfgangGerard C. L. WongGeorge A. O’TooleAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 1 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Yun Luo Kun Zhao Amy E. Baker Sherry L. Kuchma Kimberly A. Coggan Matthew C. Wolfgang Gerard C. L. Wong George A. O’Toole A Hierarchical Cascade of Second Messengers Regulates <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Surface Behaviors
description	ABSTRACT Biofilms are surface-attached multicellular communities. Using single-cell tracking microscopy, we showed that a pilY1 mutant of Pseudomonas aeruginosa is defective in early biofilm formation. We leveraged the observation that PilY1 protein levels increase on a surface to perform a genetic screen to identify mutants altered in surface-grown expression of this protein. Based on our genetic studies, we found that soon after initiating surface growth, cyclic AMP (cAMP) levels increase, dependent on PilJ, a chemoreceptor-like protein of the Pil-Chp complex, and the type IV pilus (TFP). cAMP and its receptor protein Vfr, together with the FimS-AlgR two-component system (TCS), upregulate the expression of PilY1 upon surface growth. FimS and PilJ interact, suggesting a mechanism by which Pil-Chp can regulate FimS function. The subsequent secretion of PilY1 is dependent on the TFP assembly system; thus, PilY1 is not deployed until the pilus is assembled, allowing an ordered signaling cascade. Cell surface-associated PilY1 in turn signals through the TFP alignment complex PilMNOP and the diguanylate cyclase SadC to activate downstream cyclic di-GMP (c-di-GMP) production, thereby repressing swarming motility. Overall, our data support a model whereby P. aeruginosa senses the surface through the Pil-Chp chemotaxis-like complex, TFP, and PilY1 to regulate cAMP and c-di-GMP production, thereby employing a hierarchical regulatory cascade of second messengers to coordinate its program of surface behaviors. IMPORTANCE Biofilms are surface-attached multicellular communities. Here, we show that a stepwise regulatory circuit, involving ordered signaling via two different second messengers, is required for Pseudomonas aeruginosa to control early events in cell-surface interactions. We propose that our studies have uncovered a multilayered “surface-sensing” system that allows P. aeruginosa to effectively coordinate its surface-associated behaviors. Understanding how cells transition into the biofilm state on a surface may provide new approaches to prevent formation of these communities.
format	article
author	Yun Luo Kun Zhao Amy E. Baker Sherry L. Kuchma Kimberly A. Coggan Matthew C. Wolfgang Gerard C. L. Wong George A. O’Toole
author_facet	Yun Luo Kun Zhao Amy E. Baker Sherry L. Kuchma Kimberly A. Coggan Matthew C. Wolfgang Gerard C. L. Wong George A. O’Toole
author_sort	Yun Luo
title	A Hierarchical Cascade of Second Messengers Regulates <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Surface Behaviors
title_short	A Hierarchical Cascade of Second Messengers Regulates <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Surface Behaviors
title_full	A Hierarchical Cascade of Second Messengers Regulates <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Surface Behaviors
title_fullStr	A Hierarchical Cascade of Second Messengers Regulates <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Surface Behaviors
title_full_unstemmed	A Hierarchical Cascade of Second Messengers Regulates <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Surface Behaviors
title_sort	hierarchical cascade of second messengers regulates <named-content content-type="genus-species">pseudomonas aeruginosa</named-content> surface behaviors
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/be6bd3d3d44c4a6bb7990dda35c5e3af
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A Hierarchical Cascade of Second Messengers Regulates <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Surface Behaviors

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