The Fitness of <italic toggle="yes">Pseudomonas aeruginosa</italic> Quorum Sensing Signal Cheats Is Influenced by the Diffusivity of the Environment

ABSTRACT Experiments examining the social dynamics of bacterial quorum sensing (QS) have focused on mutants which do not respond to signals and the role of QS-regulated exoproducts as public goods. The potential for QS signal molecules to themselves be social public goods has received much less atte...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Anne Mund, Stephen P. Diggle, Freya Harrison
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	Pseudomonas aeruginosa evolution infectious disease microbial ecology opportunistic infections quorum sensing Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/2751d466b36f4696ab61ce8416133b11
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:2751d466b36f4696ab61ce8416133b11
record_format	dspace
spelling	oai:doaj.org-article:2751d466b36f4696ab61ce8416133b112021-11-15T15:51:28ZThe Fitness of <italic toggle="yes">Pseudomonas aeruginosa</italic> Quorum Sensing Signal Cheats Is Influenced by the Diffusivity of the Environment10.1128/mBio.00353-172150-7511https://doaj.org/article/2751d466b36f4696ab61ce8416133b112017-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00353-17https://doaj.org/toc/2150-7511ABSTRACT Experiments examining the social dynamics of bacterial quorum sensing (QS) have focused on mutants which do not respond to signals and the role of QS-regulated exoproducts as public goods. The potential for QS signal molecules to themselves be social public goods has received much less attention. Here, we analyze how signal-deficient (lasI) mutants of the opportunistic pathogen Pseudomonas aeruginosa interact with wild-type cells in an environment where QS is required for growth. We show that when growth requires a “private” intracellular metabolic mechanism activated by the presence of QS signal, lasI mutants act as social cheats and outcompete signal-producing wild-type bacteria in mixed cultures, because they can exploit the signals produced by wild-type cells. However, reducing the ability of signal molecules to diffuse through the growth medium results in signal molecules becoming less accessible to mutants, leading to reduced cheating. Our results indicate that QS signal molecules can be considered social public goods in a way that has been previously described for other exoproducts but that spatial structuring of populations reduces exploitation by noncooperative signal cheats. IMPORTANCE Bacteria communicate via signaling molecules to regulate the expression of a whole range of genes. This process, termed quorum sensing (QS), moderates bacterial metabolism under many environmental conditions, from soil and water (where QS-regulated genes influence nutrient cycling) to animal hosts (where QS-regulated genes determine pathogen virulence). Understanding the ecology of QS could therefore yield vital clues to how we might modify bacterial behavior for environmental or clinical gains. Here, we demonstrate that QS signals act as shareable public goods. This means that their evolution, and therefore population-level responses to interference with QS, will be constrained by population structure. Further, we show that environmental structure (constraints on signal diffusion) alters the accessibility of QS signals and demonstrates that we need to consider population and environmental structure to help us further our understanding of QS signaling systems.Anne MundStephen P. DiggleFreya HarrisonAmerican Society for MicrobiologyarticlePseudomonas aeruginosaevolutioninfectious diseasemicrobial ecologyopportunistic infectionsquorum sensingMicrobiologyQR1-502ENmBio, Vol 8, Iss 3 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Pseudomonas aeruginosa evolution infectious disease microbial ecology opportunistic infections quorum sensing Microbiology QR1-502
spellingShingle	Pseudomonas aeruginosa evolution infectious disease microbial ecology opportunistic infections quorum sensing Microbiology QR1-502 Anne Mund Stephen P. Diggle Freya Harrison The Fitness of <italic toggle="yes">Pseudomonas aeruginosa</italic> Quorum Sensing Signal Cheats Is Influenced by the Diffusivity of the Environment
description	ABSTRACT Experiments examining the social dynamics of bacterial quorum sensing (QS) have focused on mutants which do not respond to signals and the role of QS-regulated exoproducts as public goods. The potential for QS signal molecules to themselves be social public goods has received much less attention. Here, we analyze how signal-deficient (lasI) mutants of the opportunistic pathogen Pseudomonas aeruginosa interact with wild-type cells in an environment where QS is required for growth. We show that when growth requires a “private” intracellular metabolic mechanism activated by the presence of QS signal, lasI mutants act as social cheats and outcompete signal-producing wild-type bacteria in mixed cultures, because they can exploit the signals produced by wild-type cells. However, reducing the ability of signal molecules to diffuse through the growth medium results in signal molecules becoming less accessible to mutants, leading to reduced cheating. Our results indicate that QS signal molecules can be considered social public goods in a way that has been previously described for other exoproducts but that spatial structuring of populations reduces exploitation by noncooperative signal cheats. IMPORTANCE Bacteria communicate via signaling molecules to regulate the expression of a whole range of genes. This process, termed quorum sensing (QS), moderates bacterial metabolism under many environmental conditions, from soil and water (where QS-regulated genes influence nutrient cycling) to animal hosts (where QS-regulated genes determine pathogen virulence). Understanding the ecology of QS could therefore yield vital clues to how we might modify bacterial behavior for environmental or clinical gains. Here, we demonstrate that QS signals act as shareable public goods. This means that their evolution, and therefore population-level responses to interference with QS, will be constrained by population structure. Further, we show that environmental structure (constraints on signal diffusion) alters the accessibility of QS signals and demonstrates that we need to consider population and environmental structure to help us further our understanding of QS signaling systems.
format	article
author	Anne Mund Stephen P. Diggle Freya Harrison
author_facet	Anne Mund Stephen P. Diggle Freya Harrison
author_sort	Anne Mund
title	The Fitness of <italic toggle="yes">Pseudomonas aeruginosa</italic> Quorum Sensing Signal Cheats Is Influenced by the Diffusivity of the Environment
title_short	The Fitness of <italic toggle="yes">Pseudomonas aeruginosa</italic> Quorum Sensing Signal Cheats Is Influenced by the Diffusivity of the Environment
title_full	The Fitness of <italic toggle="yes">Pseudomonas aeruginosa</italic> Quorum Sensing Signal Cheats Is Influenced by the Diffusivity of the Environment
title_fullStr	The Fitness of <italic toggle="yes">Pseudomonas aeruginosa</italic> Quorum Sensing Signal Cheats Is Influenced by the Diffusivity of the Environment
title_full_unstemmed	The Fitness of <italic toggle="yes">Pseudomonas aeruginosa</italic> Quorum Sensing Signal Cheats Is Influenced by the Diffusivity of the Environment
title_sort	fitness of <italic toggle="yes">pseudomonas aeruginosa</italic> quorum sensing signal cheats is influenced by the diffusivity of the environment
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/2751d466b36f4696ab61ce8416133b11
work_keys_str_mv	AT annemund thefitnessofitalictoggleyespseudomonasaeruginosaitalicquorumsensingsignalcheatsisinfluencedbythediffusivityoftheenvironment AT stephenpdiggle thefitnessofitalictoggleyespseudomonasaeruginosaitalicquorumsensingsignalcheatsisinfluencedbythediffusivityoftheenvironment AT freyaharrison thefitnessofitalictoggleyespseudomonasaeruginosaitalicquorumsensingsignalcheatsisinfluencedbythediffusivityoftheenvironment AT annemund fitnessofitalictoggleyespseudomonasaeruginosaitalicquorumsensingsignalcheatsisinfluencedbythediffusivityoftheenvironment AT stephenpdiggle fitnessofitalictoggleyespseudomonasaeruginosaitalicquorumsensingsignalcheatsisinfluencedbythediffusivityoftheenvironment AT freyaharrison fitnessofitalictoggleyespseudomonasaeruginosaitalicquorumsensingsignalcheatsisinfluencedbythediffusivityoftheenvironment
_version_	1718427387790622720

The Fitness of <italic toggle="yes">Pseudomonas aeruginosa</italic> Quorum Sensing Signal Cheats Is Influenced by the Diffusivity of the Environment

Ejemplares similares