The <italic toggle="yes">Pseudomonas aeruginosa</italic> PSL Polysaccharide Is a Social but Noncheatable Trait in Biofilms

ABSTRACT Extracellular polysaccharides are compounds secreted by microorganisms into the surrounding environment, and they are important for surface attachment and maintaining structural integrity within biofilms. The social nature of many extracellular polysaccharides remains unclear, and it has be...

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Autores principales:	Yasuhiko Irie, Aled E. L. Roberts, Kasper N. Kragh, Vernita D. Gordon, Jaime Hutchison, Rosalind J. Allen, Gavin Melaugh, Thomas Bjarnsholt, Stuart A. West, Stephen P. Diggle
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	Pseudomonas aeruginosa social evolution biofilms Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/9b8f3b6e394949d9a807d06669491db4
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spelling	oai:doaj.org-article:9b8f3b6e394949d9a807d06669491db42021-11-15T15:51:29ZThe <italic toggle="yes">Pseudomonas aeruginosa</italic> PSL Polysaccharide Is a Social but Noncheatable Trait in Biofilms10.1128/mBio.00374-172150-7511https://doaj.org/article/9b8f3b6e394949d9a807d06669491db42017-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00374-17https://doaj.org/toc/2150-7511ABSTRACT Extracellular polysaccharides are compounds secreted by microorganisms into the surrounding environment, and they are important for surface attachment and maintaining structural integrity within biofilms. The social nature of many extracellular polysaccharides remains unclear, and it has been suggested that they could function as either cooperative public goods or as traits that provide a competitive advantage. Here, we empirically tested the cooperative nature of the PSL polysaccharide, which is crucial for the formation of biofilms in Pseudomonas aeruginosa. We show that (i) PSL is not metabolically costly to produce; (ii) PSL provides population-level benefits in biofilms, for both growth and antibiotic tolerance; (iii) the benefits of PSL production are social and are shared with other cells; (iv) the benefits of PSL production appear to be preferentially directed toward cells which produce PSL; (v) cells which do not produce PSL are unable to successfully exploit cells which produce PSL. Taken together, this suggests that PSL is a social but relatively nonexploitable trait and that growth within biofilms selects for PSL-producing strains, even when multiple strains are on a patch (low relatedness at the patch level). IMPORTANCE Many studies have shown that bacterial traits, such as siderophores and quorum sensing, are social in nature. This has led to an impression that secreted traits act as public goods, which are costly to produce but benefit both the producing cell and its surrounding neighbors. Theories and subsequent experiments have shown that such traits are exploitable by asocial cheats, but we show here that this does not always hold true. We demonstrate that the Pseudomonas aeruginosa exopolysaccharide PSL provides social benefits to populations but that it is nonexploitable, because most of the fitness benefits accrue to PSL-producing cells. Our work builds on an increasing body of work showing that secreted traits can have both private and public benefits to cells.Yasuhiko IrieAled E. L. RobertsKasper N. KraghVernita D. GordonJaime HutchisonRosalind J. AllenGavin MelaughThomas BjarnsholtStuart A. WestStephen P. DiggleAmerican Society for MicrobiologyarticlePseudomonas aeruginosasocial evolutionbiofilmsMicrobiologyQR1-502ENmBio, Vol 8, Iss 3 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Pseudomonas aeruginosa social evolution biofilms Microbiology QR1-502
spellingShingle	Pseudomonas aeruginosa social evolution biofilms Microbiology QR1-502 Yasuhiko Irie Aled E. L. Roberts Kasper N. Kragh Vernita D. Gordon Jaime Hutchison Rosalind J. Allen Gavin Melaugh Thomas Bjarnsholt Stuart A. West Stephen P. Diggle The <italic toggle="yes">Pseudomonas aeruginosa</italic> PSL Polysaccharide Is a Social but Noncheatable Trait in Biofilms
description	ABSTRACT Extracellular polysaccharides are compounds secreted by microorganisms into the surrounding environment, and they are important for surface attachment and maintaining structural integrity within biofilms. The social nature of many extracellular polysaccharides remains unclear, and it has been suggested that they could function as either cooperative public goods or as traits that provide a competitive advantage. Here, we empirically tested the cooperative nature of the PSL polysaccharide, which is crucial for the formation of biofilms in Pseudomonas aeruginosa. We show that (i) PSL is not metabolically costly to produce; (ii) PSL provides population-level benefits in biofilms, for both growth and antibiotic tolerance; (iii) the benefits of PSL production are social and are shared with other cells; (iv) the benefits of PSL production appear to be preferentially directed toward cells which produce PSL; (v) cells which do not produce PSL are unable to successfully exploit cells which produce PSL. Taken together, this suggests that PSL is a social but relatively nonexploitable trait and that growth within biofilms selects for PSL-producing strains, even when multiple strains are on a patch (low relatedness at the patch level). IMPORTANCE Many studies have shown that bacterial traits, such as siderophores and quorum sensing, are social in nature. This has led to an impression that secreted traits act as public goods, which are costly to produce but benefit both the producing cell and its surrounding neighbors. Theories and subsequent experiments have shown that such traits are exploitable by asocial cheats, but we show here that this does not always hold true. We demonstrate that the Pseudomonas aeruginosa exopolysaccharide PSL provides social benefits to populations but that it is nonexploitable, because most of the fitness benefits accrue to PSL-producing cells. Our work builds on an increasing body of work showing that secreted traits can have both private and public benefits to cells.
format	article
author	Yasuhiko Irie Aled E. L. Roberts Kasper N. Kragh Vernita D. Gordon Jaime Hutchison Rosalind J. Allen Gavin Melaugh Thomas Bjarnsholt Stuart A. West Stephen P. Diggle
author_facet	Yasuhiko Irie Aled E. L. Roberts Kasper N. Kragh Vernita D. Gordon Jaime Hutchison Rosalind J. Allen Gavin Melaugh Thomas Bjarnsholt Stuart A. West Stephen P. Diggle
author_sort	Yasuhiko Irie
title	The <italic toggle="yes">Pseudomonas aeruginosa</italic> PSL Polysaccharide Is a Social but Noncheatable Trait in Biofilms
title_short	The <italic toggle="yes">Pseudomonas aeruginosa</italic> PSL Polysaccharide Is a Social but Noncheatable Trait in Biofilms
title_full	The <italic toggle="yes">Pseudomonas aeruginosa</italic> PSL Polysaccharide Is a Social but Noncheatable Trait in Biofilms
title_fullStr	The <italic toggle="yes">Pseudomonas aeruginosa</italic> PSL Polysaccharide Is a Social but Noncheatable Trait in Biofilms
title_full_unstemmed	The <italic toggle="yes">Pseudomonas aeruginosa</italic> PSL Polysaccharide Is a Social but Noncheatable Trait in Biofilms
title_sort	<italic toggle="yes">pseudomonas aeruginosa</italic> psl polysaccharide is a social but noncheatable trait in biofilms
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/9b8f3b6e394949d9a807d06669491db4
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The <italic toggle="yes">Pseudomonas aeruginosa</italic> PSL Polysaccharide Is a Social but Noncheatable Trait in Biofilms

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