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The Pseudomonas aeruginosa PSL Polysaccharide Is a Social but Noncheatable Trait in Biofilms

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Author
Irie, Yasuhiko
Roberts, Aled Edward Lloyd
Kragh, Kasper
Gordon, Vernita
Hutchison, Jaime
Allen, Rosalind
Melaugh, Gavin
Bjarnsholt, Thomas
West, Stuart
Diggle, Stephen
Date
2017-06-20
Acceptance date
2017-05-19
Type
Article
Publisher
American Society for Microbiology
ISSN
2150-7511
Metadata
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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.
Journal/conference proceeding
mBio;
Citation
Irie, Y., Roberts, A.E., Kragh, K.N., Gordon, V.D., Hutchison, J., Allen, R.J., Melaugh, G., Bjarnsholt, T., West, S.A. and Diggle, S.P. (2017) 'The Pseudomonas aeruginosa PSL polysaccharide is a social but noncheatable trait in biofilms', MBio, 8(3), pp.e00374-17. DOI: 10.1128/mBio.00374-17.
URI
http://hdl.handle.net/10369/10502
DOI
http://dx.doi.org/10.1128/mBio.00374-17
Description
Article published in mBio on 20 June 2017, available at: http://dx.doi.org/10.1128/mBio.00374-17.
Rights
https://creativecommons.org/licenses/by/4.0/
Sponsorship
Cardiff Metropolitan University (Grant ID: Cardiff Metropolian (Internal))
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  • Health and Risk Management [392]

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