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Editor's Pick Research Article

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

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
Kevin Foster, Invited Editor, Dianne K. Newman, Editor
Yasuhiko Irie
School of Life Sciences, Centre for Biomolecular Sciences, University of Nottingham, Nottingham, United KingdomDepartment of Biology and Biochemistry, University of Bath, Bath, United KingdomDepartment of Biology, University of Dayton, Dayton, Ohio, USA
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Aled E. L. Roberts
School of Life Sciences, Centre for Biomolecular Sciences, University of Nottingham, Nottingham, United Kingdom
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Kasper N. Kragh
Department of International Health, Immunology and Microbiology, University of Copenhagen, Copenhagen, Denmark
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Vernita D. Gordon
Center for Nonlinear Dynamics and Department of Physics, The University of Texas at Austin, Austin, Texas, USA
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Jaime Hutchison
Center for Nonlinear Dynamics and Department of Physics, The University of Texas at Austin, Austin, Texas, USA
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Rosalind J. Allen
School of Physics and Astronomy, University of Edinburgh, Edinburgh, United Kingdom
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Gavin Melaugh
Department of Clinical Microbiology, Rigshospitalet, Copenhagen, Denmark
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Thomas Bjarnsholt
Department of International Health, Immunology and Microbiology, University of Copenhagen, Copenhagen, DenmarkDepartment of Clinical Microbiology, Rigshospitalet, Copenhagen, Denmark
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Stuart A. West
Department of Zoology, University of Oxford, Oxford, United Kingdom
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Stephen P. Diggle
School of Life Sciences, Centre for Biomolecular Sciences, University of Nottingham, Nottingham, United Kingdom
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Kevin Foster
University of Oxford
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Dianne K. Newman
California Institute of Technology/HHMI
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DOI: 10.1128/mBio.00374-17
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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.

  • Copyright © 2017 Irie et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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The Pseudomonas aeruginosa PSL Polysaccharide Is a Social but Noncheatable Trait in Biofilms
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
mBio Jun 2017, 8 (3) e00374-17; DOI: 10.1128/mBio.00374-17

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The Pseudomonas aeruginosa PSL Polysaccharide Is a Social but Noncheatable Trait in Biofilms
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
mBio Jun 2017, 8 (3) e00374-17; DOI: 10.1128/mBio.00374-17
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KEYWORDS

Pseudomonas aeruginosa
social evolution
biofilms

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