The Pseudomonas aeruginosa PSL polysaccharide is a social but noncheatable trait in biofilms

Yasuhiko Irie, Aled E.L. Roberts, Kasper Nørskov Kragh, Vernita D. Gordon, Jaime Hutchison, Rosalind J. Allen, Gavin Melaugh, Thomas Bjarnsholt, Stuart A. West, Stephen P. Diggle

Research output: Contribution to journalArticle

19 Citations (Scopus)

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 populationlevel 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.

Original languageEnglish
Article numbere00374-17
JournalmBio
Volume8
Issue number3
DOIs
Publication statusPublished - 1 Jun 2017

Keywords

  • Biofilms
  • Pseudomonas aeruginosa
  • Social evolution

ASJC Scopus subject areas

  • Microbiology
  • Virology

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    Irie, Y., Roberts, A. E. L., Kragh, K. N., Gordon, V. D., Hutchison, J., Allen, R. J., Melaugh, G., Bjarnsholt, T., West, S. A., & Diggle, S. P. (2017). The Pseudomonas aeruginosa PSL polysaccharide is a social but noncheatable trait in biofilms. mBio, 8(3), [e00374-17]. https://doi.org/10.1128/mBio.00374-17