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Cooperation and conflict in quorum-sensing bacterial populations

Nature volume 450, pages 411–414 (2007)Cite this article

Abstract

It has been suggested that bacterial cells communicate by releasing and sensing small diffusible signal molecules in a process commonly known as quorum sensing (QS)1,2,3,4. It is generally assumed that QS is used to coordinate cooperative behaviours at the population level3,5. However, evolutionary theory predicts that individuals who communicate and cooperate can be exploited6,7,8,9,10. Here we examine the social evolution of QS experimentally in the opportunistic pathogen Pseudomonas aeruginosa, and show that although QS can provide a benefit at the group level, exploitative individuals can avoid the cost of producing the QS signal or of performing the cooperative behaviour that is coordinated by QS, and can therefore spread. We also show that a solution to the problem of exploitation is kin selection, if interacting bacterial cells tend to be close relatives. These results show that the problem of exploitation, which has been the focus of considerable attention in animal communication, also arises in bacteria.

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Figure 1: QS-controlled public goods provide a benefit at the population level in QSM.
Figure 2: QS-dependent cooperation is costly.
Figure 3: QS is subject to cheating.
Figure 4: Kin selection and QS.

References

  1. Keller, L. & Surette, M. G. Communication in bacteria: an ecological and evolutionary perspective. Nat. Rev. Microbiol. 4, 249–258 (2006)

    CAS  Article  Google Scholar 

  2. Diggle, S. P., Gardner, A., West, S. A. & Griffin, A. S. Evolutionary theory of bacterial quorum sensing: when is a signal not a signal? Phil. Trans. R. Soc. B 362, 1241–1249 (2007)

    CAS  Article  Google Scholar 

  3. Henke, J. M. & Bassler, B. L. Bacterial social engagements. Trends Cell Biol. 14, 648–656 (2004)

    CAS  Article  Google Scholar 

  4. Williams, P., Winzer, K., Chan, W. C. & Camara, M. Look who's talking: communication and quorum sensing in the bacterial world. Phil. Trans. R. Soc. B 362, 1119–1134 (2007)

    CAS  Article  Google Scholar 

  5. Shapiro, J. A. Thinking about bacterial populations as multicellular organisms. Annu. Rev. Microbiol. 52, 81–104 (1998)

    CAS  Article  Google Scholar 

  6. Maynard Smith, J. & Harper, D. Animal Signals (Oxford Univ. Press, Oxford, 2003)

    Google Scholar 

  7. Lehmann, L. & Keller, L. The evolution of cooperation and altruism-a general framework and a classification of models. J. Evol. Biol. 19, 1365–1376 (2006)

    CAS  Article  Google Scholar 

  8. Hamilton, W. D. Genetical evolution of social behaviour. I & II. J. Theor. Biol. 7, 1–52 (1964)

    ADS  CAS  Article  Google Scholar 

  9. Frank, S. A. Foundations of Social Evolution (Princeton Univ. Press, Princeton, NJ, 1998)

    Book  Google Scholar 

  10. Ratnieks, F. L. W., Foster, K. R. & Wenseleers, T. Conflict resolution in insect societies. Annu. Rev. Entomol. 51, 581–608 (2006)

    CAS  Article  Google Scholar 

  11. West, S. A., Griffin, A. S., Gardner, A. & Diggle, S. P. Social evolution theory for microorganisms. Nat. Rev. Microbiol. 4, 597–607 (2006)

    CAS  Article  Google Scholar 

  12. West, S. A., Griffin, A. S. & Gardner, A. Social semantics: altruism, cooperation, mutualism, strong reciprocity and group selection. J. Evol. Biol. 20, 415–432 (2007)

    CAS  Article  Google Scholar 

  13. Redfield, R. J. Is quorum sensing a side effect of diffusion sensing? Trends Microbiol. 10, 365–370 (2002)

    CAS  Article  Google Scholar 

  14. Brown, S. P. & Johnstone, R. A. Cooperation in the dark: signalling and collective action in quorum-sensing bacteria. Proc. R. Soc. Lond. B 268, 961–965 (2001)

    CAS  Article  Google Scholar 

  15. Venturi, V. Regulation of quorum sensing in Pseudomonas. . FEMS Microbiol. Rev. 30, 274–291 (2006)

    CAS  Article  Google Scholar 

  16. Schuster, M., Lostroh, C. P., Ogi, T. & Greenberg, E. P. Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J. Bacteriol. 185, 2066–2079 (2003)

    CAS  Article  Google Scholar 

  17. Pesci, E. C., Pearson, J. P., Seed, P. C. & Iglewski, B. H. Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa . J. Bacteriol. 179, 3127–3132 (1997)

    CAS  Article  Google Scholar 

  18. Latifi, A. et al. A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhIR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol. Microbiol. 21, 1137–1146 (1996)

    CAS  Article  Google Scholar 

  19. Fletcher, M. P. et al. A dual biosensor for 2-alkyl-4-quinolone quorum sensing signal molecules. Environ. Microbiol. 9, 2683–2693 (2007)

    MathSciNet  CAS  Article  Google Scholar 

  20. Schaber, J. A. et al. Analysis of quorum sensing-deficient clinical isolates of Pseudomonas aeruginosa . J. Med. Microbiol. 53, 841–853 (2004)

    CAS  Article  Google Scholar 

  21. Chhabra, S. R. et al. Synthetic analogues of the bacterial signal (quorum sensing) molecule N-(3-oxododecanoyl)-l-homoserine lactone as immune modulators. J. Med. Chem. 46, 97–104 (2003)

    CAS  Article  Google Scholar 

  22. Ross-Gillespie, A., Gardner, A., West, S. A. & Griffin, A. S. Frequency dependence and cooperation: theory and a test with bacteria. Am. Nat. 170, 331–342 (2007)

    Article  Google Scholar 

  23. MacLean, R. C. & Gudelj, I. Resource competition and social conflict in experimental populations of yeast. Nature 441, 498–501 (2006)

    ADS  CAS  Article  Google Scholar 

  24. Griffin, A. S., West, S. A. & Buckling, A. Cooperation and competition in pathogenic bacteria. Nature 430, 1024–1027 (2004)

    ADS  CAS  Article  Google Scholar 

  25. Smith, E. E. et al. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc. Natl Acad. Sci. USA 103, 8487–8492 (2006)

    ADS  CAS  Article  Google Scholar 

  26. Denervaud, V. et al. Characterization of cell-to-cell signaling-deficient Pseudomonas aeruginosa strains colonizing intubated patients. J. Clin. Microbiol. 42, 554–562 (2004)

    CAS  Article  Google Scholar 

  27. Salunkhe, P. et al. A cystic fibrosis epidemic strain of Pseudomonas aeruginosa displays enhanced virulence and antimicrobial resistance. J. Bacteriol. 187, 4908–4920 (2005)

    CAS  Article  Google Scholar 

  28. Jones, A. M. et al. Identification of airborne dissemination of epidemic multiresistant strains of Pseudomonas aeruginosa at a CF centre during a cross infection outbreak. Thorax 58, 525–527 (2003)

    CAS  Article  Google Scholar 

  29. West, S. A., Pen, I. & Griffin, A. S. Conflict and cooperation—cooperation and competition between relatives. Science 296, 72–75 (2002)

    ADS  CAS  Article  Google Scholar 

  30. Heurlier, K. et al. Quorum-sensing-negative (lasR) mutants of Pseudomonas aeruginosa avoid cell lysis and death. J. Bacteriol. 187, 4875–4883 (2005)

    CAS  Article  Google Scholar 

  31. Winzer, K. et al. The Pseudomonas aeruginosa lectins PA-IL and PA-IIL are controlled by quorum sensing and by RpoS. J. Bacteriol. 182, 6401–6411 (2000)

    CAS  Article  Google Scholar 

  32. Chhabra, S. R. et al. Autoregulation of carbapenem biosynthesis in Erwinia carotovora by analogs of N-(3-oxohexanoyl)-l-homoserine lactone. J. Antibiot. (Tokyo) 46, 441–454 (1993)

    CAS  Article  Google Scholar 

  33. Diggle, S. P. et al. Advancing the quorum in Pseudomonas aeruginosa: MvaT and the regulation of N-acylhomoserine lactone production and virulence gene expression. J. Bacteriol. 184, 2576–2586 (2002)

    CAS  Article  Google Scholar 

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Acknowledgements

We thank P. Williams and R. Chhabra for the provision of AHL compounds; D. Jackson for comments on the manuscript; and A. Ross-Gillespie for help in analysing the data. We acknowledge funding from the Royal Society and the Leverhulme Trust.

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Authors and Affiliations

  1. Institute of Infection, Immunity & Inflammation, Centre for Biomolecular Sciences, University Park, University of Nottingham, Nottingham NG7 2RD, UK

    Stephen P. Diggle & Genevieve S. Campbell

  2. Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, King’s Buildings, Edinburgh EH9 3JT, UK ,

    Ashleigh S. Griffin & Stuart A. West

Authors
  1. Stephen P. Diggle
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  2. Ashleigh S. Griffin
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  3. Genevieve S. Campbell
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  4. Stuart A. West
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Correspondence to Stephen P. Diggle or Stuart A. West.

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Diggle, S., Griffin, A., Campbell, G. et al. Cooperation and conflict in quorum-sensing bacterial populations. Nature 450, 411–414 (2007). https://doi.org/10.1038/nature06279

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