1887

Abstract

In the opportunistic pathogen quorum sensing (QS) is a social trait that is exploitable by non-cooperating cheats. Previously it has been shown that by linking QS to the production of both public and private goods, cheats can be prevented from invading populations of cooperators and this was described by Dandekar . (Science 2012;338:264–266) as ‘a metabolic incentive to cooperate’. We hypothesized that could evolve novel cheating strategies to circumvent private goods metabolism by rewiring its combinatorial response to two QS signals (3O-C12-HSL and C4-HSL). We performed a selection experiment that cycled between public and private goods growth media and evolved an isolate that rewired its control of cooperative protease expression from a synergistic (AND-gate) response to dual-signal input to a 3O-C12-HSL-only response. We show that this isolate circumvents metabolic incentives to cooperate and acts as a combinatorial signalling cheat, with higher fitness in competition with its ancestor. Our results show three important principles: first, combinatorial QS allows for diverse social strategies to emerge; second, restrictions levied by private goods are not sufficient to explain the maintenance of cooperation in natural populations; and third, modifying combinatorial QS responses could result in important physiological outcomes in bacterial populations.

Funding
This study was supported by the:
  • Simons Foundation (Award 396001)
    • Principle Award Recipient: James Gurney
  • Human Frontier Science Program (FR) (Award RGY0081/2012)
    • Principle Award Recipient: Not Applicable
  • Natural Environment Research Council (Award NE/J007064/1)
    • Principle Award Recipient: James Gurney
  • Medical Research Council
    • Principle Award Recipient: James Gurney
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000941
2020-06-08
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/166/8/777.html?itemId=/content/journal/micro/10.1099/mic.0.000941&mimeType=html&fmt=ahah

References

  1. Diggle SP, Griffin AS, Campbell GS, West SA. Cooperation and conflict in quorum-sensing bacterial populations. Nature 2007; 450:411–414 [View Article][PubMed]
    [Google Scholar]
  2. West SA, Griffin AS, Gardner A, Diggle SP. Social evolution theory for microorganisms. Nat Rev Microbiol 2006; 4:597–607 [View Article][PubMed]
    [Google Scholar]
  3. Sandoz KM, Mitzimberg SM, Schuster M. Social cheating in Pseudomonas aeruginosa quorum sensing. Proc Natl Acad Sci U S A 2007; 104:15876–15881 [View Article][PubMed]
    [Google Scholar]
  4. Xavier JB, Kim W, Foster KR. A molecular mechanism that stabilizes cooperative secretions in Pseudomonas aeruginosa . Mol Microbiol 2011; 79:166–179 [View Article][PubMed]
    [Google Scholar]
  5. Dandekar AA, Chugani S, Greenberg EP. Bacterial quorum sensing and metabolic incentives to cooperate. Science 2012; 338:264–266 [View Article][PubMed]
    [Google Scholar]
  6. Rumbaugh KP, Diggle SP, Watters CM, Ross-Gillespie A, Griffin AS et al. Quorum sensing and the social evolution of bacterial virulence. Curr Biol 2009; 19:341–345 [View Article][PubMed]
    [Google Scholar]
  7. Popat R, Pollitt EJG, Harrison F, Naghra H, Hong K-W et al. Conflict of interest and signal interference lead to the breakdown of honest signaling. Evolution 2015; 69:2371–2383 [View Article][PubMed]
    [Google Scholar]
  8. Popat R, Crusz SA, Messina M, Williams P, West SA et al. Quorum-Sensing and cheating in bacterial biofilms. Proc Biol Sci 2012; 279:4765–4771 [View Article][PubMed]
    [Google Scholar]
  9. Pollitt EJG, West SA, Crusz SA, Burton-Chellew MN, Diggle SP. Cooperation, quorum sensing, and evolution of virulence in Staphylococcus aureus . Infect Immun 2014; 82:1045–1051 [View Article][PubMed]
    [Google Scholar]
  10. Popat R, Harrison F, da Silva AC, Easton SAS, McNally L et al. Environmental modification via a quorum sensing molecule influences the social landscape of siderophore production. Proc Biol Sci 2017; 284:20170200 [View Article][PubMed]
    [Google Scholar]
  11. Brown SP, West SA, Diggle SP, Griffin AS. Social evolution in micro-organisms and a Trojan horse approach to medical intervention strategies. Philos Trans R Soc Lond B Biol Sci 2009; 364:3157–3168 [View Article][PubMed]
    [Google Scholar]
  12. Köhler T, Buckling A, van Delden C. Cooperation and virulence of clinical Pseudomonas aeruginosa populations. Proc Natl Acad Sci U S A 2009; 106:6339–6344 [View Article][PubMed]
    [Google Scholar]
  13. Darch SE, West SA, Winzer K, Diggle SP. Density-Dependent fitness benefits in quorum-sensing bacterial populations. Proc Natl Acad Sci U S A 2012; 109:8259–8263 [View Article][PubMed]
    [Google Scholar]
  14. Allen RC, McNally L, Popat R, Brown SP. Quorum sensing protects bacterial co-operation from exploitation by cheats. Isme J 2016; 10:1706–1716 [View Article][PubMed]
    [Google Scholar]
  15. Smith EE, Buckley DG, Wu Z, Saenphimmachak C, Hoffman LR et al. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci U S A 2006; 103:8487–8492 [View Article][PubMed]
    [Google Scholar]
  16. Feltner JB, Wolter DJ, Pope CE, Groleau M-C, Smalley NE et al. LasR Variant Cystic Fibrosis Isolates Reveal an Adaptable Quorum-Sensing Hierarchy in Pseudomonas aeruginosa . mBio 2016; 7:e01513-16 [View Article][PubMed]
    [Google Scholar]
  17. Whiteley M, Diggle SP, Greenberg EP. Progress in and promise of bacterial quorum sensing research. Nature 2017; 551:313–320 [View Article][PubMed]
    [Google Scholar]
  18. Mund A, Diggle SP, Harrison F. The Fitness of Pseudomonas aeruginosa Quorum Sensing Signal Cheats Is Influenced by the Diffusivity of the Environment. MBio 2017; 8: [View Article]
    [Google Scholar]
  19. Hamilton WD. The genetical evolution of social behaviour. I. J Theor Biol 1964; 7:1–16 [View Article][PubMed]
    [Google Scholar]
  20. Hamilton WD. The genetical evolution of social behaviour. II. J Theor Biol 1964; 7:17–52 [View Article][PubMed]
    [Google Scholar]
  21. Griffin AS, West SA, Buckling A. Cooperation and competition in pathogenic bacteria. Nature 2004; 430:1024–1027 [View Article][PubMed]
    [Google Scholar]
  22. Rumbaugh KP, Trivedi U, Watters C, Burton-Chellew MN, Diggle SP et al. Kin selection, quorum sensing and virulence in pathogenic bacteria. Proc Biol Sci 2012; 279:3584–3588 [View Article][PubMed]
    [Google Scholar]
  23. Foster KR, Shaulsky G, Strassmann JE, Queller DC, Thompson CRL. Pleiotropy as a mechanism to stabilize cooperation. Nature 2004; 431:693–696 [View Article][PubMed]
    [Google Scholar]
  24. Cornforth DM, Popat R, McNally L, Gurney J, Scott-Phillips TC et al. Combinatorial quorum sensing allows bacteria to resolve their social and physical environment. Proc Natl Acad Sci U S A 2014; 111:4280–4284 [View Article][PubMed]
    [Google Scholar]
  25. Strassmann JE, Gilbert OM, Queller DC. Kin discrimination and cooperation in microbes. Annu Rev Microbiol 2011; 65:349–367 [View Article][PubMed]
    [Google Scholar]
  26. West SA, Winzer K, Gardner A, Diggle SP. Quorum sensing and the confusion about diffusion. Trends Microbiol 2012; 20:586–594 [View Article][PubMed]
    [Google Scholar]
  27. Wilder CN, Diggle SP, Schuster M. Cooperation and cheating in Pseudomonas aeruginosa: the roles of the las, rhl and pqs quorum-sensing systems. Isme J 2011; 5:1332–1343 [View Article][PubMed]
    [Google Scholar]
  28. West SA, Altruism GA. Spite, and greenbeards. Science 2010; 327:1341–1344
    [Google Scholar]
  29. Whiteley M, Lee KM, Greenberg EP. Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa . Proc Natl Acad Sci U S A 1999; 96:13904–13909 [View Article][PubMed]
    [Google Scholar]
  30. Brint JM, Ohman DE. Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under the control of RhlR-RhlI, another set of regulators in strain PAO1 with homology to the autoinducer-responsive LuxR-LuxI family. J Bacteriol 1995; 177:7155–7163 [View Article][PubMed]
    [Google Scholar]
  31. Pearson JP, Pesci EC, Iglewski BH. Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol 1997; 179:5756–5767 [View Article][PubMed]
    [Google Scholar]
  32. Scott-Phillips TC, Gurney J, Ivens A, Diggle SP, Popat R. Combinatorial communication in bacteria: implications for the origins of linguistic generativity. PLoS One 2014; 9:e95929 [View Article][PubMed]
    [Google Scholar]
  33. Kostylev M, Kim DY, Smalley NE, Salukhe I, Greenberg EP et al. Evolution of the Pseudomonas aeruginosa quorum-sensing hierarchy. Proc Natl Acad Sci U S A 2019; 116:7027–7032 [View Article][PubMed]
    [Google Scholar]
  34. Oshri RD, Zrihen KS, Shner I, Omer Bendori S, Eldar A. Selection for increased quorum-sensing cooperation in Pseudomonas aeruginosa through the shut-down of a drug resistance pump. Isme J 2018; 12:2458–2469 [View Article][PubMed]
    [Google Scholar]
  35. Dos Santos M, Ghoul M, West SA. Pleiotropy, cooperation, and the social evolution of genetic architecture. PLoS Biol 2018; 16:e2006671 [View Article][PubMed]
    [Google Scholar]
  36. Becher A, Schweizer HP. Integration-proficient Pseudomonas aeruginosa vectors for isolation of single-copy chromosomal lacZ and lux gene fusions. Biotechniques 2000; 29:948–952 [View Article][PubMed]
    [Google Scholar]
  37. Ross-Gillespie A, Gardner A, West SA, Griffin AS. Frequency dependence and cooperation: theory and a test with bacteria. Am Nat 2007; 170:331–342 PubMed PMID [View Article][PubMed]
    [Google Scholar]
  38. Grubbs FE. Sample criteria for testing Outlying observations. The Annals of Mathematical Statistics 1950; 21:27–58 [View Article]
    [Google Scholar]
  39. McDonald JH. Handbook of Biological Statistics, 3rd ed. Baltimore, Maryland: Sparky House Publishing; 2014
    [Google Scholar]
  40. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article][PubMed]
    [Google Scholar]
  41. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article][PubMed]
    [Google Scholar]
  42. Alikhan N-F, Petty NK, Ben Zakour NL, Beatson SA. Blast ring image generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 2011; 12:402 [View Article][PubMed]
    [Google Scholar]
  43. Darling AE, Mau B, Perna NT. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 2010; 5:e11147 [View Article][PubMed]
    [Google Scholar]
  44. Deatherage DE, Barrick JE. Identification of mutations in laboratory-evolved microbes from next-generation sequencing data using breseq. Methods Mol Biol 2014; 1151:165–188 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000941
Loading
/content/journal/micro/10.1099/mic.0.000941
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error