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Developmental cheating in the social bacterium Myxococcus xanthus

Abstract

Cheating is a potential problem in any social system that depends on cooperation and in which actions that benefit a group are costly to individuals that perform them1,2,3,4,5. Genetic mutants that fail to perform a group-beneficial function but that reap the benefits of belonging to the group should have a within-group selective advantage, provided that the mutants are not too common. Here we show that social cheating exists even among prokaryotes. The bacterium Myxococcus xanthus exhibits several social behaviours, including aggregation of cells into spore-producing fruiting bodies during starvation. We examined a number of M. xanthus genotypes that were defective for fruiting-body development, including several lines that evolved for 1,000 generations under asocial conditions6 and others carrying defined mutations in developmental pathways7,8,9,10, to determine whether they behaved as cheaters when mixed with their developmentally proficient progenitor. Clones from several evolved lines and two defined mutants exhibited cheating during development, being over-represented among resulting spores relative to their initial frequency in the mixture. The ease of finding anti-social behaviours suggests that cheaters may be common in natural populations of M. xanthus.

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Figure 1: Spore production for six independently evolved clones6 of M. xanthus and their common ancestor (DK1622).
Figure 2: Spore production of two evolved clones when mixed with their wild-type progenitor at nine initial ratios, and the corresponding relative sporulation efficiencies.
Figure 3: Spore production of mutants DK4312 (asgB) (a) and LS523 (csgA) (b), and their respective wild-type progenitors in pure and mixed culture.

References

  1. Maynard Smith,J. Evolution and the Theory of Games (Cambridge Univ. Press, Cambridge, 1982).

    Book  Google Scholar 

  2. Axelrod,R. M. The Evolution of Cooperation (Basic Books, New York, 1984).

    MATH  Google Scholar 

  3. Pellmyr,O., Leebens-Mack,J. & Huth, C. J. Non-mutualistic yucca moths and their evolutionary consequences. Nature 380, 155– 156 (1996).

    Article  ADS  CAS  Google Scholar 

  4. Matapurkar,A. K. & Watve,M. G. Altruist cheater dynamics in Dictyostelium: aggregated distribution gives stable oscillations. Am. Nat. 150, 790–797 (1997).

    Article  CAS  Google Scholar 

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

    Google Scholar 

  6. Velicer,G. J., Kroos,L. & Lenski,R. E. Loss of social behaviors by Myxococcus xanthus during evolution in an unstructured habitat. Proc. Natl Acad. Sci. USA 95, 12376–12380 ( 1998).

    Article  ADS  CAS  Google Scholar 

  7. Kuspa,A., Kroos,L. & Kaiser,D. Intercellular signaling is required for developmental gene expression in Myxococcus xanthus. Dev. Biol. 117, 267–276 (1986).

    Article  CAS  Google Scholar 

  8. Shimkets,L. J. & Asher,S. J. Use of recombination techniques to examine the structure of the csg locus of Myxococcus xanthus . Mol. Gen. Genet. 211, 63– 71 (1988).

    Article  CAS  Google Scholar 

  9. Kuspa,A. & Kaiser,D. Genes required for developmental signaling in Myxococcus xanthus: three asg loci. J. Bacteriol. 171, 2762–2772 ( 1989).

    Article  CAS  Google Scholar 

  10. Garza,A. G., Harris,B. Z., Pollack,J. S., Tzeng,L. & Singer,M. The asgE locus is required for cell-cell signaling during Myxococcus xanthus development. Mol. Microbiol. 35, 812–824 (2000).

    Article  CAS  Google Scholar 

  11. Bonner,J. T. The Cellular Slime Molds (Princeton Univ. Press, Princeton, 1967).

    Google Scholar 

  12. Kaiser,D. Control of multicellular development: Dictyostelium and Myxococcus. Annu. Rev. Genet. 20, 539– 566 (1986).

    Article  CAS  Google Scholar 

  13. Reichenbach,H. in Myxobacteria II (eds Dworkin, M. & Kaiser, D.) 13– 62 (Am. Soc. Microbiol., Washington, DC, 1993).

    Google Scholar 

  14. Dworkin,M. & Kaiser,D. (eds) Myxobacteria II (Am. Soc. Microbiol., Washington, DC, 1993).

    Google Scholar 

  15. Rosenberg,E. & Varon,M. in Myxobacteria: Development and Cell Interactions (ed. Rosenberg, E.) 109–125 (Springer, New York, 1984).

    Google Scholar 

  16. Kaiser,D. Social gliding is correlated with the presence of pili in Myxococcus xanthus . Proc. Natl Acad. Sci. USA 76, 5952 –5956 (1979).

    Article  ADS  CAS  Google Scholar 

  17. Hagen,D. C., Bretscher,A. P. & Kaiser, D. Synergism between morphogenetic mutants of Myxococcus xanthus. Dev. Biol. 64, 284– 296 (1978).

    Article  CAS  Google Scholar 

  18. Downard,J., Ramaswamy,S. V. & Kil, K. Identification of esg, a genetic locus involved in cell–cell signaling during Myxococcus xanthus development. J. Bacteriol. 175, 7762– 7770 (1993).

    Article  CAS  Google Scholar 

  19. Laue,B. E. & Gill,R. E. Using a phase-locked mutant of Myxococcus xanthus to study the role of phase variation in development. J. Bacteriol. 177, 4089– 4096 (1995).

    Article  CAS  Google Scholar 

  20. Buss,L. W. Somatic cell parasitism and the evolution of somatic tissue compatibility. Proc. Natl Acad. Sci. USA 79, 5337– 5341 (1982).

    Article  ADS  CAS  Google Scholar 

  21. Nowak,M. A. & May,R. M. Evolutionary games and spatial chaos. Nature 359, 826–829 (1992).

    Article  ADS  Google Scholar 

  22. Frank,S. A. Mutual policing and repression of competition in the evolution of cooperative groups. Nature 377, 520– 522 (1995).

    Article  ADS  CAS  Google Scholar 

  23. Maynard Smith,J. & Szathmáry,E. The Major Transitions in Evolution (Oxford Univ. Press, New York, 1995).

    Google Scholar 

  24. Grosberg,R. K. & Strathmann,R. R. One cell, two cell, red cell, blue cell: the persistence of a unicellular stage in multicellular life histories. Trends Ecol. Evol. 13, 112 –116 (1998).

    Article  CAS  Google Scholar 

  25. Buss,L. W. Slime molds, ascidians, and the utility of evolutionary theory. Proc. Natl Acad. Sci. USA 96, 8801– 8803 (1999).

    Article  ADS  CAS  Google Scholar 

  26. Stoner,D. S., Rinkevich,B. & Weissman, I. L. Heritable germ and somatic cell lineage competitions in chimeric colonial protochordates. Proc. Natl Acad. Sci. USA 96, 9148–9153 ( 1999).

    Article  ADS  CAS  Google Scholar 

  27. Turner,P. E. & Chao,L. Prisoner's dilemma in an RNA virus. Nature 398, 441–443 (1999).

    Article  ADS  CAS  Google Scholar 

  28. Hodgkin,J. & Kaiser,D. Cell-to-cell stimulation of motility in nonmotile mutants of M. xanthus. Proc. Natl Acad. Sci. USA 74, 2938–2942 ( 1977).

    Article  ADS  CAS  Google Scholar 

  29. Wall,D., Kolenbrander,P. E. & Kaiser, D. The Myxococcus xanthus pilQ (sglA) gene encodes a secretin homolog required for type IV pilus biogenesis, social motility and development. J. Bacteriol. 181, 24– 33 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Kroos,L., Kuspa,A. & Kaiser,D. A global analysis of developmentally regulated genes in Myxococcus xanthus . Dev. Biol. 117, 252– 266 (1986).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank A. Garza, L. Shimkets, M. Singer and J. Strassman for helpful discussion, A. Garza for providing strain MS2021, and N. Hajela and J. Jiang for technical assistance. This research was supported by Michigan State University and an NSF grant to R.E.L.

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Correspondence to Gregory J. Velicer.

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Velicer, G., Kroos, L. & Lenski, R. Developmental cheating in the social bacterium Myxococcus xanthus . Nature 404, 598–601 (2000). https://doi.org/10.1038/35007066

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