Skip to main content
NCBI home page
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2003 Jul 22;270(1523):1527–1534. doi: 10.1098/rspb.2003.2387

Competitive fates of bacterial social parasites: persistence and self-induced extinction of Myxococcus xanthus cheaters.

Francesca Fiegna 1, Gregory J Velicer 1
PMCID: PMC1691394  PMID: 12965020

Abstract

Cooperative biological systems are susceptible to disruption by cheating. Using the social bacterium Myxococcus xanthus, we have tested the short-term competitive fates of mixed cheater and wild-type strains over multiple cycles of cooperative development. Cheater/wild-type mixes underwent several cycles of starvation-induced multicellular development followed by spore germination and vegetative population growth. The population sizes of cheater and wild-type strains in each pairwise mixture were measured at the end of each developmental phase and each growth phase. Cheater genotypes showed several distinct competitive fates, including cheater persistence at high frequencies with little effect on total population dynamics, cheater persistence after major disruption of total population dynamics, self-extinction of cheaters with wild-type survival, and total population extinction. Our results empirically demonstrate that social exploitation can destabilize a cooperative biological system and increase the risk of local extinction events.

Full Text

The Full Text of this article is available as a PDF (138.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Axelrod R., Hamilton W. D. The evolution of cooperation. Science. 1981 Mar 27;211(4489):1390–1396. doi: 10.1126/science.7466396. [DOI] [PubMed] [Google Scholar]
  2. Brown Sam P., Hochberg Michael E., Grenfell Bryan T. Does multiple infection select for raised virulence? Trends Microbiol. 2002 Sep;10(9):401–405. doi: 10.1016/s0966-842x(02)02413-7. [DOI] [PubMed] [Google Scholar]
  3. Chao L., Hanley K. A., Burch C. L., Dahlberg C., Turner P. E. Kin selection and parasite evolution: higher and lower virulence with hard and soft selection. Q Rev Biol. 2000 Sep;75(3):261–275. doi: 10.1086/393499. [DOI] [PubMed] [Google Scholar]
  4. Chao L., Levin B. R. Structured habitats and the evolution of anticompetitor toxins in bacteria. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6324–6328. doi: 10.1073/pnas.78.10.6324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Clutton-Brock Tim. Breeding together: kin selection and mutualism in cooperative vertebrates. Science. 2002 Apr 5;296(5565):69–72. doi: 10.1126/science.296.5565.69. [DOI] [PubMed] [Google Scholar]
  6. Crespi B. J. The evolution of social behavior in microorganisms. Trends Ecol Evol. 2001 Apr 1;16(4):178–183. doi: 10.1016/s0169-5347(01)02115-2. [DOI] [PubMed] [Google Scholar]
  7. Kaiser D. Social gliding is correlated with the presence of pili in Myxococcus xanthus. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5952–5956. doi: 10.1073/pnas.76.11.5952. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Kroos L., Kuspa A., Kaiser D. A global analysis of developmentally regulated genes in Myxococcus xanthus. Dev Biol. 1986 Sep;117(1):252–266. doi: 10.1016/0012-1606(86)90368-4. [DOI] [PubMed] [Google Scholar]
  9. Kuspa A., Plamann L., Kaiser D. A-signalling and the cell density requirement for Myxococcus xanthus development. J Bacteriol. 1992 Nov;174(22):7360–7369. doi: 10.1128/jb.174.22.7360-7369.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. O'Connor K. A., Zusman D. R. Behavior of peripheral rods and their role in the life cycle of Myxococcus xanthus. J Bacteriol. 1991 Jun;173(11):3342–3355. doi: 10.1128/jb.173.11.3342-3355.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. O'Connor K. A., Zusman D. R. Development in Myxococcus xanthus involves differentiation into two cell types, peripheral rods and spores. J Bacteriol. 1991 Jun;173(11):3318–3333. doi: 10.1128/jb.173.11.3318-3333.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Shimkets L. J., Asher S. J. Use of recombination techniques to examine the structure of the csg locus of Myxococcus xanthus. Mol Gen Genet. 1988 Jan;211(1):63–71. doi: 10.1007/BF00338394. [DOI] [PubMed] [Google Scholar]
  13. Shimkets L. J. Intercellular signaling during fruiting-body development of Myxococcus xanthus. Annu Rev Microbiol. 1999;53:525–549. doi: 10.1146/annurev.micro.53.1.525. [DOI] [PubMed] [Google Scholar]
  14. Shimkets L., Woese C. R. A phylogenetic analysis of the myxobacteria: basis for their classification. Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9459–9463. doi: 10.1073/pnas.89.20.9459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Strassmann J. E., Zhu Y., Queller D. C. Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature. 2000 Dec 21;408(6815):965–967. doi: 10.1038/35050087. [DOI] [PubMed] [Google Scholar]
  16. Turner P. E., Chao L. Prisoner's dilemma in an RNA virus. Nature. 1999 Apr 1;398(6726):441–443. doi: 10.1038/18913. [DOI] [PubMed] [Google Scholar]
  17. Velicer G. J., Kroos L., Lenski R. E. Developmental cheating in the social bacterium Myxococcus xanthus. Nature. 2000 Apr 6;404(6778):598–601. doi: 10.1038/35007066. [DOI] [PubMed] [Google Scholar]
  18. Velicer Gregory J., Lenski Richard E., Kroos Lee. Rescue of social motility lost during evolution of Myxococcus xanthus in an asocial environment. J Bacteriol. 2002 May;184(10):2719–2727. doi: 10.1128/JB.184.10.2719-2727.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Vulic M., Kolter R. Evolutionary cheating in Escherichia coli stationary phase cultures. Genetics. 2001 Jun;158(2):519–526. doi: 10.1093/genetics/158.2.519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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. 1999 Jan;181(1):24–33. doi: 10.1128/jb.181.1.24-33.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Wedekind Claus, Braithwaite Victoria A. The long-term benefits of human generosity in indirect reciprocity. Curr Biol. 2002 Jun 25;12(12):1012–1015. doi: 10.1016/s0960-9822(02)00890-4. [DOI] [PubMed] [Google Scholar]
  22. West Stuart A., Buckling Angus. Cooperation, virulence and siderophore production in bacterial parasites. Proc Biol Sci. 2003 Jan 7;270(1510):37–44. doi: 10.1098/rspb.2002.2209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Wireman J. W., Dworkin M. Developmentally induced autolysis during fruiting body formation by Myxococcus xanthus. J Bacteriol. 1977 Feb;129(2):798–802. doi: 10.1128/jb.129.2.798-802.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES