Positively Frequency-Dependent Interference Competition Maintains Diversity and Pervades a Natural Population of Cooperative Microbes

Current Biology

Volumn 25, Issue 13, 2015, Pages 1673-1681

  Rendueles, Olaya ^a   Amherd, Michaela ^a   Velicer, Gregory J ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

allelopathy; frequency dependence; mutual antagonism; social evolution; territoriality

Indexed keywords

BACTERIA (MICROORGANISMS); MYXOCOCCUS XANTHUS;

ANTIBIOSIS; BIODIVERSITY; GENETIC SELECTION; MYXOCOCCUS XANTHUS; ORGANISMAL INTERACTION; PHYSIOLOGY; POPULATION DENSITY; SPECIES DIFFERENCE;

ANTIBIOSIS; BIODIVERSITY; MICROBIAL INTERACTIONS; MYXOCOCCUS XANTHUS; POPULATION DENSITY; SELECTION, GENETIC; SPECIES SPECIFICITY;

EID: 84937526278     PISSN: 09609822     EISSN: 18790445     Source Type: Journal    
DOI: 10.1016/j.cub.2015.04.057     Document Type: Article

References (60)

1. L.F. Roesch, R.R. Fulthorpe, A. Riva, G. Casella, A.K.M. Hadwin, A.D. Kent, S.H. Daroub, F.A.O. Camargo, W.G. Farmerie, and E.W. Triplett Pyrosequencing enumerates and contrasts soil microbial diversity ISME J. 1 2007 283 290
2. I.M. Young, and J.W. Crawford Interactions and self-organization in the soil-microbe complex Science 304 2004 1634 1637
3. O.X. Cordero, and M.F. Polz Explaining microbial genomic diversity in light of evolutionary ecology Nat. Rev. Microbiol. 12 2014 263 273
4. M. Vos, A.B. Wolf, S.J. Jennings, and G.A. Kowalchuk Micro-scale determinants of bacterial diversity in soil FEMS Microbiol. Rev. 37 2013 936 954
5. P.B. Rainey, and M. Travisano Adaptive radiation in a heterogeneous environment Nature 394 1998 69 72
6. M. Bressan, C. Mougel, S. Dequiedt, P.A. Maron, P. Lemanceau, and L. Ranjard Response of soil bacterial community structure to successive perturbations of different types and intensities Environ. Microbiol. 10 2008 2184 2187
7. P.B. Rainey, A. Buckling, R. Kassen, and M. Travisano The emergence and maintenance of diversity: insights from experimental bacterial populations Trends Ecol. Evol. 15 2000 243 247
8. J.W. Crawford, L. Deacon, D. Grinev, J.A. Harris, K. Ritz, B.K. Singh, and I. Young Microbial diversity affects self-organization of the soil-microbe system with consequences for function J. R. Soc. Interface 9 2012 1302 1310
9. R. Bürger, and A. Gimelfarb The effects of intraspecific competition and stabilizing selection on a polygenic trait Genetics 167 2004 1425 1443
10. P. Chesson General theory of competitive coexistence in spatially-varying environments Theor. Popul. Biol. 58 2000 211 237
11. M.L. Rosenzweig Competitive speciation Biol. J. Linn. Soc. Lond. 10 1978 275 289
12. A. Ross-Gillespie, A. Gardner, S.A. West, and A.S. Griffin Frequency dependence and cooperation: theory and a test with bacteria Am. Nat. 170 2007 331 342
13. M.J. Eppstein, J.D. Bever, and J. Molofsky Spatio-temporal community dynamics induced by frequency dependent interactions Ecol. Modell. 197 2006 133 147
14. B.R. Levin Frequency-dependent selection in bacterial populations Philos. Trans. R. Soc. Lond. B Biol. Sci. 319 1988 459 472
15. F.B. Christiansen Frequency dependence and competition Philos. Trans. R. Soc. Lond. B Biol. Sci. 319 1988 587 600
16. J.D. Bever Dynamics within mutualism and the maintenance of diversity: inference from a model of interguild frequency dependence Ecol. Lett. 2 1999 52 62
17. R.E. Lenski, and S.E. Hattingh Coexistence of two competitors on one resource and one inhibitor: a chemostat model based on bacteria and antibiotics J. Theor. Biol. 122 1986 83 93
18. J. Molofsky, and J.D. Bever A novel theory to explain species diversity in landscapes: positive frequency dependence and habitat suitability Proc. Biol. Sci. 269 2002 2389 2393
19. G.J. Velicer, L. Kroos, and R.E. Lenski Developmental cheating in the social bacterium Myxococcus xanthus Nature 404 2000 598 601
20. L.D.B. Gigord, M.R. Macnair, and A. Smithson Negative frequency-dependent selection maintains a dramatic flower color polymorphism in the rewardless orchid Dactylorhiza sambucina (L.) Soo Proc. Natl. Acad. Sci. USA 98 2001 6253 6255
21. Y. Takahashi, and M. Kawata A comprehensive test for negative frequency-dependent selection Popul. Ecol. 55 2013 499 509
22. D.E. Rozen, and R.E. Lenski Long-term experimental evolution in Escherichia coli. VIII. Dynamics of a balanced polymorphism Am. Nat. 155 2000 24 35
23. R. Levins Discussion paper: the qualitative analysis of partially specified systems Ann. N Y Acad. Sci. 231 1974 123 138
24. R. May Stability and Complexity in Model Ecosystems 1974 Princeton University Press
25. S.A. Frank Spatial polymorphism of bacteriocins and other allelopathic traits Evol. Ecol. 8 1994 369 386
26. M. Kimura, and T. Ohta Theoretical Aspects of Population Genetics 1971 Princeton University Press
27. L. Chao, and B.R. Levin Structured habitats and the evolution of anticompetitor toxins in bacteria Proc. Natl. Acad. Sci. USA 78 1981 6324 6328
28. J. Molofsky, J.D. Bever, and J. Antonovics Coexistence under positive frequency dependence Proc. Biol. Sci. 268 2001 273 277
29. Y. Iwasa, M. Nakamaru, and S.A. Levin Allelopathy of bacteria in a lattice population: Competition between colicin-sensitive and colicin-producing strains Evol. Ecol. 12 1998 785 802
30. M.A. Riley, and J.E. Wertz Bacteriocins: evolution, ecology, and application Annu. Rev. Microbiol. 56 2002 117 137
31. M. Lemonnier, B.R. Levin, T. Romeo, K. Garner, M.R. Baquero, J. Mercante, E. Lemichez, F. Baquero, and J. Blázquez The evolution of contact-dependent inhibition in non-growing populations of Escherichia coli Proc. Biol. Sci. 275 2008 3 10
32. B. Kerr, M.A. Riley, M.W. Feldman, and B.J.M. Bohannan Local dispersal promotes biodiversity in a real-life game of rock-paper-scissors Nature 418 2002 171 174
33. E.M.F. Mauriello, T. Mignot, Z. Yang, and D.R. Zusman Gliding motility revisited: how do the myxobacteria move without flagella? Microbiol. Mol. Biol. Rev. 74 2010 229 249
34. M. Vos, and G.J. Velicer Natural variation of gliding motility in a centimetre-scale population of Myxococcus xanthus FEMS Microbiol. Ecol. 64 2008 343 350
35. A.D. Morgan, R.C. MacLean, K.L. Hillesland, and G.J. Velicer Comparative analysis of myxococcus predation on soil bacteria Appl. Environ. Microbiol. 76 2010 6920 6927
36. J.E. Berleman, and J.R. Kirby Deciphering the hunting strategy of a bacterial wolfpack FEMS Microbiol. Rev. 33 2009 942 957
37. R. Rajagopalan, Z. Sarwar, A.G. Garza, and L. Kroos Developmental gene regulation Z. Yang, P.I. Higgs, Myxobacteria: Genomics, Cellular and Molecular Biology 2013 Caister Academic Press
38. S.A. Kraemer, and G.J. Velicer Endemic social diversity within natural kin groups of a cooperative bacterium Proc. Natl. Acad. Sci. USA 108 Suppl 2 2011 10823 10830
39. S.A. Kraemer, M.A. Toups, and G.J. Velicer Natural variation in developmental life-history traits of the bacterium Myxococcus xanthus FEMS Microbiol. Ecol. 73 2010 226 233
40. D. Krug, G. Zurek, O. Revermann, M. Vos, G.J. Velicer, and R. Müller Discovering the hidden secondary metabolome of Myxococcus xanthus: a study of intraspecific diversity Appl. Environ. Microbiol. 74 2008 3058 3068
41. M. Vos, and G.J. Velicer Genetic population structure of the soil bacterium Myxococcus xanthus at the centimeter scale Appl. Environ. Microbiol. 72 2006 3615 3625
42. F. Fiegna, and G.J. Velicer Exploitative and hierarchical antagonism in a cooperative bacterium PLoS Biol. 3 2005 e370
43. M. Vos, and G.J. Velicer Social conflict in centimeter-and global-scale populations of the bacterium Myxococcus xanthus Curr. Biol. 19 2009 1763 1767
44. G.J. Velicer, and M. Vos Sociobiology of the myxobacteria Annu. Rev. Microbiol. 63 2009 599 623
45. A.E. Magurran Ecological Diversity and Its Measurements 1988 Princeton University Press
46. J.A. Allen, and M.E. Weale Anti-apostatic selection by wild birds on quasi-natural morphs of the land snail Cepaea hortensis: a generalised linear mixed models approach Oikos 108 2005 335 343
47. A. Faber, and K. Frenken Models in evolutionary economics and environmental policy: Towards an evolutionary environmental economics Technol. Forecast Soc. Change 76 2009 462 470
48. O. Hallatschek, P. Hersen, S. Ramanathan, and D.R. Nelson Genetic drift at expanding frontiers promotes gene segregation Proc. Natl. Acad. Sci. USA 104 2007 19926 19930
49. L. Dienes Reproductive processes in Proteus cultures J. Bacteriol. 51 1946 585
50. E.L. Munson, M.A. Pfaller, and G.V. Doern Modification of dienes mutual inhibition test for epidemiological characterization of Pseudomonas aeruginosa isolates J. Clin. Microbiol. 40 2002 4285 4288
51. J.E. Strassmann, O.M. Gilbert, and D.C. Queller Kin discrimination and cooperation in microbes Annu. Rev. Microbiol. 65 2011 349 367
52. D. Greig, and M. Travisano Density-dependent effects on allelopathic interactions in yeast Evolution 62 2008 521 527
53. B.T. Ho, T.G. Dong, and J.J. Mekalanos A view to a kill: the bacterial type VI secretion system Cell Host Microbe 15 2014 9 21
54. S. Koskiniemi, J.G. Lamoureux, K.C. Nikolakakis, C. t'Kint de Roodenbeke, M.D. Kaplan, D.A. Low, and C.S. Hayes Rhs proteins from diverse bacteria mediate intercellular competition Proc. Natl. Acad. Sci. USA 110 2013 7032 7037
55. S.K. Aoki, R. Pamma, A.D. Hernday, J.E. Bickham, B.A. Braaten, and D.A. Low Contact-dependent inhibition of growth in Escherichia coli Science 309 2005 1245 1248
56. P. Youderian, and P.L. Hartzell Triple mutants uncover three new genes required for social motility in Myxococcus xanthus Genetics 177 2007 557 566
57. A. Konovalova, T. Petters, and L. Søgaard-Andersen Extracellular biology of Myxococcus xanthus FEMS Microbiol. Rev. 34 2010 89 106
58. G.J. Velicer, H. Mendes-Soares, and S. Wielgoss Whence social diversity? Ecological and evolutionary analysis of the myxobacteria Z. Yang, P.I. Higgs, Myxobacteria: Genomics, Cellular and Molecular Biology 2014 Caister Academic Press
59. F. Fiegna, Y.T.N. Yu, S.V. Kadam, and G.J. Velicer Evolution of an obligate social cheater to a superior cooperator Nature 441 2006 310 314
60. Y.T.N. Yu, X. Yuan, and G.J. Velicer Adaptive evolution of an sRNA that controls Myxococcus development Science 328 2010 993