Evolution by flight and fight: Diverse mechanisms of adaptation by actively motile microbes

ISME Journal

Volumn 11, Issue 2, 2017, Pages 555-568

  Rendueles, Olaya ^a,b   Velicer, Gregory J ^a  

^a ETH ZURICH   (Switzerland)

^b INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; ANCESTRY; BACTERIUM; EVOLUTIONARY BIOLOGY; FITNESS; INTERFERENCE COMPETITION; INTERSPECIFIC INTERACTION; MOTILITY; NATURAL SELECTION; PHENOTYPE; SWARMING;

BACTERIA (MICROORGANISMS); MYXOCOCCUS XANTHUS;

ADAPTATION; EVOLUTION; GENETICS; LOCOMOTION; MYXOCOCCUS XANTHUS; PHENOTYPE; PHYSIOLOGY;

ADAPTATION, PHYSIOLOGICAL; BIOLOGICAL EVOLUTION; LOCOMOTION; MYXOCOCCUS XANTHUS; PHENOTYPE;

EID: 84988578976     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2016.115     Document Type: Article

References (75)

1. Angst DC, Hall AR. (2013). The cost of antibiotic resistance depends on evolutionary history in Escherichia coli. BMC Evol Biol 13.
2. Bailey SF, Kassen R. (2012). Spatial structure of ecological opportunity drives adaptation in a bacterium. Am Nat 180: 270-283.
3. Blount ZD, Borland CZ, Lenski RE. (2008). Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli. Proc Natl Acad Sci USA 105: 7899-7906.
4. Bowler DE, Benton TG. (2005). Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev C Phil Soc 80: 205-225.
5. Bull JJ, Badgett MR, Wichman HA, Huelsenbeck JP, Hillis DM, Gulati A, et al. (1997). Exceptional convergent evolution in a virus. Genetics 147: 1497-1507.
6. Caberoy NB, Welch RD, Jakobsen JS, Slater SC, Garza AG. (2003). Global mutational analysis of NtrC-like activators in Myxococcus xanthus: identifying activator mutants defective for motility and fruiting body development. J Bacteriol 185: 6083-6094.
7. Chao L, Levin BR. (1981). Structured habitats and the evolution of anticompetitor toxins in bacteria. Proc Natl Acad Sci USA 78: 6324-6328.
8. Chou HH, Chiu HC, Delaney NF, Segre D, Marx CJ. (2011). Diminishing returns epistasis among beneficial mutations decelerates adaptation. Science 332: 1190-1192.
9. Cornforth DM, Foster KR. (2013). Competition sensing: the social side of bacterial stress responses. Nat Rev Microbiol 11: 285-293.
10. Dettman JR, Rodrigue N, Melnyk AH, Wong A, Bailey SF, Kassen R. (2012). Evolutionary insight from wholegenome sequencing of experimentally evolved microbes. Mol Ecol 21: 2058-2077.
11. Fong SS, Joyce AR, Palsson BO. (2005). Parallel adaptive evolution cultures of Escherichia coli lead to convergent growth phenotypes with different gene expression states. Genome Res 15: 1365-1372.
12. Goldman BS, Nierman WC, Kaiser D, et al. (2006). Evolution of sensory complexity recorded in a myxobacterial genome. Proc Natl Acad Sci USA 103: 15200-15205.
13. Hall AR, Griffiths VF, MacLean RC, Colegrave N. (2010). Mutational neighbourhood and mutation supply rate constrain adaptation in Pseudomonas aeruginosa. Proc Bio Sci R Soc 277: 643-650.
14. Hibbing ME, Fuqua C, Parsek MR, Peterson SB. (2010). Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 8: 15-25.
15. Hillesland KL, Velicer GJ. (2005). Resource level affects relative performance of the two motility systems of Myxococcus xanthus. Microb Ecol 49: 558-566.
16. Hodgkin J, Kaiser D. (1979). Genetics of gliding motility on Myxococcus xanthus (myxobacteriales)-Two gene systems control movement. Mol Gen Genet 171: 177-191.
17. Holder KK, Bull JJ. (2001). Profiles of adaptation in two similar viruses. Genetics 159: 1393-1404.
18. Huang Y, Wright SI, Agrawal AF. (2014). Genome-wide patterns of genetic variation within and among alternative selective regimes. PLoS Genet 10: e1004527.
19. Josenhans C, Suerbaum S. (2002). The role of motility as a virulence factor in bacteria. Int J Med Microbiol 291: 605-614.
20. Kaimer C, Berleman JE, Zusman DR. (2012). Chemosensory signaling controls motility and subcellular polarity in Myxococcus xanthus. Curr Opin Microbiol 15: 751-757.
21. Kaiser D. (1979). Social gliding is correlated with the presence of pili in Myxococcus xanthus. Proc Natl Acad Sci USA 76: 5952-5956.
22. Kawecki TJ, Lenski RE, Ebert D, Hollis B, Olivieri I, Whitlock MC. (2012). Experimental evolution. Trends Ecol Evol 27: 547-560.
23. Kearns DB. (2013). You get what you select for: better swarming through more flagella. Trends Microbiol 21: 508-509.
24. Korona R. (1996). Adaptation to structurally different environments. P Roy Soc B Biol Sci 263: 1665-1669.
25. Korona R. (1996). Genetic divergence and fitness convergence under uniform selection in experimental populations of bacteria. Genetics 143: 637-644.
26. Korona R, Nakatsu CH, Forney LJ, Lenski RE. (1994). Evidence for multiple adaptive peaks from populations of bacteria evolving in a structured habitat. Proc Natl Acad Sci USA 91: 9037-9041.
27. Kraemer SA, Velicer GJ. (2011). Endemic social diversity within natural kin groups of a cooperative bacterium. Proc Natl Acad Sci USA 108: 10823-10830.
28. Kvitek DJ, Sherlock G. (2011). Reciprocal sign epistasis between frequently experimentally evolved adaptive mutations causes a rugged fitness landscape. PLoS Genet 7: e1002056.
29. Lemonnier M, Levin BR, Romeo T, Garner K, Baquero MR, Mercante J, et al. (2008). The evolution of contactdependent inhibition in non-growing populations of Escherichia coli. Proc Bio Sci R Soc 275: 3-10.
30. MacLean RC, Bell G. (2003). Divergent evolution during an experimental adaptive radiation. Proc Bio Sci R Soc 270: 1645-1650.
31. Magsig-Castillo J, Morse JG, Walker GP, Bi JL, Rugman-Jones PF, Stouthamer R. (2010). Phoretic dispersal of armored scale crawlers (Hemiptera: Diaspididae). J Econ Entom 103: 1172-1179.
32. Melnyk AH, Kassen R. (2011). Adaptive landscapes in evolving populations of Pseudomonas fluorescens. Evolution 65: 3048-3059.
33. Mignot T, Shaevitz JW, Hartzell PL, Zusman DR. (2007). Evidence that focal adhesion complexes power bacterial gliding motility. Science 315: 853-856.
34. Mitri S, Foster KR. (2013). The genotypic view of social interactions in microbial communities. Annu Rev Genet 47: 247-273.
35. Ottemann KM, Miller JF. (1997). Roles for motility in bacterial-host interactions. Mol Microbiol 24: 1109-1117.
36. Phillips PC. (2008). Epistasis-The essential role of gene interactions in the structure and evolution of genetic systems. Nat Rev Genet 9: 855-867.
37. Pratt LA, Kolter R. (1998). Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol Microbiol 30: 285-293.
38. Rebolleda-Gomez M, Ratcliff W, Travisano M. (2012). Adaptation and divergence during experimental evolution of multicellular Saccharomyces cerevisiae. Artif Life 13: 99-104.
39. Rendueles O, Zee PC, Dinkelacker I, Amherd M, Wielgoss S, Velicer GJ. (2015). Rapid and widespread de novo evolution of kin discrimination. Proc Natl Acad Sci USA 112: 9076-9081.
40. Reynolds AM, Bohan DA, Bell JR. (2006). Ballooning dispersal in arthropod taxa with convergent behaviours: dynamic properties of ballooning silk in turbulent flows. Biol Lett 2: 371-373.
41. Riley MS, Cooper VS, Lenski RE, Forney LJ, Marsh TL. (2001). Rapid phenotypic change and diversification of a soil bacterium during 1000 generations of experimental evolution. Microbiology 147: 995-1006.
42. Rodriguez AM, Spormann AM. (1999). Genetic and molecular analysis of cglB, a gene essential for singlecell gliding in Myxococcus xanthus. J Bacteriol 181: 4381-4390.
43. Shi W, Zusman DR. (1993). The two motility systems of Myxococcus xanthus show different selective advantages on various surfaces. Proc Natl Acad Sci USA 90: 3378-3382.
44. Spor A, Kvitek DJ, Nidelet T, Martin J, Legrand J, Dillmann C, et al. (2014). Phenotypic and genotypic convergences are influenced by historical contingency and environment in yeast. Evolution 68: 772-790.
45. Stocker R, Seymour JR, Samadani A, Hunt DE, Polz MF. (2008). Rapid chemotactic response enables marine bacteria to exploit ephemeral microscale nutrient patches. Proc Natl Acad Sci USA 105: 4209-4214.
46. Sun H, Zusman DR, Shi W. (2000). Type IV pilus of Myxococcus xanthus is a motility apparatus controlled by the frz chemosensory system. Curr Biol 10: 1143-1146.
47. Sun M, Wartel M, Cascales E, Shaevitz JW, Mignot T. (2011). Motor-driven intracellular transport powers bacterial gliding motility. Proc Natl Acad Sci USA 108: 7559-7564.
48. Swingland IR, Greenwood PJ. (1983). The Ecology of Animal Movement. Oxford University Press: New York, NY, USA.
49. Tatusov RL, Galperin MY, Natale DA, Koonin EV. (2000). The COG database: a tool for genome-scale analysis of protein functions and evolution. NAR 28: 33-36.
50. Taylor JR, Stocker R. (2012). Trade-offs of chemotactic foraging in turbulent water. Science 338: 675-679.
51. Taylor TB, Buckling A. (2011). Selection experiments reveal trade-offs between swimming and twitching motilities in Pseudomonas aeruginosa. Evolution 65: 3060-3069.
52. Taylor TB, Buckling A. (2013). Bacterial motility confers fitness advantage in the presence of phages. J Evol Biol 26: 2154-2160.
53. Tenaillon O, Rodriguez-Verdugo A, Gaut RL, McDonald P, Bennett AF, Long AD, et al. (2012). The molecular diversity of adaptive convergence. Science 335: 457-461.
54. Teseo S, Chaline N, Jaisson P, Kronauer DJ. (2014). Epistasis between adults and larvae underlies caste fate and fitness in a clonal ant. Nat Commun 5: 3363.
55. Travisano M, Velicer GJ. (2004). Strategies of microbial cheater control. Trends Microbiol 12: 72-78.
56. Travisano M, Mongold JA, Bennett AF, Lenski RE. (1995). Experimental tests of the roles of adaptation, chance, and history in evolution. Science 267: 87-90.
57. Turnbull GA, Morgan JA, Whipps JM, Saunders JR. (2001). The role of bacterial motility in the survival and spread of Pseudomonas fluorescens in soil and in the attachment and colonisation of wheat roots. FEMS Microbiol Ecol 36: 21-31.
58. Tyerman J, Havard N, Saxer G, Travisano M, Doebeli M. (2005). Unparallel diversification in bacterial microcosms. Proc Bio Sci R Soc 272: 1393-1398.
59. van Ditmarsch D, Boyle KE, Sakhtah H, Oyler JE, Nadell CD, Deziel E, et al. (2013). Convergent evolution of hyperswarming leads to impaired biofilm formation in pathogenic bacteria. Cell Rep 4: 697-708.
60. Vasi F, Travisano M, Lenski RE. (1994). Long-Term experimental evolution in Escherichia coli 2. Changes in life-history traits during adaptation to a seasonal environment. Am Nat 144: 432-456.
61. Velicer GJ, Yu YT. (2003). Evolution of novel cooperative swarming in the bacterium Myxococcus xanthus. Nature 425: 75-78.
62. Velicer GJ, Vos M. (2009). Sociobiology of the myxobacteria. Annu Rev Microbiol 63: 599-623.
63. Velicer GJ, Kroos L, Lenski RE. (1998). Loss of social behaviors by Myxococcus xanthus during evolution in an unstructured habitat. Proc Natl Acad Sci USA 95: 12376-12380.
64. Vogwill T, Kojadinovic M, Furio V, MacLean RC. (2014). Testing the role of genetic background in parallel evolution Using the comparative experimental evolution of antibiotic resistance. Mol Biol Evol 31: 3314-3323.
65. Vos M, Velicer GJ. (2008). Natural variation of gliding motility in a centimetre-scale population of Myxococcus xanthus. FEMS Microbiol Ecol 64: 343-350.
66. Wielgoss S, Didelot X, Chaudhuri RR, Liu X, Weedall GD, Velicer GJ, et al. (2016). A barrier to homologous recombination between sympatric strains of the cooperative soil bacterium Myxococcus xanthus. ISME J; e-pub ahead of print 5 April 2016; doi:10.1038/ismej.2016.34.
67. Wloch-Salamon DM, Gerla D, Hoekstra RF, de Visser JA. (2008). Effect of dispersal and nutrient availability on the competitive ability of toxin-producing yeast. Proc Bio Sci R Soc 275: 535-541.
68. Wolf JB, Brodie ED, M.J. W. (2000). Epistasis and the evolutionary process. Oxford University Press: New York, NY, USA.
69. Wu SS, Kaiser D. (1995). Genetic and functional evidence that Type IV pili are required for social gliding motility in Myxococcus xanthus. Mol Microbiol 18: 547-558.
70. Wu SS, Kaiser D. (1997). Regulation of expression of the pilA gene in Myxococcus xanthus. J Bacteriol 179: 7748-7758.
71. Youderian P, Hartzell PL. (2006). Transposon insertions of magellan-4 that impair social gliding motility in Myxococcus xanthus. Genetics 172: 1397-1410.
72. Youderian P, Burke N, White DJ, Hartzell PL. (2003). Identification of genes required for adventurous gliding motility in Myxococcus xanthus with the transposable element mariner. Mol Microbiol 49: 555-570.
73. Young IM, Crawford JW. (2004). Interactions and selforganization in the soil-microbe complex. Science 304: 1634-1637.
74. Zhang H, Travisano M. (2006). Predicting fitness effects of beneficial mutations in digital organisms. Ieee Symp Art Life, 39-46.
75. Zusman DR, Scott AE, Yang Z, Kirby JR. (2007). Chemosensory pathways, motility and development in Myxococcus xanthus. Nat Rev Microbiol 5: 862-872.