The multiplicity of divergence mechanisms in a single evolving population

Genome Biology

Volumn 13, Issue 6, 2012, Pages

  Maharjan, Ram P ^a   Ferenci, Thomas ^a   Reeves, Peter R ^a   Li, Yang ^b,c   Liu, Bin ^b,c   Wang, Lei ^b,c  

^a UNIVERSITY OF SYDNEY   (Australia)

^b NANKAI UNIVERSITY   (China)

^c BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL MUTATION; BACTERIUM CULTURE; CONTROLLED STUDY; DIVERSIFYING SELECTION; ESCHERICHIA COLI; EVOLUTION; FITNESS; GROWTH RATE; MICROBIAL POPULATION DYNAMICS; NONHUMAN; PHENOTYPIC VARIATION; PLEIOTROPY; SEQUENCE ANALYSIS;

EID: 84861930803     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2012-13-6-r41     Document Type: Article

References (74)

1. Feil EJ: Small change: keeping pace with microevolution. Nat Rev Microbiol 2004, 2: 483-495.
2. Wirth T, Falush D, Lan RT, Colles F, Mensa P, Wieler LH, Karch H, Reeves PR, Maiden MCJ, Ochman H, Achtman M: Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 2006, 60: 1136-1151.
3. Levert M, Zamfir O, Clermont O, Bouvet O, Lespinats S, Hipeaux M, Branger C, Picard B, Saint-Ruf C, Norel F, Balliau T, Zivy M, Le Nagard H, Cruvellier S, Chane-Woon-Ming B, Nilsson S, Gudelj I, Phan K, Ferenci T, Tenaillon O, Denamur E: Molecular and evolutionary bases of withinpatient genotypic and phenotypic diversity in Escherichia coli extraintestinal infections. PLoS Path 2010, 6: e1001125.
4. Hardin G: Competitive exclusion principle. Science 1960, 131: 1292-1297.
5. Kassen R, Rainey PB: The ecology and genetics of microbial diversity. Annu Rev Microbiol 2004, 58: 207-231.
6. Maharjan R, Seeto S, Notley-McRobb L, Ferenci T: Clonal adaptive radiation in a constant environment. Science 2006, 313: 514-517.
7. Gresham D, Desai MM, Tucker CM, Jenq HT, Pai DA, Ward A, DeSevo CG, Botstein D, Dunham MJ: The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genet 2008, 4: e1000303.
8. Kinnersley MA, Holben WE, Rosenzweig F: E Unibus Plurum: genomic analysis of an experimentally evolved polymorphism in Escherichia coli. PLoS Genet 2009, 5: e1000713.
9. Levin BR: Frequency dependent selection in bacterial populations. Phil Trans R Soc B 1988, 319: 459-472.
10. Doebeli M, Ispolatov I: Complexity and diversity. Science 2010, 328: 494-497.
11. Friesen ML, Saxer G, Travisano M, Doebeli M: Experimental evidence for sympatric ecological diversification due to frequency-dependent competition in Escherichia coli. Evolution 2004, 58: 245-260.
12. Rosenzweig RF, Sharp RR, Treves DS, Adams J: Microbial evolution in a simple unstructured environment: Genetic differentiation in Escherichia coli. Genetics 1994, 137: 903-917.
13. Gudelj I, Weitz JS, Ferenci T, Horner-Devine MC, Marx CJ, Meyer JR, Forde SE: An integrative approach to understanding microbial diversity: from intracellular mechanisms to community structure. Ecol Lett 2010, 13: 1073-1084.
14. Beardmore RE, Gudelj I, Lipson DA, Hurst LD: Metabolic trade-offs and the maintenance of the fittest and the flattest. Nature 2011, 472: 342-346.
15. Zhang X-S, Hill WG: Genetic variability under mutation selection balance. Trends Ecol Evol 2005, 20: 468-470.
16. Desai MM, Fisher DS: Beneficial mutation selection balance and the effect of linkage on positive selection. Genetics 2007, 176: 1759-1798.
17. Wang L, Spira B, Zhou ZM, Feng L, Maharjan RP, Li XM, Li FF, McKenzie C, Reeves PR, Ferenci T: Divergence involving global regulatory gene mutations in an Escherichia coli population evolving under phosphate limitation. Genome Biol Evol 2010, 2: 478-487.
18. Conrad TM, Lewis NE, Palsson BO: Microbial laboratory evolution in the era of genome-scale science. Mol Syst Biol 2011, 7: 509-509.
19. Elena SF, Lenski RE: Evolution experiments with microorganisms: The dynamics and genetic bases of adaptation. Nat Rev Genet 2003, 4: 457-469.
20. Barrick JE, Lenski RE: Genome-wide mutational diversity in an evolving population of Escherichia coli. Cold Spring Harb Symp Quant Biol 2009, 74: 119-129.
21. Conrad TM, Joyce AR, Applebee MK, Barrett CL, Xie B, Gao Y, Palsson BO: Whole-genome resequencing of Escherichia coli K-12 MG1655 undergoing short-term laboratory evolution in lactate minimal media reveals flexible selection of adaptive mutations. Genome Biol 2009, 10: R118.
22. Brockhurst MA, Rainey PB, Buckling A: The effect of spatial heterogeneity and parasites on the evolution of host diversity. Proc R Soc Lond Ser BBiol Sci 2004, 271: 107-111.
23. Kerr B, Riley MA, Feldman MW, Bohannan BJM: Local dispersal promotes biodiversity in a real-life game of rock-paper-scissors. Nature 2002, 418: 171-174.
24. Rainey PB, Travisano M: Adaptive radiation in a heterogeneous environment. Nature 1998, 394: 69-72.
25. Barrett RDH, MacLean RC, Bell G: Experimental evolution of Pseudomonas fluorescens in simple and complex environments. Am Nat 2005, 166: 470-480.
26. Habets M, Rozen DE, Hoekstra RF, de Visser J: The effect of population structure on the adaptive radiation of microbial populations evolving in spatially structured environments. Ecol Lett 2006, 9: 1041-1048.
27. Tyerman J, Havard N, Saxer G, Travisano M, Doebeli M: Unparallel diversification in bacterial microcosms. Proc R Soc B Biol Sci 2005, 272: 1393-1398.
28. Rozen DE, Philippe N, Arjan de Visser J, Lenski RE, Schneider D: Death and cannibalism in a seasonal environment facilitate bacterial coexistence. Ecol Lett 2009, 12: 34-44.
29. Crozat E, Hindre T, Kuhn L, Garin J, Lenski RE, Schneider D: Altered regulation of the OmpF porin by Fis in Escherichia coli during an evolution experiment and between B and K-12 strains. J Bacteriol 2011, 193: 429-440.
30. Philippe N, Crozat E, Lenski RE, Schneider D: Evolution of global regulatory networks during a long-term experiment with Escherichia coli. Bioessays 2007, 29: 846-860.
31. Sniegowski PD, Gerrish PJ, Lenski RE: Evolution of high mutation rates in experimental populations of E. coli. Nature 1997, 387: 703-705.
32. Notley-McRobb L, Seeto S, Ferenci T: Enrichment and elimination of mutY mutators in Escherichia coli populations. Genetics 2002, 162: 1055-1062.
33. Maharjan R, Seeto S, Ferenci T: Divergence and redundancy of transport and metabolic rate-yield strategies in a single Escherichia coli population. J Bacteriol 2007, 189: 2350-2358.
34. Ferenci T: Maintaining a healthy SPANC balance through regulatory and mutational adaptation. Mol Microbiol 2005, 57: 1-8.
35. Notley-McRobb L, Seeto S, Ferenci T: The influence of cellular physiology on the initiation of mutational pathways in Escherichia coli populations. Proc R Soc Lond Ser B Biol Sci 2003, 270: 843-848.
36. Ferenci T, Zhou ZM, Betteridge T, Ren Y, Liu Y, Feng L, Reeves PR, Wang L: Genomic sequencing reveals regulatory mutations and recombinational events in the widely used MC4100 lineage of Escherichia coli K-12. J Bacteriol 2009, 191: 4025-4029.
37. Gaffe J, McKenzie C, Maharjan RP, Coursange E, Ferenci T, Schneider D: Insertion sequence-driven evolution of Escherichia coli in chemostats. J Mol Evol 2011, 72: 398-412.
38. Miller JH: Spontaneous mutators in bacteria-insights into pathways of mutagenesis and repair. Annu Rev Microbiol 1996, 50: 625-643.
39. Ng PC, HenikoffS: SIFT: predicting amino acid changes that affect protein function. Nucleic Acids Res 2003, 31: 3812-3814.
40. Herring CD, Raghunathan A, Honisch C, Patel T, Applebee MK, Joyce AR, Albert TJ, Blattner FR, van den Boom D, Cantor CR, Palsson BO: Comparative genome sequencing of Escherichia coli allows observation of bacterial evolution on a laboratory timescale. Nat Genet 2006, 38: 1406-1412.
41. Barrick JE, Yu DS, Yoon SH, Jeong H, Oh TK, Schneider D, Lenski RE, Kim JF: Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 2009, 461: 1243-U1274.
42. Ochman H: Neutral mutations and neutral substitutions in bacterial genomes. Mol Biol Evol 2003, 20: 2091-2096.
43. Chen JQ, Wu Y, Yang HW, Bergelson J, Kreitman M, Tian DC: Variation in the ratio of nucleotide substitution and indel rates across genomes in mammals and bacteria. Mol Biol Evol 2009, 26: 1523-1531.
44. Drake JW, Charlesworth B, Charlesworth D, Crow JF: Rates of spontaneous mutation. Genetics 1998, 148: 1667-1686.
45. Rozen DE, de Visser J, Gerrish PJ: Fitness effects of fixed beneficial mutations in microbial populations. Curr Biol 2002, 12: 1040-1045.
46. de Visser JAGM, Zeyl CW, Gerrish PJ, Blanchard JL, Lenski RE: Diminishing returns from mutation supply rate in asexual populations. Science 1999, 283: 404-406.
47. Blatter EE, Ross W, Tang H, Gourse RL, Ebright RH: Domain organization of RNA polymerase alpha subunit: C-terminal 85 amino acids constitute a domain capable of dimerization and DNA binding. Cell 1994, 78: 889-896.
48. Maharjan R, Zhou ZM, Ren Y, Li Y, Gaffe J, Schneider D, McKenzie C, Reeves PR, Ferenci T, Wang L: Genomic identification of a novel mutation in hfq that provides multiple benefits in evolving glucose-limited populations of Escherichia coli. J Bacteriol 2010, 192: 4517-4521.
49. Notley-McRobb L, Ferenci T: The generation of multiple coexisting malregulatory mutations through polygenic evolution in glucose-limited populations of Escherichia coli. Environ Microbiol 1999, 1: 45-52.
50. Maharjan R, McKenzie C, Yeung A, Ferenci T: The basis of antagonistic pleiotropy in hfq mutations that have opposite effects on fitness at slow and fast growth rates. Heredity 2012.
51. Desai MM, Fisher DS, Murray AW: The speed of evolution and maintenance of variation in asexual populations. Curr Biol 2007, 17: 385-394.
52. Perfeito L, Fernandes L, Mota C, Gordo I: Adaptive mutations in bacteria: High rate and small effects. Science 2007, 317: 813-815.
53. Kao KC, Sherlock G: Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nat Genet 2008, 40: 1499-1504.
54. Gualdi L, Tagliabue L, Landini P: Biofilm formation-gene expression relay system in Escherichia coli: Modulation of sigma(s)-dependent gene expression by the CsgD regulatory protein via sigma(s) protein stabilization. J Bacteriol 2007, 189: 8034-8043.
55. White AP, Weljie AM, Apel D, Zhang P, Shaykhutdinov R, Vogel HJ, Surette MG: A Global metabolic shift is linked to Salmonella multicellular development. PLoS ONE 2010, 5: e11814.
56. Becker G, Klauck E, Hengge-Aronis R: The response regulator RssB, a recognition factor for sigma(s) proteolysis in Escherichia coli, can act like an anti-sigma(s) factor. Mol Microbiol 2000, 35: 657-666.
57. Tenaillon O, Rodriguez-Verdugo A, Gaut RL, McDonald P, Bennett AF, Long AD, Gaut BS: The molecular diversity of adaptive convergence. Science 2012, 335: 457-461.
58. Ferenci T: Bacterial physiology, regulation and mutational adaptation in a chemostat environment. Adv Microb Physiol 2007, 53: 169-229.
59. Doebeli N: A model for the evolutionary dynamics of cross-feeding polymorphisms in microorganisms. Popul Ecol 2002, 44: 59-70.
60. Dykhuizen DE, Dean AM: Evolution of specialists in an experimental microcosm. Genetics 2004, 167: 2015-2026.
61. Park SC, Krug J: Clonal interference in large populations. Proc Natl Acad Sci USA 2007, 104: 18135-18140.
62. Gudelj I, Beardmore RE, Arkin SS, Maclean RC: Constraints on microbial metabolism drive evolutionary diversification in homogeneous environments. J Evol Biol 2007, 20: 1882-1889.
63. Pfeiffer T, Schuster S, Bonhoeffer S: Cooperation and competition in the evolution of ATP-producing pathways. Science 2001, 292: 504-507.
64. Novak M, Pfeiffer T, Lenski RE, Sauer U, Bonhoeffer S: Experimental tests for an evolutionary trade-offbetween growth rate and yield in E. coli. Am Nat 2006, 168: 242-251.
65. King T, Ishihama A, Kori A, Ferenci T: A regulatory trade-offas a source of strain variation in the species Escherichia coli. J Bacteriol 2004, 186: 5614-5620.
66. Ferenci T: Regulation by nutrient limitation. Curr Opin Microbiol 1999, 2: 208-213.
67. Notley L, Ferenci T: Differential expression of mal genes under cAMP and endogenous inducer control in nutrient stressed Escherichia coli. Mol Microbiol 1995, 16: 121-129.
68. Notley-McRobb L, Ferenci T: Substrate specificity and signal transduction pathways in the glucose-specific enzyme II (EIIGlc) component of the Escherichia coli phosphotransferase system. J Bacteriol 2000, 182: 4437-4442.
69. Hammer O, Harper DAT, Ryan PD: PAST: Palaeontological Statistics software package for education and data analysis. Palaeontologica Electronica 2001, 4, Article 4.
70. Li H, Durbin R: Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25: 1754-1760.
71. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R: The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25: 2078-2079.
72. Bentley DR, Balasubramanian S, Swerdlow HP, Smith GP, Milton J, Brown CG, Hall KP, Evers DJ, Barnes CL, Bignell HR, Boutell JM, Bryant J, Carter RJ, Cheetham RK, Cox AJ, Ellis DJ, Flatbush MR, Gormley NA, Humphray SJ, Irving LJ, Karbelashvili MS, Kirk SM, Li H, Liu XH, Maisinger KS, Murray LJ, Obradovic B, Ost T, Parkinson ML, Pratt MR, et al: Accurate whole human genome sequencing using reversible terminator chemistry. Nature 2008, 456: 53-59.
73. Dykhuizen DE, Hartl DE: Selection in chemostats. Microbiol Rev 1983, 47: 150-168.
74. Tatusov RL, Koonin EV, Lipman DJ: A genomic perspective on protein families. Science 1997, 278: 631-637.