Parallel genetic and phenotypic evolution of DNA superhelicity in experimental populations of escherichia coli

Molecular Biology and Evolution

Volumn 27, Issue 9, 2010, Pages 2113-2128

  Crozat, Estelle ^a,b   Winkworth, Cynthia ^c,f   Gaffé, Joël ^a,b   Hallin, Peter F ^d   Riley, Margaret A ^c   Lenski, Richard E ^e   Schneider, Dominique ^a,b  

^a UNIV GRENOBLE ALPES   (France)

^b CNRS   (France)

^c Department of Biology   (Denmark)

^d TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^e Michigan State University ^*  (United States)

^f UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

bacteria; DNA superhelicity; evolution; fitness; phenotypic and genetic parallelism

Indexed keywords

ALLELE; ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; DNA SEQUENCE; DNA SUPERCOILING; DUSB GENE; ESCHERICHIA COLI; EVOLUTION; FIS GENE; GENE EXPRESSION; GENE LOCUS; GENE MUTATION; GENETIC ANALYSIS; GENETIC POLYMORPHISM; GENETIC TRANSCRIPTION; NONHUMAN; OPERON; PHENOTYPE; PHYLOGENY; RNA TRANSLATION; TOPA GENE;

ESCHERICHIA COLI;

EID: 77955933105     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msq099     Document Type: Article

References (100)

1. Almiron M, Link AJ, Furlong D, Kolter R. 1992. A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev. 6:2646-2654
2. Appleman JA, Ross W, Salomon J, Gourse RL. 1998. Activation of Escherichia coli rRNA transcription by FIS during a growth cycle. J Bacteriol. 180:1525-1532
3. Arfin SM, Long AD, Ito ET, Tolleri L, Riehle MM, Paegle ES, Hatfield GW. 2000. Global gene expression profiling in Escherichia coli K12. The effects of integration host factor. J Biol Chem. 275:29672-29684
4. Balke VL, Gralla JD. 1987. Changes in the linking number of supercoiled DNA accompany growth transitions in Escherichia coli. J Bacteriol. 169:4499-4506
5. Ball CA, Osuna R, Ferguson KC, Johnson RC. 1992. Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli. J Bacteriol. 174:8043-8056
6. Bantinaki E, Kassen R, Knight CG, Robinson Z, Spiers AJ, Rainey PB. 2007. Adaptive divergence in experimental populations of Pseudomonas fluorescens. III. Mutational origins of Wrinkly Spreader diversity. Genetics 176:441-453
7. Barrick JE, Lenski RE. 2009. Genome-wide mutational diversity in an evolving population of Escherichia coli. Cold Spring Harb Symp Quant Biol. Advance Access published September 23, 2009, doi:10.1101/sqb.2009.74.018.
8. Barrick JE, Yu DS, Yoon SH, Jeong H, Oh TK, Schneider D, Lenski RE, Kim JF. 2009. Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature 461:1243-1247
9. Bhriain NN, Dorman CJ, Higgins CF. 1989. An overlap between osmotic and anaerobic stress responses: a potential role for DNA supercoiling in the coordinate regulation of gene expression. Mol Microbiol. 3:933-942
10. Bishop AC, Xu J, Johnson RC, Schimmel P, Crecy-Lagard V. 2002. Identification of the tRNA-dihydrouridine synthase family. J Biol Chem. 277:25090-25095
11. 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
12. Champoux JJ. 2001. DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem. 70:369-413
13. Conrad TM, Joyce AR, Applebee MK, Barrett CL, Xie B, Gao Y, Palsson BO. 2009. 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. 10(10):R118.
14. Cooper TF, Remold SK, Lenski RE, Schneider D. 2008. Expression profiles reveal parallel evolution of epistatic interactions involving the CRP regulon in Escherichia coli. PLoS Genet. 4:e35.
15. Cooper TF, Rozen DE, Lenski RE. 2003. Parallel changes in gene expression after 20,000 generations of evolution in Escherichia coli. Proc Natl Acad Sci\USA. 100:1072-1077
16. Cooper VS, Lenski RE. 2000. The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407:736-739
17. Cooper VS, Schneider D, Blot M, Lenski RE. 2001. Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B. J Bacteriol. 183:2834-2841
18. Crandall KA, Kelsey CR, Imamichi H, Lane HC, Salzman NP. 1999. Parallel evolution of drug resistance in HIV: failure of non-synonymous/synonymous substitution rate ratio to detect selection. Mol Biol Evol. 16:372-382
19. Crozat E, Philippe N, Lenski RE, Geiselmann J, Schneider D. 2005. Long-term experimental evolution in Escherichia coli. XII. DNA topology as a key target of selection. Genetics 169:523-532
20. Dai X, Rothman-Denes LB. 1999. DNA structure and transcription. Curr Opin Microbiol. 2:126-130
21. Deng S, Stein RA, Higgins NP. 2005. Organization of supercoil domains and their reorganization by transcription. Mol Micro-biol. 57:1511-1521
22. Dorman CJ, Deighan P. 2003. Regulation of gene expression by histone-like proteins in bacteria. Curr Opin Genet Dev. 13: 179-184
23. Elena SF, Lenski RE. 1997. Long-term experimental evolution in Escherichia coli. VII. Mechanisms maintaining genetic variability within populations. Evolution 51:1058-1067
24. Elena SF, Lenski RE. 2003. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat Rev Genet. 4:457-469
25. Feldman-Cohen LS, Shao Y, Meinhold D, Miller C, Colon W, Osuna R. 2006. Common and variable contributions of Fis residues to high-affinity binding at different DNA sequences. J Bacteriol. 188:2081-2095
26. Ferea TL, Botstein D, Brown PO, Rosenzweig RF. 1999. Systematic changes in gene expression patterns following adaptive evolution in yeast. Proc Natl Acad Sci\USA. 96:9721-9726
27. Ferenci T. 2008. The spread of a beneficial mutation in experimental bacterial populations: the influence of the environment and genotype on the fixation of rpoS mutations. Heredity 100:446-452
28. Finkel SE, Johnson RC. 1992. The Fis protein: it's not just for DNA inversion anymore. Mol Microbiol. 6:3257-3265
29. Funchain P, Yeung A, Stewart JL, Lin R, Slupska MM, Miller JH. 2000. The consequences of growth of a mutator strain of Escherichia coli as measured by loss of function among multiple gene targets and loss of fitness. Genetics 154:959-970
30. Gellert M, Mizuuchi K, O'Dea MH, Nash HA. 1976. DNA gyrase: an enzyme that introduces superhelical turns into DNA. Proc Natl Acad Sci\USA. 73:3872-3876
31. Giraud A, Matic I, Tenaillon O, Clara A, Radman M, Fons M, Taddei F. 2001. Costs and benefits of high mutation rates: adaptive evolution of bacteria in the mouse gut. Science 291:2606-2608
32. Goldstein E, Drlica K. 1984. Regulation of bacterial DNA super-coiling: plasmid linking numbers vary with growth temperature. Proc Natl Acad Sci\USA. 81:4046-4050
33. Gonzalez-Gil G, Bringmann P, Kahmann R. 1996. FIS is a regulator of metabolism in Escherichia coli. Mol Microbiol. 22:21-29
34. Gosink KK, Gaal T, Bokal AJ, Gourse RL. 1996. A positive control mutant of the transcription activator protein FIS. J Bacteriol. 178:5182-5187
35. Grainger DC, Hurd D, Goldberg MD, Busby SJ. 2006. Association of nucleoid proteins with coding and non-coding segments of the Escherichia coli genome. Nucleic Acids Res. 34:4642-4652
36. Gresham D, Desai MM, Tucker CM, Jenq HT, Pai DA, Ward A, DeSevo CG, Botstein D, Dunham MJ. 2008. The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genet. 4:e1000303.
37. Hardy CD, Cozzarelli NR. 2005. A genetic selection for supercoiling mutants of Escherichia coli reveals proteins implicated in chromosome structure. Mol Microbiol. 57:1636-1652
38. Herring CD, Raghunathan A, Honisch C, et al. (11 co-authors). 2006. Comparative genome sequencing of Escherichia coli allows observation of bacterial evolution on a laboratory timescale. Nat Genet. 38:1406-1412
39. Higgins CF, Dorman CJ, Stirling DA, Waddell L, Booth IR, May G, Bremer E. 1988. A physiological role for DNA supercoiling in the osmotic regulation of gene expression in Salmonella typhimu-rium and Escherichia coli. Cell 52:569-584
40. Hommais F, Krin E, Laurent-Winter C, Soutourina O, Malpertuy A, Le Caer JP, Danchin A, Bertin P. 2001. Large-scale monitoring of pleiotropic regulation of gene expression by the prokaryotic nucleoid-associated protein, H-NS. Mol Microbiol. 40:20-36
41. Huey RB, Gilchrist GW, Carlson ML, Berrigan D, Serra L. 2000. Rapid evolution of a geographic cline in size in an introduced fly. Science 287:308-309
42. Jeong H, Barbe V, Lee CH, et al. (19 co-authors). 2009. Genome sequences of Escherichia coli B strains REL606 and BL21(DE3). J Mol Biol. 394:644-652
43. Jeong KS, Ahn J, Khodursky AB. 2004. Spatial patterns of transcriptional activity in the chromosome of Escherichia coli. Genome Biol. 5:R86.
44. Johansson J, Balsalobre C, Wang SY, Urbonaviciene J, Jin DJ, Sonden B, Uhlin BE. 2000. Nucleoid proteins stimulate stringently controlled bacterial promoters: a link between the cAMP-CRP and the (p)ppGpp regulons in Escherichia coli. Cell 102:475-485
45. Kar S, Edgar R, Adhya S. 2005. Nucleoid remodeling by an altered HU protein: reorganization of the transcription program. Proc Natl Acad Sci\USA. 102:16397-16402
46. Karem K, Foster JW. 1993. The influence of DNA topology on the environmental regulation of a pH-regulated locus in Salmonella typhimurium. Mol Microbiol. 10:75-86
47. Kelly A, Goldberg MD, Carroll RK, Danino V, Hinton JC, Dorman CJ. 2004. A global role for Fis in the transcriptional control of metabolism and type III secretion in Salmonella enterica serovar Typhimurium. Microbiology 150:2037-2053
48. Lang GI, Murray AW, Botstein D. 2009. The cost of gene expression underlies a fitness trade-off in yeast. Proc Natl Acad Sci\USA. 106:5755-5760
49. Lenski RE. 2004. Phenotypic and genomic evolution during a 20,000-generation experiment with the bacterium Escherichia coli. Plant Breed Rev. 24:225-265
50. Lenski RE, Mongold JA, Sniegowski PD, Travisano M, Vasi F, Gerrish PJ, Schmidt TM. 1998. Evolution of competitive fitness in experimental populations of Escherichia coli: what makes one genotype a better competitor than another? Antonie Van Leeuwenhoek. 73:35-47
51. Lenski RE, Rose MR, Simpson SC, Tadler SC. 1991. Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am Nat. 138:1315-1341
52. Lenski RE, Winkworth CL, Riley MA. 2003. Rates of DNA sequence evolution in experimental populations of Escherichia coli during 20,000 generations. J Mol Evol. 56:498-508
53. Link AJ, Phillips D, Church GM. 1997. Methods for generating precise deletions and insertions in the genome of wild-type Escherichia coli: application to open reading frame characterization. J Bacteriol. 179:6228-6237
54. Losos JB, Jackman TR, Larson A, Queiroz K, Rodriguez-Schettino L. 1998. Contingency and determinism in replicated adaptive radiations of island lizards. Science 279:2115-2118
55. Luijsterburg MS, Noom MC, Wuite GJ, Dame RT. 2006. The architectural role of nucleoid-associated proteins in the organization of bacterial chromatin: a molecular perspective. J Struct Biol. 156:262-272
56. Mallik P, Pratt TS, Beach MB, Bradley MD, Undamatla J, Osuna R. 2004. Growth phase-dependent regulation and stringent control of fis are conserved processes in enteric bacteria and involve a single promoter (fis P) in Escherichia coli. J Bacteriol. 186:122-135
57. McLeod SM, Aiyar SE, Gourse RL, Johnson RC. 2002. The C-terminal domains of the RNA polymerase alpha subunits: contact site with Fis and localization during co-activation with CRP at the Escherichia coli proP P2 promoter. J Mol Biol. 316:517-529
58. Morett E, Bork P. 1998. Evolution of new protein function: recombinational enhancer Fis originated by horizontal gene transfer from the transcriptional regulator NtrC. FEBS Lett. 433:108-112
59. Nei M, Gojobori T. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 3:418-426
60. O'Croinin T, Carroll RK, Kelly A, Dorman CJ. 2006. Roles for DNA supercoiling and the Fis protein in modulating expression of virulence genes during intracellular growth of Salmonella enterica serovar Typhimurium. Mol Microbiol. 62:869-882
61. Owens RM, Pritchard G, Skipp P, Hodey M, Connell SR, Nierhaus KH, O'Connor CD. 2004. A dedicated translation factor controls the synthesis of the global regulator Fis. EMBO J. 23:3375-3385
62. Pan CQ, Finkel SE, Cramton SE, Feng JA, Sigman DS, Johnson RC. 1996. Variable structures of Fis-DNA complexes determined by flanking DNA-protein contacts. J Mol Biol. 264:675-695
63. Papadopoulos D, Schneider D, Meier-Eiss J, Arber W, Lenski RE, Blot M. 1999. Genomic evolution during a 10,000-generation experiment with bacteria. Proc Natl Acad Sci\USA. 96:3807-3812
64. Pelosi L, Kuhn L, Guetta D, Garin J, Geiselmann J, Lenski RE, Schneider D. 2006. Parallel changes in global protein profiles during long-term experimental evolution in Escherichia coli. Genetics 173:1851-1869
65. Peng H, Marians KJ. 1993. Escherichia coli topoisomerase IV. Purification, characterization, subunit structure, and subunit interactions. J Biol Chem. 268:24481-24490
66. Peter BJ, Arsuaga J, Breier AM, Khodursky AB, Brown PO, Cozzarelli NR. 2004. Genomic transcriptional response to loss of chromosomal supercoiling in Escherichia coli. Genome Biol. 5:R87.
67. Philippe N, Crozat E, Lenski RE, Schneider D. 2007. Evolution of global regulatory networks during a long-term experiment with Escherichia coli. Bioessays 29:846-860
68. Philippe N, Pelosi L, Lenski RE, Schneider D. 2009. Evolution of penicillin-binding protein 2 concentration and cell shape during a long-term experiment with Escherichia coli. J Bacteriol. 191:909-921
69. Pigeon D, Chouinard A, Bernatchez L. 1997. Multiple modes of speciation involved in the parallel evolution of sympatric morphotypes of lake whitefish (Coregonus clupeaformis Salmo-nidae). Evolution 51:196-205
70. Postow L, Hardy CD, Arsuaga J, Cozzarelli NR. 2004. Topological domain structure of the Escherichia coli chromosome. Genes Dev. 18:1766-1779
71. Powell BS, Rivas MP, Court DL, Nakamura Y, Turnbough CL Jr. 1994. Rapid confirmation of single copy lambda prophage integration by PCR. Nucleic Acids Res. 22:5765-5766
72. Reid SD, Herbelin CJ, Bumbaugh AC, Selander RK, Whittam TS. 2000. Parallel evolution of virulence in pathogenic Escherichia coli. Nature 406:64-67
73. Reyes-Dominguez Y, Contreras-Ferrat G, Ramirez-Santos J, Membrillo-Hernandez J, Gomez-Eichelmann MC. 2003. Plasmid DNA supercoiling and gyrase activity in Escherichia coli wild-type and rpoS stationary-phase cells. J Bacteriol. 185:1097-1100
74. Rosenzweig RF, Sharp RR, Treves DS, Adams J. 1994. Microbial evolution in a simple unstructured environment: genetic differentiation in Escherichia coli. Genetics 137:903-917
75. Ross W, Thompson JF, Newlands JT, Gourse RL. 1990. Escherichia coli Fis protein activates ribosomal RNA transcription in vitro and in vivo. EMBO J. 9:3733-3742
76. Rozen DE, Schneider D, Lenski RE. 2005. Long-term experimental evolution in Escherichia coli. XIII. Phylogenetic history of a balanced polymorphism. J Mol Evol. 61:171-180
77. Sambrook J, Fritsch JE, Maniatis T. 1989. Molecular cloning: a laboratory manual. Plainview (NY): Cold Spring Harbor Laboratory Press.
78. Savage DF, de Crécy-Lagard V, Bishop AC. 2006. Molecular determinants of dihydrouridine synthase activity. FEBS Lett. 580:5198-5202
79. Schneider D, Duperchy E, Coursange E, Lenski RE, Blot M. 2000. Long-term experimental evolution in Escherichia coli. IX. Characterization of insertion sequence-mediated mutations and rearrangements. Genetics 156:477-488
80. Schneider DA, Ross W, Gourse RL. 2003. Control of rRNA expression in Escherichia coli. Curr Opin Microbiol. 6:151-156
81. Schneider R, Travers A, Kutateladze T, Muskhelishvili G. 1999. A DNA architectural protein couples cellular physiology and DNA topology in Escherichia coli. Mol Microbiol. 34:953-964
82. Schneider R, Travers A, Muskhelishvili G. 2000. The expression of the Escherichia coli fis gene is strongly dependent on the superhelical density of DNA. Mol Microbiol. 38:167-175
83. Simons RW, Houman F, Kleckner N. 1987. Improved single and multicopy lac-based cloning vectors for protein and operon fusions. Gene 53:85-96
84. Sniegowski PD, Gerrish PJ, Lenski RE. 1997. Evolution of high mutation rates in experimental populations of E. coli. Nature 387:703-705
85. Talukder AA, Iwata A, Nishimura A, Ueda S, Ishihama A. 1999. Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J Bacteriol. 181:6361-6370
86. Travers A, Muskhelishvili G. 2005. DNA supercoiling\a global transcriptional regulator for enterobacterial growth? Nat Rev Microbiol. 3:157-169
87. Valens M, Penaud S, Rossignol M, Cornet F, Boccard F. 2004. Macrodomain organization of the Escherichia coli chromosome. EMBO J. 23:4330-4341
88. Vasi F, Travisano M, Lenski RE. 1994. Long-term experimental evolution in Escherichia coli. II. Changes in life-history traits during adaptation to a seasonal environment. Am Nat. 144:432-456
89. Velicer GJ, Raddatz G, Keller H, Deiss S, Lanz C, Dinkelacker I, Schuster SC. 2006. Comprehensive mutation identification in an evolved bacterial cooperator and its cheating ancestor. Proc Natl Acad Sci\USA. 103:8107-8112
90. Walker KA, Atkins CL, Osuna R. 1999. Functional determinants of the Escherichia coli fis promoter: roles of-35,-10, and transcription initiation regions in the response to stringent control and growth phase-dependent regulation. J Bacteriol. 181:1269-1280
91. Wang JC. 1971. Interaction between DNA and an Escherichia coli protein omega. J Mol Biol. 55:523-533
92. Weinstein-Fischer D, Elgrably-Weiss M, Altuvia S. 2000. Escherichia coli response to hydrogen peroxide: a role for DNA supercoiling, topoisomerase I and Fis. Mol Microbiol. 35:1413-1420
93. Wichman HA, Badgett MR, Scott LA, Boulianne CM, Bull JJ. 1999. Different trajectories of parallel evolution during viral adaptation. Science 285:422-424
94. Woods R, Schneider D, Winkworth CL, Riley MA, Lenski RE. 2006. Tests of parallel molecular evolution in a long-term experiment with Escherichia coli. Proc Natl Acad Sci\USA. 103:9107-9112
95. Xu J, Johnson RC. 1995. Fis activates the RpoS-dependent stationary-phase expression of proP in Escherichia coli. J Bacteriol. 177:5222-5231
96. Xu J, Johnson RC. 1997. Activation of RpoS-dependent proP P2 transcription by the Fis protein in vitro. J Mol Biol. 270:346-359
97. Yamada H, Yoshida T, Tanaka K, Sasakawa C, Mizuno T. 1991. Molecular analysis of the Escherichia coli hns gene encoding a DNA-binding protein, which preferentially recognizes curved DNA sequences. Mol Gen Genet. 230:332-336
98. Yanisch-Perron C, Vieira J, Messing J. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119
99. Yuan HS, Finkel SE, Feng JA, Kaczor-Grzeskowiak M, Johnson RC, Dickerson RE. 1991. The molecular structure of wild-type and a mutant Fis protein: relationship between mutational changes and recombinational enhancer function or DNA binding. Proc Natl Acad Sci\USA. 88:9558-9562
100. Zechiedrich EL, Khodursky AB, Bachellier S, Schneider R, Chen D, Lilley DM, Cozzarelli NR. 2000. Roles of topoisomerases in maintaining steady-state DNA supercoiling in Escherichia coli. J Biol Chem. 275:8103-8113