Determinants of phase variation rate and the fitness implications of differing rates for bacterial pathogens and commensals

FEMS Microbiology Reviews

Volumn 33, Issue 3, 2009, Pages 504-520

  Bayliss, Christopher D ^a  

^a UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Localized hypermutation; Pathogenic bacteria; Phase variation; Repetitive DNA

Indexed keywords

DAM METHYLASE; METHYLTRANSFERASE; REPETITIVE DNA; UNCLASSIFIED DRUG;

BACTERIAL GENE; BACTERIUM PILUS; COMPUTER MODEL; CONFERENCE PAPER; DNA METHYLATION; DNA MODIFICATION; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; DNA SEQUENCE; ESCHERICHIA COLI; GENE EXPRESSION; GENE LOCUS; GENE MUTATION; GENETIC RECOMBINATION; GENOTYPE; HOMOLOGOUS RECOMBINATION; METHYLATION; NONHUMAN; PHENOTYPE; SIMPLE SEQUENCE REPEAT;

ANTIGENIC VARIATION; ANTIGENS, BACTERIAL; BACTERIAL PHYSIOLOGICAL PHENOMENA; DNA, BACTERIAL; RECOMBINATION, GENETIC;

BACTERIA (MICROORGANISMS);

EID: 64349088719     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1111/j.1574-6976.2009.00162.x     Document Type: Conference Paper

References (95)

1. Alexander HL, Richardson AR Stojiljkovic I (2004) Natural transformation and phase variation modulation in Neisseria meningitidis. Mol Microbiol 52 : 771 783.
2. Barbour AG, Dai Q, Restrepo BI, Stoenner HG Frank SA (2006) Pathogen escape from host immunity by a genome program for antigenic variation. P Natl Acad Sci USA 103 : 18290 18295.
3. Bayliss CD Moxon ER (2005) Repeats and variation in pathogen selection. The Implicit Genome (Caporale LH, ed), pp. 54 76. Oxford University Press, New York.
4. Bayliss CD, van de Ven T Moxon ER (2002) Mutations in polI but not mutSLH destabilize Haemophilus influenzae tetranucleotide repeats. EMBO J 21 : 1465 1476.
5. Bayliss CD, Dixon KM Moxon ER (2004) Simple sequence repeats (microsatellites): mutational mechanisms and contributions to bacterial pathogenesis. A meeting review. FEMS Immunol Med Mic 40 : 11 19.
6. Bayliss CD, Sweetman WA Moxon ER (2005) Destabilization of tetranucleotide repeats in Haemophilus influenzae mutants lacking RnaseHI or the Klenow domain of PolI. Nucleic Acids Res 33 : 400 408.
7. Bayliss CD, Hoe JC, Makepeace K, Martin P, Hood DW Moxon ER (2008) Escape by Neisseria meningitidis of the bactericidal activity of a monoclonal antibody is mediated by phase variation of lgtG and enhanced by a mutator phenotype. Infect Immun 76 : 5038 5048.
8. Blazquez J (2003) Hypermutation as a factor contributing to the acquisition of antimicrobial resistance. Clin Infect Dis 37 : 1201 1209.
9. Braaten BA, Nou X, Kaltenbach LS Low DA (1994) Methylation patterns in pap regulatory DNA control pyelonephritis-associated pili phase variation in E. coli. Cell 76 : 577 588.
10. Bryan A, Roesch P, Davis L, Moritz R, Pellett S Welch RA (2006) Regulation of type 1 fimbriae by unlinked FimB- and FimE-like recombinases in uropathogenic Escherichia coli strain CFT073. Infect Immun 74 : 1072 1083.
11. Chopra-Dewasthaly R, Citti C, Glew MD, Zimmermann M, Rosengarten R Jechlinger W (2008) Phase-locked mutants of Mycoplasma agalactiae: defining the molecular switch of high-frequency Vpma antigenic variation. Mol Microbiol 67 : 1196 1210.
12. Chu D Blomfield IC (2007) Orientational control is an efficient control mechanism for phase switching in the E. coli fim system. J Theor Biol 244 : 541 551.
13. Corn PG, Anders JA, Takala AK, Kayhty H Hoiseth SK (1993) Genes involved in Haemophilus influenzae type b capsule expression are frequently amplified. J Infect Dis 167 : 356 364.
14. Coyne MJ, Weinacht KG, Krinos CM Comstock LE (2003) Mpi recombinase globally modulates the surface architecture of a human commensal bacterium. P Natl Acad Sci USA 100 : 10446 10451.
15. Criss AK, Kline KA Seifert HS (2005) The frequency and rate of pilin antigenic variation in Neisseria gonorrhoeae. Mol Microbiol 58 : 510 519.
16. De Bolle X, Bayliss CD, Field D, van de Ven T, Saunders NJ, Hood DW Moxon ER (2000) The length of a tetranucleotide repeat tract in Haemophilus influenzae determines the phase variation rate of a gene with homology to type III DNA methyltransferases. Mol Microbiol 35 : 211 222.
17. Dixon K, Bayliss CD, Makepeace K, Moxon ER Hood DW (2007) Identification of the functional initiation codons of a phase-variable gene of Haemophilus influenzae, lic2A, with the potential for differential expression. J Bacteriol 189 : 511 521.
18. Dybvig K (1993) DNA rearrangements and phenotypic switching in prokaryotes. Mol Microbiol 10 : 465 471.
19. Dybvig K, Sitaraman R French CT (1998) A family of phase-variable restriction enzymes with differing specificities generated by high-frequency gene rearrangements. P Natl Acad Sci USA 95 : 13923 13928.
20. Forsman K, Goransson M Uhlin BE (1989) Autoregulation and multiple DNA interactions by a transcriptional regulatory protein in E. coli pili biogenesis. EMBO J 8 : 1271 1277.
21. Galhardo RS, Hastings PJ Rosenberg SM (2007) Mutation as a stress response and the regulation of evolvability. Crit Rev Biochem Mol 42 : 399 435.
22. Gally DL, Leathart J Blomfield IC (1996) Interaction of FimB and FimE with the fim switch that controls the phase variation of type 1 fimbriae in Escherichia coli K-12. Mol Microbiol 21 : 725 738.
23. Grant AJ, Restif O, McKinley TJ, Sheppard M, Maskell DJ Mastroeni P (2008) Modelling within-host spatiotemporal dynamics of invasive bacterial disease. PLoS Biol 6 : e74.
24. Gunther IV. NW, Snyder JA, Lockatell V, Blomfield I, Johnson DE Mobley HLT (2002) Assessment of virulence of uropathogenic Escherichia coli type I fimbrial mutants in which the invertible element is phase-locked on or off. Infect Immun 70 : 3344 3354.
25. Hall LM Henderson-Begg SK (2006) Hypermutable bacteria isolated from humans - a critical analysis. Microbiology 152 : 2505 2514.
26. Hallet B (2001) Playing Dr Jekyll and Mr Hyde: combined mechanisms of phase variation in bacteria. Curr Opin Microbiol 4 : 570 581.
27. Hannan TJ, Mysorekar IU, Chen SL, Walker JN, Jones JM, Pinkner JS, Hultgren SJ Seed PC (2008) LeuX tRNA-dependent and -independent mechanisms of Escherichia coli pathogenesis in acute cystitis. Mol Microbiol 67 : 116 128.
28. Henderson IR, Owen P Nataro JP (1999) Molecular switches - the ON and OFF of bacterial phase variation. Mol Microbiol 33 : 919 932.
29. Hernday A, Braaten B Low D (2004) The intricate workings of a bacterial epigenetic switch. Adv Exp Med Biol 547 : 83 89.
30. High NJ, Jennings MP Moxon ER (1996) Tandem repeats of the tetramer 5′-CAAT-3′ present in lic2A are required for phase variation but not lipopolysaccharide biosynthesis in Haemophilus influenzae. Mol Microbiol 20 : 165 174.
31. Hinde P, Deighan P Dorman CJ (2005) Characterization of the detachable Rho-dependent transcription terminator of the fimE gene in Escherichia coli K-12. J Bacteriol 187 : 8256 8266.
32. Hoiseth SK, Connelly CJ Moxon ER (1985) Genetics of spontaneous, high-frequency loss of b capsule expression in Haemophilus influenzae. Infect Immun 49 : 389 395.
33. Hoiseth SK, Moxon ER Silver RP (1986) Genes involved in Haemophilus influenzae type b capsule expression are part of an 18-kb tandem duplication. P Natl Acad Sci USA 83 : 1106 1110.
34. Holden N, Blomfield IC, Uhlin BE, Totsika M, Kulasekara DH Gally DL (2007a) Comparative analysis of FimB and FimE recombinase activity. Microbiology 153 : 4138 4149.
35. Holden N, Totsika M, Dixon L, Catherwood K Gally DL (2007b) Regulation of P-fimbrial phase variation frequencies in Escherichia coli CFT073. Infect Immun 75 : 3325 3334.
36. Holden NJ, Totsika M, Mahler E, Roe AJ, Catherwood K, Lindner K, Dobrindt U Gally DL (2006) Demonstration of regulatory cross-talk between P fimbriae and type 1 fimbriae in uropathogenic Escherichia coli. Microbiology 152 : 1143 1153.
37. Hood DW, Deadman ME, Allen T, Masoud H, Martin A, Brisson JR, Fleischmann R, Venter JC, Richards JC Moxon ER (1996a) Use of the complete genome sequence information of Haemophilus influenzae strain Rd to investigate lipopolysaccharide biosynthesis. Mol Microbiol 22 : 951 965.
38. Hood DW, Deadman ME, Jennings MP, Bisercic M, Fleischmann RD, Venter JC Moxon ER (1996b) DNA repeats identify novel virulence genes in Haemophilus influenzae. P Natl Acad Sci USA 93 : 11121 11125.
39. Ishii K, Matsuda H, Iwasa Y Sasaki A (1989) Evolutionarily stable mutation rate in a periodically changing environment. Genetics 121 : 163 174.
40. Jennings MP, Srikhanta YN, Moxon ER, Kramer M, Poolman JT, Kuipers B van der Ley P (1999) The genetic basis of the phase variation repertoire of lipopolysaccharide immunotypes in Neisseria meningitidis. Microbiology 145 : 3013 3021.
41. Jerse AE, Cohen MS, Drown PM, Whicker LG, Isbey SF, Seifert HS Cannon JG (1994) Multiple gonococcal opacity proteins are expressed during experimental urethral infection in the male. J Exp Med 179 : 911 920.
42. Kaltenbach L, Braaten B, Tucker J, Krabbe M Low D (1998) Use of a two-color genetic screen to identify a domain of the global regulator Lrp that is specifically required for pap phase variation. J Bacteriol 180 : 1224 1231.
43. Kim SH, Pytlos MJ Sinden RR (2006) Replication restart: a pathway for (CTG).(CAG) repeat deletion in Escherichia coli. Mutat Res 595 : 5 22.
44. Klemm P (1986) Two regulatory fim genes, fimB and fimE, control the phase variation of type 1 fimbriae in Escherichia coli. EMBO J 5 : 1389 1393.
45. Kroll JS Moxon ER (1988) Capsulation and gene copy number at the cap locus of Haemophilus influenzae type b. J Bacteriol 170 : 859 864.
46. Kroll JS, Loynds BM Moxon ER (1991) The Haemophilus influenzae capsulation gene cluster: a compound transposon. Mol Microbiol 5 : 1549 1560.
47. Kroll JS, Moxon ER Loynds BM (1993) An ancestral mutation enhancing the fitness and increasing the virulence of Haemophilus influenzae type b. J Infect Dis 168 : 172 176.
48. Kumar GA, Woodhall MR, Hood DW, Moxon ER Bayliss CD (2008) RecJ, ExoI and RecG are required for genome maintenance but not for generation of genetic diversity by repeat-mediated phase variation in Haemophilus influenzae. Mutat Res 640 : 46 53.
49. Lahooti M, Roesch PL Blomfield IC (2005) Modulation of the sensitivity of FimB recombination to branched-chain amino acids and alanine in Escherichia coli K-12. J Bacteriol 187 : 6273 6280.
50. Lane MC, Simms AN Mobley HL (2007) complex interplay between type 1 fimbrial expression and flagellum-mediated motility of uropathogenic Escherichia coli. J Bacteriol 189 : 5523 5533.
51. Leathart JB Gally DL (1998) Regulation of type 1 fimbrial expression in uropathogenic Escherichia coli: heterogeneity of expression through sequence changes in the fim switch region. Mol Microbiol 28 : 371 381.
52. Leigh Jr. EG (1970) Natural selection and mutability. Am Nat 104 : 301 335.
53. Levinson G Gutman G (1987) Slipped-strand mispairing: a major mechanism for DNA sequence evolution. Mol Biol Evol 4 : 203 221.
54. Linton D, Gilbert M, Hitchen PG, Dell A, Morris HR, Wakarchuk WW, Gregson NA Wren BW (2000) Phase variation of a beta-1,3 galactosyltransferase involved in generation of the ganglioside GM1-like lipo-oligosaccharide of Campylobacter jejuni. Mol Microbiol 37 : 501 514.
55. Martin P, van de Ven T, Mouchel N, Jeffries AC, Hood DW Moxon ER (2003) Experimentally revised repertoire of putative contingency loci in Neisseria meningitidis strain MC58: evidence for a novel mechanism of phase variation. Mol Microbiol 50 : 245 257.
56. Martin P, Sun L, Hood DW Moxon ER (2004) Involvement of genes of genome maintenance in the regulation of phase variation frequencies in Neisseria meningitidis. Microbiology 150 : 3001 3012.
57. Martin P, Makepeace K, Hill SA, Hood DW Moxon ER (2005) Microsatellite instability regulates transcription factor binding and gene expression. P Natl Acad Sci USA 102 : 3800 3804.
58. McClain MS, Blomfield IC Eisenstein BI (1991) Roles of fimB and fimE in site-specific DNA inversion associated with phase variation of type 1 fimbriae in Escherichia coli. J Bacteriol 173 : 5308 5314.
59. McCusker MP, Turner EC Dorman CJ (2008) DNA sequence heterogeneity in Fim tyrosine-integrase recombinase-binding elements and functional motif asymmetries determine the directionality of the fim genetic switch in Escherichia coli K-12. Mol Microbiol 67 : 171 187.
60. Morel P, Reverdy C, Michel B, Ehrlich SD Cassuto E (1998) The role of SOS and flap processing in microsatellite instability in Escherichia coli. P Natl Acad Sci USA 95 : 10003 10008.
61. Morelle S, Carbonnelle E, Matic I Nassif X (2005) Contact with host cells induces a DNA repair system in pathogenic Neisseriae. Mol Microbiol 55 : 853 861.
62. Moxon ER Murphy PA (1978) Haemophilus influenzae bacteremia and meningitis resulting from survival of a single organism. P Natl Acad Sci USA 75 : 1534 1536.
63. Moxon ER, Rainey PB, Nowak MA Lenski R (1994) Adaptive evolution of highly mutable loci in pathogenic bacteria. Curr Biol 4 : 24 33.
64. Moxon ER, Bayliss CD Hood DW (2007) Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Ann Rev Genet 40 : 307 333.
65. Nou X, Braaten B, Kaltenbach L Low DA (1995) Differential binding of Lrp to two sets of pap DNA binding sites mediated by Pap I regulates Pap phase variation in Escherichia coli. EMBO J 14 : 5785 5797.
66. Olsen PB, Schembri MA, Gally DL Klemm P (1998) Differential temperature modulation by H-NS of the fimB and fimE recombinase genes which control the orientation of the type 1 fimbrial phase switch. FEMS Microbiol Lett 162 : 17 23.
67. Palmer ME Lipsitch M (2006) The influence of hitchhiking and deleterious mutation upon asexual mutation rates. Genetics 173 : 461 472.
68. Parkhill J, Wren BW, Mungall K et al 2000) The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403 : 665 668.
69. Pettersson ME, Andersson DI, Roth JR Berg OG (2005) The amplification model for adaptive mutation: simulations and analysis. Genetics 169 : 1105 1115.
70. Richardson AR Stojiljkovic I (2001) Mismatch repair and the regulation of phase variation in Neisseria meningitidis. Mol Microbiol 40 : 645 655.
71. Richardson AR, Yu Z, Popovic T Stojiljkovic I (2002) Mutator clones of Neisseria meningitidis in epidemic serogroup A disease. P Natl Acad Sci USA 99 : 6103 6107.
72. Rosen DA, Pinkner JS, Jones JM, Walker JN, Clegg S Hultgren SJ (2008) Utilization of an intracellular bacterial community pathway in Klebsiella pneumoniae urinary tract infection and the effects of FimK on type 1 pilus expression. Infect Immun 76 : 3337 3345.
73. Salvatore P, Bucci C, Pagliarulo C et al 2002) Phenotypes of a naturally defective recB allele in Neisseria meningitidis clinical isolates. Infect Immun 70 : 4185 4195.
74. Saunders NJ, Peden J, Hood D Moxon ER (1998) Simple sequence repeats in the Helicobacter pylori genome. Mol Microbiol 27 : 1091 1098.
75. Saunders NJ, Jeffries AC, Peden JF, Hood DW, Tettelin H, Rappouli R Moxon ER (2000) Repeat-associated phase variable genes in the complete genome sequence of Neisseria meningitidis strain MC58. Mol Microbiol 37 : 207 215.
76. Saunders NJ, Moxon ER Gravenor MB (2003) Mutation rates: estimating phase variation rates when fitness differences are present and their impact on population structure. Microbiology 149 : 485 495.
77. Smith SG Dorman CJ (1999) Functional analysis of the FimE integrase of Escherichia coli K-12: isolation of mutant derivatives with altered DNA inversion preferences. Mol Microbiol 34 : 965 979.
78. Snyder JA, Lloyd AL, Lockatell CV, Johnson DE Mobley HL (2006) Role of phase variation of type 1 fimbriae in a uropathogenic Escherichia coli cystitis isolate during urinary tract infection. Infect Immun 74 : 1387 1393.
79. Snyder LAS, Butcher SA Saunders NJ (2001) Comparative whole-genome analyses reveal over 100 putative phase-variable genes in the pathogenic Neisseria spp. Microbiology 147 : 2321 2332.
80. Sohanpal BK, Friar S, Roobol J, Plumbridge JA Blomfield IC (2007) Multiple co-regulatory elements and IHF are necessary for the control of fimB expression in response to sialic acid and N-acetylglucosamine in Escherichia coli K-12. Mol Microbiol 63 : 1223 1236.
81. Strauss BS, Sagher D Acharya S (1997) Role of proofreading and mismatch repair in maintaining the stability of nucleotide repeats in DNA. Nucleic Acids Res 25 : 806 813.
82. Streisinger G, Okada Y, Emrich J, Newton J, Tsugita A, Terzaghi E Inouye M (1966) Frameshift mutations and the genetic code. Cold Spring Harb Sym 31 : 77 84.
83. Struve C, Bojer M Krogfelt KA (2008) Characterization of Klebsiella pneumoniae type 1 fimbriae by detection of phase variation during colonization and infection and impact on virulence. Infect Immun 76 : 4055 4065.
84. Sweetman WA, Moxon ER Bayliss CD (2005) Induction of the SOS regulon of Haemophilus influenzae does not affect phase variation rates at tetranucleotide or dinucleotide repeats. Microbiology 151 : 2751 2763.
85. Taddei F, Radman M, Maynard-Smith J, Toupance B, Gouyon PH Godelle B (1997) Role of mutator alleles in adaptive evolution. Nature 387 : 700 702.
86. Totsika M, Beatson SA, Holden N Gally DL (2008) Regulatory interplay between pap operons in uropathogenic Escherichia coli. Mol Microbiol 67 : 996 1011.
87. van der Ende A, Hopman CT Dankert J (2000) Multiple mechanisms of phase variation of PorA in Neisseria meningitidis. Infect Immun 68 : 6685 6690.
88. van der Woude MW Baumler AJ (2004) Phase and antigenic variation in bacteria. Clin Microbiol Rev 17 : 581 611, table of contents.
89. van der Woude MW, Kaltenbach LS Low DA (1995) Leucine-responsive regulatory protein plays dual roles as both an activator and a repressor of the Escherichia coli pap fimbrial operon. Mol Microbiol 17 : 303 312.
90. Weyand NJ, Braaten BA, van der Woude M, Tucker J Low DA (2001) The essential role of the promoter-proximal subunit of CAP in pap phase variation: Lrp- and helical phase-dependent activation of papBA transcription by CAP from -215. Mol Microbiol 39 : 1504 1522.
91. White-Ziegler CA, Angus Hill ML, Braaten BA, van der Woude MW Low DA (1998) Thermoregulation of Escherichia coli pap transcription: H-NS is a temperature-dependent DNA methylation blocking factor. Mol Microbiol 28 : 1121 1137.
92. White-Ziegler CA, Black AM, Eliades SH, Young S Porter K (2002) The N-acetyltransferase RimJ responds to environmental stimuli to repress pap fimbrial transcription in Escherichia coli. J Bacteriol 184 : 4334 4342.
93. Wolf DM, Vazirani VV Arkin AP (2005) A microbial modified prisoner's dilemma game: how frequency-dependent selection can lead to random phase variation. J Theor Biol 234 : 255 262.
94. Xie Y, Yao Y, Kolisnychenko V, Teng CH Kim KS (2006) HbiF regulates type 1 fimbriation independently of FimB and FimE. Infect Immun 74 : 4039 4047.
95. Zaleski P, Wojciechowski M Piekarowicz A (2005) The role of Dam methylation in phase variation of Haemophilus influenzae genes involved in defence against phage infection. Microbiology 151 : 3361 3369.