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Role of DNA Methyltransferases in Epigenetic Regulation in Bacteria

  • Ritesh Kumar
  • Desirazu N. RaoEmail author
Part of the Subcellular Biochemistry book series (SCBI, volume 61)

Abstract

In prokaryotes, alteration in gene expression was observed with the modification of DNA, especially DNA methylation. Such changes are inherited from generation to generation with no alterations in the DNA sequence and represent the epigenetic signal in prokaryotes. DNA methyltransferases are enzymes involved in DNA modification and thus in epigenetic regulation of gene expression. DNA methylation not only affects the thermodynamic stability of DNA, but also changes its curvature. Methylation of specific residues on DNA can affect the protein-DNA interactions. DNA methylation in prokaryotes regulates a number of physiological processes in the bacterial cell including transcription, DNA mismatch repair and replication initiation. Significantly, many reports have suggested a role of DNA methylation in regulating the expression of a number of genes in virulence and pathogenesis thus, making DNA methlytransferases novel targets for the designing of therapeutics. Here, we summarize the current knowledge about the influence of DNA methylation on gene regulation in different bacteria, and on bacterial virulence.

Keywords

Epigenetic Regulation Phase Variation GATC Site GATC Sequence Target Recognition Domain 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Adamczyk-Poplawska M, Lower M, Piekarowicz A (2009) Characterization of the NgoAXP: phase-variable type III restriction-modification system in Neisseria gonorrhoeae. FEMS Microbiol Lett 300:25–35PubMedGoogle Scholar
  2. Alm RA, Ling LSL, Moir DT, King BL, Brown ED, Doig PC, Smith DR, Noonan B, Guild BC, deJonge BL, Carmel G, Tummino PJ, Caruso A, Uria-Nickelsen M, Mills DM, Ives C, Gibson R, Merberg D, Mills SD, Jiang Q, Taylor DE, Vovis GF, Trost TJ (1999) Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397:176–180PubMedGoogle Scholar
  3. Ando T, Ishiguro K, Watanabe O, Miyake N, Kato T, Hibi S, Mimura S, Nakamura M, Miyahara R, Ohmiya N, Niwa Y, Goto H (2010) Restriction-modification systems may be associated with Helicobacter pylori virulence. J Gastroenterol Hepatol 1:S95–S98Google Scholar
  4. Arber W (2000) Genetic variation: molecular mechanisms and impact on microbial evolution. FEMS Microbiol Rev 24:1–7PubMedGoogle Scholar
  5. Arber W (2002) Evolution of prokaryotic genomes. Curr Top Microbiol Immunol 264:1–14PubMedGoogle Scholar
  6. Arber W, Dussoix D (1962) Host specificity of DNA produced by Escherichia coli. I. Host controlled modification of bacteriophage lambda. J Mol Biol 5:18–36PubMedGoogle Scholar
  7. Au KG, Welsh K, Modrich P (1992) Initiation of methyl-directed mismatch repair. J Biol Chem 267:12142–12148PubMedGoogle Scholar
  8. Barbeyron T, Kean K, Forterre P (1984) DNA adenine methylation of GATC sequences appeared recently in the Escherichia coli lineage. J Bacteriol 160:586–590PubMedGoogle Scholar
  9. Bell DC, Cupples CG (2001) Very-short-patch repair in Escherichia coli requires the dam adenine methylase. J Bacteriol 183:3631–3635PubMedGoogle Scholar
  10. Bergerat A, Kriebardis A, Guschlbauer W (1989) Preferential site-specific hemimethylation of GATC sites in pBR322 DNA by Dam methyltransferase from Escherichia coli. J Biol Chem 264:4064–4070PubMedGoogle Scholar
  11. Bertani G, Weigle JJ (1953) Host controlled variation in bacterial viruses. J Bacteriol 65:113–121PubMedGoogle Scholar
  12. Bestor TH (2000) The DNA methyltransferases of mammals. Hum Mol Genet 9:2395–2402PubMedGoogle Scholar
  13. Bheemanaik S, Reddy YV, Rao DN (2006) Structure, function and mechanism of exocyclic DNA methyltransferases. Biochem J 399:177–190PubMedGoogle Scholar
  14. Bickle TA, Kruger DH (1993) Biology of DNA restriction. Microbiol Rev 57:434–450PubMedGoogle Scholar
  15. Blaisdell BE, Campbell AM, Karlin S (1996) Similarities and dissimilarities of phage genomes. Proc Natl Acad Sci USA 93:5854–5859PubMedGoogle Scholar
  16. Bogan JA, Helmstetter CE (1997) DNA sequestration and transcription in the oriC region of Escherichia coli. Mol Microbiol 26:889–896PubMedGoogle Scholar
  17. 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 76:577–588PubMedGoogle Scholar
  18. Braun RE, O’Day K, Wright A (1985) Autoregulation of the DNA replication gene dnaA in E. coli K-12. Cell 40:159–169PubMedGoogle Scholar
  19. Broadbent SE, Davies MR, van der Woude MW (2010) Phase variation controls expression of Salmonella lipopolysaccharide modification genes by a DNA methylation-dependent mechanism. Microbiology 77:337–353Google Scholar
  20. Bucci C, Lavitola A, Salvatore P, Del Giudice L, Massardo DR, Bruni CB, Alifano P (1999) Hypermutation in pathogenic bacteria: frequent phase variation in meningococci is a phenotypic trait of a specialized mutator biotype. Mol Cell 3:435–445PubMedGoogle Scholar
  21. Bujnicki JM (2002) Sequence permutations in the molecular evolution of DNA methyltransferases. BMC Evol Biol 2:3PubMedGoogle Scholar
  22. Bujnicki JM, Radlinska M (1999) Molecular evolution of DNA-(−cytosine N4) methyltransferases: evidence for their polyphyletic origin. Nucleic Acids Res 27:4501–4509PubMedGoogle Scholar
  23. Calmann MA, Marinus MG (2003) Regulated expression of the Escherichia coli dam gene. J Bacteriol 185:5012–5014PubMedGoogle Scholar
  24. Camacho EM, Casadesus J (2002) Conjugal transfer of the virulence plasmid of Salmonella enterica is regulated by the leucine-responsive regulatory protein and DNA adenine methylation. Mol Microbiol 44:1589–1598PubMedGoogle Scholar
  25. Campbell JL, Kleckner N (1990) E. coli oriC and the dnaA gene promoter are sequestered from dam methyltransferase following the passage of the chromosomal replication fork. Cell 62:967–979PubMedGoogle Scholar
  26. Carlson K, Kosturko LD (1998) Endonuclease II of coliphage T4: a recombinase disguised as a restriction endonuclease? Mol Microbiol 27:671–676PubMedGoogle Scholar
  27. Casadesu’s J, Low D (2006) Epigenetic gene regulation in the bacterial world. Microbiol Mol Biol Rev 70:830–856Google Scholar
  28. Chen L, Paulsen DB, Scruggs DW, Banes MM, Reeks BY, Lawrence ML (2003) Alteration of DNA adenine methylase (Dam) activity in Pasteurella multocida causes increased spontaneous mutation frequency and attenuation in mice. Microbiology 149:2283–2290PubMedGoogle Scholar
  29. Cheng X (1995) Structure and function of DNA methyltransferases. Annu Rev Biophys Biomol Struct 24:293–318PubMedGoogle Scholar
  30. 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 35:211–222PubMedGoogle Scholar
  31. de Vries N, Duinsbergen D, Kuipers EJ, Pot RG, Wiesenekker P, Penn CW, van Vliet AH, Vandenbroucke-Grauls CM, Kusters JG (2002) Transcriptional phase variation of a type III restriction-modification system in Helicobacter pylori. J Bacteriol 184:6615–6623PubMedGoogle Scholar
  32. Dodson KW, Berg DE (1989) Factors affecting transposition activity of IS50 and Tn5 ends. Gene 76:207–213PubMedGoogle Scholar
  33. Donahue JP, Israel DA, Torres VJ, Necheva AS, Miller GG (2002) Inactivation of a Helicobacter pylori DNA methyltransferase alters dnaK operon expression following host-cell adherence. FEMS Microbiol Lett 208:295–301PubMedGoogle Scholar
  34. Dybvig K, Sitaraman R, French CT (1998) A family of phase-variable restriction enzymes with differing specificities generated by high-frequency gene rearrangements. Proc Natl Acad Sci USA 95:13923–13928PubMedGoogle Scholar
  35. Fa¨lker S, Schmidt MA, Heusipp G (2005) DNA methylation in Yersinia enterocolitica: role of the DNA adenine methyltransferase in mismatch repair and regulation of virulence factors. Microbiology 151:2291–2299Google Scholar
  36. Fälker S, Schmidt MA, Heusipp G (2007) DNA adenine methylation and bacterial pathogenesis. Int J Med Microbiol 297:1–7PubMedGoogle Scholar
  37. Fox KL, Srikhanta YN, Jennings MP (2007) Phase variable Type III restriction-modification systems of host-adapted bacterial pathogens. Mol Microbiol 65:1375–1379PubMedGoogle Scholar
  38. Garcia-Del Portillo F, Pucciarelli MG, Casadesus J (1999) DNA adenine methylase mutants of Salmonella typhimurium show defects in protein secretion, cell invasion, and M cell cytotoxicity. Proc Natl Acad Sci USA 96:11578–11583PubMedGoogle Scholar
  39. Geier GE, Modrich P (1979) Recognition sequence of the dam methylase of Escherichia coli K12 and mode of cleavage of Dpn I endonuclease. J Biol Chem 254:1408–1413PubMedGoogle Scholar
  40. Haagmans W, van der Woude M (2000) Phase variation of Ag43 in Escherichia coli: dam-dependent methylation abrogates OxyR binding and OxyR-mediated repression of transcription. Mol Microbiol 35:877–887PubMedGoogle Scholar
  41. Hallet B (2001) Playing Dr Jekyll and Mr Hyde: combined mechanisms of phase variation in bacteria. Curr Opin Microbiol 4:570–581PubMedGoogle Scholar
  42. Hattman S, Malygin EG (2004) Bacteriophage T2Dam and T4Dam DNA-[N6-adenine]-methyltransferases. Prog Nucleic Acid Res Mol Biol 77:67–126PubMedGoogle Scholar
  43. Hattman S, Sun W (1997) Escherichia coli OxyR modulation of bacteriophage Mu mom expression in dam+ cells can be attributed to its ability to bind Pmom promoter DNA. Nucleic Acids Res 25:4385–4388PubMedGoogle Scholar
  44. Heithoff D, Sinsheimer RL, Low DA, Mahan MJ (1999) An essential role for DNA adenine methylation in bacterial virulence. Science 284:967–970PubMedGoogle Scholar
  45. Heithoff DM, Enioutina EI, Daynes RA, Sinsheimer RL, Low DA, Mahan MJ (2001) Salmonella DNA adenine methylase mutants confer cross-protective immunity. Infect Immun 69:6725–6730PubMedGoogle Scholar
  46. Heitman J (1993) On the origins, structures and functions of restriction-modification enzymes. Genet Eng (NY) 15:57–108Google Scholar
  47. Herman GE, Modrich P (1982) Escherichia coli dam methylase. Physical and catalytic properties of the homogeneous enzyme. J Biol Chem 257:2605–2612PubMedGoogle Scholar
  48. Heusipp G, Falker S, Schmidt MA (2006) DNA adenine methylation and bacterial pathogenesis. Int J Med Microbiol 29:1–7Google Scholar
  49. Jafri S, Chen S, Calvo JM (2002) ilvIH operon expression in Escherichia coli requires Lrp binding to two distinct regions of DNA. J Bacteriol 184:5293–5300PubMedGoogle Scholar
  50. Jeltsch A (1999) Circular permutation in the molecular evolution of DNA methyltransferases. J Mol Evol 49:161–164PubMedGoogle Scholar
  51. Jeltsch A (2002) Beyond Watson and Crick: DNA methylation and molecular enzymology of DNA methyltransferases. Chembiochem 3:274–293PubMedGoogle Scholar
  52. Jeltsch A (2003) Maintenance of species identity and controlling speciation of bacteria: a new function for restriction/modification systems? Gene 317:13–16PubMedGoogle Scholar
  53. Jennings MP, Hood DW, Peak IR, Virji M, Moxon ER (1995) Molecular analysis of a locus for the biosynthesis and phase-variable expression of the lacto-N-neotetraose terminal lipopolysaccharide structure in Neisseria meningitidis. Mol Microbiol 18:729–740PubMedGoogle Scholar
  54. Jorgensen HF, Bird A (2002) MeCP2 and other methyl-CpG binding proteins. Ment Retard Dev Disabil Res Rev 8:87–93PubMedGoogle Scholar
  55. Julio SM, Heithoff DM, Provenzano D, Klose KE, Sinsheimer RL, Low DA, Mahan MJ (2001) DNA adenine methylase is essential for viability and plays a role in the pathogenesis of Yersinia pseudotuberculosis and Vibrio cholerae. Infect Immun 69:7610–7615PubMedGoogle Scholar
  56. Julio SM, Heithoff DM, Sinsheimer RL, Low DA, Mahan MJ (2002) DNA adenine methylase overproduction in Yersinia pseudotuberculosis alters YopE expression and secretion and host immune responses to infection. Infect Immun 70:1006–1009PubMedGoogle Scholar
  57. Kim JS, Li J, Barnes IH et al (2008) Role of the Campylobacter jejuni Cj1461 DNA methyltransferase in regulating virulence characteristics. J Bacteriol 190:6524–6529PubMedGoogle Scholar
  58. Kita K, Kotani H, Sugisaki H, Takanami M (1989) The FokI restriction-modification system I. Organization and nucleotide sequences of the restriction and modification genes. J Biol Chem 264:5751–5756PubMedGoogle Scholar
  59. Klose RJ, Bird AP (2006) Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci 31:89–97PubMedGoogle Scholar
  60. Kobayashi I (2004) Restriction-modification systems as minimal forms of life. In: Pingoud A (ed) Restriction endonucleases. Springer, Berlin, pp 19–62Google Scholar
  61. Kossykh VG, Schlagman SL, Hattman S (1995) Phage T4 DNA [N6-adenine]methyltransferase. Overexpression, purification, and characterization. J Biol Chem 270:14389–14393PubMedGoogle Scholar
  62. Kumar R, Rao DN (2011) A nucleotide insertion between two solitary MTases results in a bifunctional fusion MTase in H.pylori. Biochem J 433:487–495PubMedGoogle Scholar
  63. Kumar S, Cheng X, Klimasauskas S, Mi S, Posfai J, Roberts RJ, Wilson GG (1994) The DNA (cytosine-5) methyltransferases. Nucleic Acids Res 22:1–10PubMedGoogle Scholar
  64. Kumar R, Mukhopadhyay AK, Rao DN (2010) Characterization of an N6 adenine methyltransferase from H. pylori strain 26695 which methylates adjacent adenines on the same strand. FEBS J 277:1666–1683PubMedGoogle Scholar
  65. Lewis JD, Meehan RR, Henzel WJ, Maurer-Fogy I, Jeppesen P, Klein F, Bird A (1992) Purification, sequence, and cellular localization of a novel chromosomal protein that binds to methylated DNA. Cell 69:905–914PubMedGoogle Scholar
  66. Lin LF, Posfai J, Roberts RJ, Kong H (2001) Comparative genomics of the restriction-modification systems in Helicobacter pylori. Proc Natl Acad Sci USA 98:2740–2745PubMedGoogle Scholar
  67. Løbner-Olesen A, Marinus MG, Hansen FG (2003) Role of SeqA and Dam in Escherichia coli gene expression: a global/microarray analysis. Proc Natl Acad Sci USA 100:4672–4677PubMedGoogle Scholar
  68. Lobner-Olesen A, Skovgaard O, Marinus MG (2005) Dam methylation:coordinating cellular processes. Curr Opin Microbiol 8:154–160PubMedGoogle Scholar
  69. López-Garrido J, Casadesús J (2010) Regulation of Salmonella enterica pathogenicity island 1 by DNA adenine methylation. Genetics 184:637–649PubMedGoogle Scholar
  70. Low DA, Weyand NJ, Mahan MJ (2001) Roles of DNA adenine methylation in regulating bacterial gene expression and virulence. Infect Immun 69:7197–7204PubMedGoogle Scholar
  71. Lu M, Campbell JL, Boye E, Kleckner N (1994) SeqA: a negative modulator of replication initiation in E. coli. Cell 77:413–426PubMedGoogle Scholar
  72. Lupas AN, Pointing CP, Russell RB (2001) On the evolution of protein folds: are similar motifs in different protein folds the result of convergence, insertion, or relics of an ancient peptide world? J Struct Biol 134:191–203PubMedGoogle Scholar
  73. Luria SE, Human ML (1952) A nonhereditary, host-induced variation of bacterial viruses. J Bacteriol 64:557–569PubMedGoogle Scholar
  74. Malone T, Blumenthal RM, Cheng X (1995) Structure-guided analysis reveals nine sequence motifs conserved among DNA amino-methyltransferases, and suggests a catalytic mechanism for these enzymes. J Mol Biol 253:618–632PubMedGoogle Scholar
  75. Marczynski GT, Shapiro L (2002) Control of chromosome replication in Caulobacter crescentus. Annu Rev Microbiol 56:625–656PubMedGoogle Scholar
  76. Marinus MG (1996) Methylation of DNA. In: Neidhardt FC, Curtiss R, Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington DC, pp 782–791Google Scholar
  77. Marinus MG, Casadesus J (2009) Roles of DNA adenine methylation in host-pathogen interactions: mismatch repair, transcriptional regulation, and more. FEMS Microbiol Rev 33:488–503PubMedGoogle Scholar
  78. Mashhoon N, Carroll M, Pruss C, Eberhard J, Ishikawa S, Estabrook RA, Reich N (2004) Functional characterization of Escherichia coli DNA adenine methyltransferase, a novel target for antibiotics. J Biol Chem 279:52075–52081PubMedGoogle Scholar
  79. McClain MS, Shaffer CL, Israel DA, Peek RM Jr, Cover TL (2009) Genome sequence analysis of Helicobacter pylori strains associated with gastric ulceration and gastric cancer. BMC Genomics 10:3PubMedGoogle Scholar
  80. McCommas SA, Syvanen M (1988) Temporal control of transposition in Tn5. J Bacteriol 170:889–894PubMedGoogle Scholar
  81. McKane M, Milkman R (1995) Transduction, restriction and recombination patterns in Escherichia coli. Genetics 139:35–43PubMedGoogle Scholar
  82. Mehling JS, Lavender H, Clegg S (2006) A Dam methylation mutant of Klebsiella pneumoniae, is partially attenuated. FEMS Microbiol Lett 268:187–193Google Scholar
  83. Messer W, Noyer-Weidner M (1988) Timing and targeting: the biological functions of Dam methylation in E. coli. Cell 54:735–737PubMedGoogle Scholar
  84. Modrich P, Lahue R (1996) Mismatch repair in replication fidelity, genetic recombination, and cancer biology. Annu Rev Biochem 65:101–133PubMedGoogle Scholar
  85. Moxon ER, Thaler DS (1997) Microbial genetics. The tinkerer’s evolving tool-box. Nature 387:659–662PubMedGoogle Scholar
  86. Moxon R, Bayliss C, Hood D (2006) Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Annu Rev Genet 40:307–333PubMedGoogle Scholar
  87. Naito T, Kusano K, Kobayashi I (1995) Selfish behavior of restriction-modification systems. Science 267:897–899PubMedGoogle Scholar
  88. Nan X, Cross S, Bird A (1998) Gene silencing by methyl-CpGbinding proteins. Novartis Found Symp 214:6–16PubMedGoogle Scholar
  89. Ogden GB, Pratt MJ, Schaechter M (1988) The replicative origin of the E. coli chromosome binds to cell membranes only when hemimethylated. Cell 54:121–135Google Scholar
  90. Oshima T, Wada C, Kawagoe Y, Ara T, Maeda M, Masuda Y, Hiraga S, Mori H (2002) Genome-wide analysis of deoxyadenosine methyltransferase-mediated control of gene expression in Escherichia coli. Mol Microbiol 45:673–695PubMedGoogle Scholar
  91. Oza JP, Yeh JB, Reich NO (2005) DNA methylation modulates Salmonella enterica serovar Typhimurium virulence in Caenorhabditis elegans. FEMS Microbiol Lett 245:53–59PubMedGoogle Scholar
  92. Pingoud A, Fuxreiter M, Pingoud V, Wende W (2005) Type II restriction endonucleases: structure and mechanism. Cell Mol Life Sci 62:685–707PubMedGoogle Scholar
  93. Polaczek P, Kwan K, Campbell L (1998) GATC motifs may alter the conformation of DNA depending on sequence context and N6-adenine methylation status: possible implications for DNA-protein recognition. Mol Gen Genet 258:488–493PubMedGoogle Scholar
  94. Posfai J, Bhagwat AS, Posfai G, Roberts RJ (1989) Predictive motifs derived from cytosine methyltransferases. Nucleic Acids Res 17:2421–2435PubMedGoogle Scholar
  95. Raleigh EA, Brooks JE (1998) Restriction modification systems: where they are and what they do. In: De Bruijn FJ, Lupski JR, Weinstock GM (eds) Bacterial genomes. Chapman and Hall, New York, pp 78–92Google Scholar
  96. Reisenauer A, Shapiro L (2002) DNA methylation affects the cell cycle transcription of the CtrA global regulator in Caulobacter. EMBO J 21:4969–4977PubMedGoogle Scholar
  97. Reisenauer A, Kahng LS, McCollum S, Shapiro L (1999) Bacterial DNA methylation: a cell cycle regulator? J Bacteriol 181:5135–5139PubMedGoogle Scholar
  98. Reznikoff WS (1993) The Tn5 transposon. Annu Rev Microbiol 47:945–963PubMedGoogle Scholar
  99. Roberts D, Hoopes BC, McClure WR, Kleckner N (1985) IS10 transposition is regulated by DNA adenine methylation. Cell 43:117–130PubMedGoogle Scholar
  100. Roberts RJ, Belfort M, Bestor T, Bhagwat AS, Bickle TA, Bitinaite J, Blumenthal RM, Degtyarev S, Dryden DT, Dybvig K et al (2003) A nomenclature for restriction enzymes, DNA methyltransferases, homing endonucleases and their genes. Nucleic Acids Res 31:1805–1812PubMedGoogle Scholar
  101. Roberts RJ, Vincze T, Posfai J, Macelis D (2007) REBASE–enzymes and genes for DNA restriction and modification. Nucleic Acids Res 35:D269–D270PubMedGoogle Scholar
  102. Robertson BD, Meyer TF (1992) Genetic variation in pathogenic bacteria. Trends Genet 8:422–427PubMedGoogle Scholar
  103. Robertson GT, Reisenauer A, Wright R, Jensen RB, Jensen A, Shapiro L, Roop RM II (2000) The Brucella abortus CcrM DNA methyltransferase is essential for viability, and its overexpression attenuates intracellular replication in murine macrophages. J Bacteriol 182:3482–3489PubMedGoogle Scholar
  104. Robinson VL, Oyston PC, Titball RW (2005) Oral immunization with a dam mutant of Yersinia pseudotuberrculosis protects against plague. Microbiology 151:1919–1926Google Scholar
  105. Ryan KA, Lo RY (1999) Characterization of a CACAG pentanucleotide repeat in Pasteurella haemolytica and its possible role in modulation of a novel type III restriction-modification system. Nucleic Acids Res 27:1505–1511PubMedGoogle Scholar
  106. Salaun L, Bodo L, Suerbaum S, Saunders NJ (2004) The diversity within an expanded and redefined repertoire of phase-variable genes in Helicobacter pylori. Microbiology 150:817–830PubMedGoogle Scholar
  107. Salaun L, Ayraud S, Saunders NJ (2005) Phase variation mediated niche adaptation during prolonged experimental murine infection with Helicobacter pylori. Microbiology 151:917–923PubMedGoogle Scholar
  108. Saunders NJ, Peden JF, Hood DW, Moxon ER (1998) Simple sequence repeats in the Helicobacter pylori genome. Mol Microbiol 27:1091–1098PubMedGoogle Scholar
  109. Saunders NJ, Jeffries AC, Peden JF, Hood DW, Tettelin H, Rappuoli R, Moxon ER (2000) Repeat-associated phase variable genes in the complete genome sequence of Neisseria meningitidis strain MC58. Mol Microbiol 37:207–215PubMedGoogle Scholar
  110. Schlagman SL, Hattman S (1983) Molecular cloning of a functional dam+ gene coding for phage T4 DNA adenine methylase. Gene 22:139–156PubMedGoogle Scholar
  111. Schlagman SL, Miner Z, Feher Z, Hattman S (1988) The DNA [adenine-N6]methyltransferase (Dam) of bacteriophage T4. Gene 73:517–530PubMedGoogle Scholar
  112. Schluckebier G, O’Gara M, Saenger W, Cheng X (1995) Universal catalytic domain structure of AdoMet-dependent methyltransferases. J Mol Biol 247:16–20PubMedGoogle Scholar
  113. Seib KL, Peak IR, Jennings MP (2002) Phase variable restriction-modification systems in Moraxella catarrhalis. FEMS Immunol Med Microbiol 32:159–165PubMedGoogle Scholar
  114. Sistla S, Rao DN (2004) S-Adenosyl-L-methionine-dependent restriction enzymes. Crit Rev Biochem Mol Biol 39:1–19PubMedGoogle Scholar
  115. Sohail A, Lieb M, Dar M, Bhagwat AS (1990) A gene required for very short patch repair in E. coli is adjacent to the DNA cytosine methylase gene. J Bacteriol 172:4214–4221PubMedGoogle Scholar
  116. Srikhanta YN, Maguire TL, Stacey KJ, Grimmond SM, Jennings MP (2005) The phasevarion: a genetic system controlling coordinated, random switching of expression of multiple genes. Proc Natl Acad Sci USA 102:5547–5551PubMedGoogle Scholar
  117. Srikhanta YN, Dowideit SJ, Edwards JL, Falsetta ML, Wu H-J, Harrison OB, Fox KL, Seib KL, Maguire TL, Wang AH-J, Maiden MC, Grimmond SM, Apicella MA, Jennings MP (2009) Phasevarions mediate random switching of gene expression in pathogenic Neisseria. PLoS Pathog 5:e1000400PubMedGoogle Scholar
  118. Srikhanta YN, Fox KL, Jennings MP (2010) The phasevarion: phase variation of Type III DNA methyltransferases controls coordinated switching in multiple genes. Nat Rev Microbiol 8:196–206PubMedGoogle Scholar
  119. Sternberg N, Sauer B, Hoess R, Abremski K (1986) Bacteriophage P1 cre gene and its regulatory region. Evidence for multiple promoters and for regulation by Dam methylation. J Mol Biol 187:197–212PubMedGoogle Scholar
  120. Sugisaki H, Kita K, Takanami M (1989) The FokI restriction-modification system II. Presence of two domains in FokI methylase responsible for modification of different strands. J Biol Chem 264:5757–5761PubMedGoogle Scholar
  121. Sun K, Jiao XD, Zhang M, Sun L (2010) DNA adenine methylase is involved in the pathogenesis of Edwardsiella tarda. Vet Microbiol 141:149–154PubMedGoogle Scholar
  122. Taylor VL, Titball RW, Oyston PCF (2005) Oral immunization with a dam mutant of Yersinia pseudotuberculosis protects against plague. Microbiology 151:1919–1926PubMedGoogle Scholar
  123. Tomb JF, White O, Kerlavage AR, Clayton RA, Sutton GG, Fleischmann RD et al (1997) The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539–547PubMedGoogle Scholar
  124. Torreblanca J, Marqués S, Casadesús J (1999) Synthesis of FinP RNA by plasmids F and pSLT is regulated by DNA adenine methylation. Genetics 152:31–45PubMedGoogle Scholar
  125. Urig S, Gowher H, Hermann A, Beck C, Fatemi M, Humeny A, Jeltsch A (2002) The Escherichia coli dam DNA methyltransferase modifies DNA in a highly processive reaction. J Mol Biol 319:1085–1096PubMedGoogle Scholar
  126. van der Ende A, Hopman CT, Zaat S, Essink BB, Berkhout B, Dankert J (1995) Variable expression of class 1 outer membrane protein in Neisseria meningitides is caused by variation in the spacing between the −10 and −35 regions of the promoter. J Bacteriol 177:2475–2480PubMedGoogle Scholar
  127. van der Woude MW (2006) Re-examining the role and random nature of phase variation. FEMS Microbiol Lett 254:190–197PubMedGoogle Scholar
  128. van der Woude MW, Baumler AJ (2004) Phase and antigenic variation in bacteria. Clin Microbiol Rev 17:581–611PubMedGoogle Scholar
  129. Van Etten JL (2003) Unusual life style of giant chlorella viruses. Annu Rev Genet 37:153–195PubMedGoogle Scholar
  130. van Ham SM, van Alphen L, Mooi FR, van Putten JP (1993) Phase variation of Haemophilus influenzae fimbriae: transcriptional control of two divergent genes through a variable combined promoter region. Cell 73:1187–1196PubMedGoogle Scholar
  131. Vitkute J, Stankevicius K, Tamulaitiene G, Maneliene Z, Timinskas A, Berg DE, Janulaitis A (2001) Specificities of eleven different DNA methyltransferases of Helicobacter pylori strain 26695. J Bacteriol 183:443–450PubMedGoogle Scholar
  132. Waldron DE, Owen P, Dorman CJ (2002) Competitive interaction of the OxyR DNA-binding protein and the Dam methylase at the antigen 43 gene regulatory region in Escherichia coli. Mol Microbiol 44:509–520PubMedGoogle Scholar
  133. Watson ME, Jarisch J, Smith AL (2004) Inactivation of deoxyadenosine methyltransferase (dam) attenuates Haemophilus influenzae virulence. Mol Microbiol 55:651–654Google Scholar
  134. Weiser JN, Williams A, Moxon ER (1990) Phasevariable lipopolysaccharide structures enhance the invasive capacity of Haemophilus influenzae. Infect Immun 58:3455–3457PubMedGoogle Scholar
  135. Wilson GG, Murray NE (1991) Restriction and modification systems. Annu Rev Genet 25:585–627PubMedGoogle Scholar
  136. Wion D, Casadesus J (2006) N6-methyl-adenine: an epigenetic signal for DNA-protein interactions. Nat Rev Microbiol 4:183–192PubMedGoogle Scholar
  137. Wright R, Stephens C, Zweiger G, Shapiro L, Alley MR (1996) Caulobacter Lon protease has a critical role in cell-cycle control of DNA methylation. Genes Dev 10:1532–1542PubMedGoogle Scholar
  138. Xu Q, Stickel S, Roberts RJ, Blaser MJ, Morgan RD (2000) Purification of the novel endonuclease, Hpy188I, and cloning of its restriction-modification genes reveal evidence of its horizontal transfer to the Helicobacter pylori genome. J Biol Chem 275:17086–17093PubMedGoogle Scholar
  139. Yamaki H, Ohtsubo E, Nagai K, Maeda Y (1988) The oriC unwinding by dam methylation in Escherichia coli. Nucleic Acids Res 16:5067–5073PubMedGoogle Scholar
  140. Yarmolinski MB, Sternberg N (1988) Bacteriophage P1. In: Calendar R (ed) The bacteriophages, vol 1. Plenum Press, New York, pp 782–791Google Scholar
  141. Zweiger G, Marczynski G, Shapiro L (1994) A Caulobacter DNA methyltransferase that functions only in the predivisional cell. J Mol Biol 235:472–485PubMedGoogle Scholar

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© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Department of BiochemistryIndian Institute of ScienceBangaloreIndia

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