Methylome Diversification through Changes in DNA Methyltransferase Sequence Specificity

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Living organisms are affected by epigenetic variation in addition to DNA sequence variation. DNA methylation is one of the most studied epigenetic modifications in both prokaryotes and eukaryotes. In prokaryotes, most DNA methylation is by DNA methyltransferases with high sequence specificity. Helicobacter pylori, a human stomach pathogen responsible for stomach cancer and other diseases, carries a large number of DNA methyltransferase genes that vary among strains. In this work, we examined the distribution of DNA methylation in multiple H. pylori genomes using single-molecule real-time sequencing technology, which detects DNA methylation with single-base resolution. Comparison of methylation motifs between closely related genomes allowed assignment of a recognition sequence to each DNA methylation specificity-determining gene. Highly methylated genes were detected, although the general DNA methylation pattern varied among strains. Knockout of a methylation specificity-determining gene led to changes in the transcriptome. These findings are consistent with our hypothesis that changes in the methylome lead to changes in the transcriptome and to changes in phenotypes, providing potential targets for natural and artificial selection in adaptive evolution.

Vyšlo v časopise: Methylome Diversification through Changes in DNA Methyltransferase Sequence Specificity. PLoS Genet 10(4): e32767. doi:10.1371/journal.pgen.1004272
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004272

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Zdroje

1. PoetschAR, PlassC (2011) Transcriptional regulation by DNA methylation. Cancer Treat Rev 37 Suppl 1S8–12.

2. SuzukiMM, BirdA (2008) DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 9: 465–476.

3. WionD, CasadesusJ (2006) N6-methyl-adenine: an epigenetic signal for DNA-protein interactions. Nat Rev Microbiol 4: 183–192.

4. LowDA, CasadesusJ (2008) Clocks and switches: bacterial gene regulation by DNA adenine methylation. Curr Opin Microbiol 11: 106–112.

5. OshimaT, WadaC, KawagoeY, AraT, MaedaM, et al. (2002) Genome-wide analysis of deoxyadenosine methyltransferase-mediated control of gene expression in Escherichia coli. Mol Microbiol 45: 673–695.

6. KahramanoglouC, PrietoAI, KhedkarS, HaaseB, GuptaA, et al. (2012) Genomics of DNA cytosine methylation in Escherichia coli reveals its role in stationary phase transcription. Nat Commun 3: 886.

7. Pingoud A (2004) Restriction endonucleases. Berlin: Springer Verlag. 443 p.

8. RobertsRJ, BelfortM, BestorT, BhagwatAS, BickleTA, et al. (2003) A nomenclature for restriction enzymes, DNA methyltransferases, homing endonucleases and their genes. Nucleic Acids Res 31: 1805–1812.

9. MorganRD, DwinellEA, BhatiaTK, LangEM, LuytenYA (2009) The MmeI family: type II restriction-modification enzymes that employ single-strand modification for host protection. Nucleic Acids Res 37: 5208–5221.

10. RobertsRJ, VinczeT, PosfaiJ, MacelisD (2010) REBASE—a database for DNA restriction and modification: enzymes, genes and genomes. Nucleic Acids Res 38: D234–236.

11. DrydenDTF, MurrayNE, RaoDN (2001) Nucleoside triphosphate-dependent restriction enzymes. Nucleic Acids Res 29: 3728–3741.

12. MurrayNE (2000) Type I restriction systems: sophisticated molecular machines (a legacy of Bertani and Weigle). Microbiol Mol Biol Rev 64: 412–434.

13. FurutaY, AbeK, KobayashiI (2010) Genome comparison and context analysis reveals putative mobile forms of restriction-modification systems and related rearrangements. Nucleic Acids Res 38: 2428–2443.

14. FurutaY, KobayashiI (2012) Mobility of DNA sequence recognition domains in DNA methyltransferases suggests epigenetics-driven adaptive evolution. Mob Genet Elements 2: 292–296.

15. ValeFF, MegraudF, VitorJM (2009) Geographic distribution of methyltransferases of Helicobacter pylori: evidence of human host population isolation and migration. BMC Microbiol 9: 193.

16. AlmRA, LingLS, MoirDT, KingBL, BrownED, et al. (1999) Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397: 176–180.

17. KawaiM, FurutaY, YaharaK, TsuruT, OshimaK, et al. (2011) Evolution in an oncogenic bacterial species with extreme genome plasticity: Helicobacter pylori East Asian genomes. BMC Microbiol 11: 104.

18. FurutaY, KawaiM, UchiyamaI, KobayashiI (2011) Domain movement within a gene: A novel evolutionary mechanism for protein diversification. PLoS One 6: e18819.

19. FurutaY, KobayashiI (2012) Movement of DNA sequence recognition domains between non-orthologous proteins. Nucleic Acids Res 40: 9218–9232.

20. SrikhantaYN, GorrellRJ, SteenJA, GawthorneJA, KwokT, et al. (2011) Phasevarion Mediated Epigenetic Gene Regulation in Helicobacter pylori. PLoS One 6: e27569.

21. PriceC, LingnerJ, BickleTA, FirmanK, GloverSW (1989) Basis for changes in DNA recognition by the EcoR124 and EcoR124/3 type I DNA restriction and modification enzymes. J Mol Biol 205: 115–125.

22. Fuller-PaceFV, BullasLR, DeliusH, MurrayNE (1984) Genetic recombination can generate altered restriction specificity. Proc Natl Acad Sci U S A 81: 6095–6099.

23. GannAA, CampbellAJ, CollinsJF, CoulsonAF, MurrayNE (1987) Reassortment of DNA recognition domains and the evolution of new specificities. Mol Microbiol 1: 13–22.

24. GublerM, BragugliaD, MeyerJ, PiekarowiczA, BickleTA (1992) Recombination of constant and variable modules alters DNA sequence recognition by type IC restriction-modification enzymes. EMBO J 11: 233–240.

25. Roberts GA, Houston PJ, White JH, Chen K, Stephanou AS, et al.. (2013) Impact of target site distribution for Type I restriction enzymes on the evolution of methicillin-resistant Staphylococcus aureus (MRSA) populations. Nucleic Acids Research.

26. JanscakP, BickleTA (1998) The DNA recognition subunit of the type IB restriction-modification enzyme EcoAI tolerates circular permutions of its polypeptide chain. J Mol Biol 284: 937–948.

27. ThorpePH, TernentD, MurrayNE (1997) The specificity of sty SKI, a type I restriction enzyme, implies a structure with rotational symmetry. Nucleic Acids Res 25: 1694–1700.

28. LinLF, PosfaiJ, RobertsRJ, KongH (2001) Comparative genomics of the restriction-modification systems in Helicobacter pylori. Proc Natl Acad Sci U S A 98: 2740–2745.

29. Kumar R, Mukhopadhyay AK, Rao DN (2010) Characterization of an N(6) adenine methyltransferase from Helicobacter pylori strain 26695 which methylates adjacent adenines on the same strand. FEBS J.

30. NagarajaV, ShepherdJC, BickleTA (1985) A hybrid recognition sequence in a recombinant restriction enzyme and the evolution of DNA sequence specificity. Nature 316: 371–372.

31. PiekarowiczA, GoguenJD (1986) The DNA sequence recognized by the EcoDXX1 restriction endonuclease. Eur J Biochem 154: 295–298.

32. RyuJ, RowsellE (2008) Quick identification of Type I restriction enzyme isoschizomers using newly developed pTypeI and reference plasmids. Nucleic Acids Res 36: e81.

33. FlusbergBA, WebsterDR, LeeJH, TraversKJ, OlivaresEC, et al. (2010) Direct detection of DNA methylation during single-molecule, real-time sequencing. Nat Methods 7: 461–465.

34. ClarkTA, MurrayIA, MorganRD, KislyukAO, SpittleKE, et al. (2012) Characterization of DNA methyltransferase specificities using single-molecule, real-time DNA sequencing. Nucleic Acids Res 40: e29.

35. FangG, MuneraD, FriedmanDI, MandlikA, ChaoMC, et al. (2012) Genome-wide mapping of methylated adenine residues in pathogenic Escherichia coli using single-molecule real-time sequencing. Nat Biotechnol 30: 1232–1239.

36. Lluch-SenarM, LuongK, Llorens-RicoV, DelgadoJ, FangG, et al. (2013) Comprehensive methylome characterization of Mycoplasma genitalium and Mycoplasma pneumoniae at single-base resolution. PLoS Genet 9: e1003191.

37. MurrayIA, ClarkTA, MorganRD, BoitanoM, AntonBP, et al. (2012) The methylomes of six bacteria. Nucleic Acids Res 40: 11450–11462.

38. KhosraviY, RehvathyV, WeeWY, WangS, BaybayanP, et al. (2013) Comparing the genomes of Helicobacter pylori clinical strain UM032 and Mice-adapted derivatives. Gut Pathog 5: 25.

39. Krebes J, Morgan RD, Bunk B, Sproer C, Luong K, et al.. (2013) The complex methylome of the human gastric pathogen Helicobacter pylori. Nucleic Acids Res: 10.1093/nar/gkt1201.

40. FischerW, WindhagerL, RohrerS, ZeillerM, KarnholzA, et al. (2010) Strain-specific genes of Helicobacter pylori: genome evolution driven by a novel type IV secretion system and genomic island transfer. Nucleic Acids Res 38: 6089–6101.

41. YaharaK, FurutaY, OshimaK, YoshidaM, AzumaT, et al. (2013) Chromosome painting in silico in a bacterial species reveals fine population structure. Mol Biol Evol 30: 1454–1464.

42. FurutaY, KawaiM, YaharaK, TakahashiN, HandaN, et al. (2011) Birth and death of genes linked to chromosomal inversion. Proc Natl Acad Sci U S A 108: 1501–1506.

43. TakataT, ArasR, TavakoliD, AndoT, OlivaresAZ, et al. (2002) Phenotypic and genotypic variation in methylases involved in type II restriction-modification systems in Helicobacter pylori. Nucleic Acids Res 30: 2444–2452.

44. BarrozoRM, CookeCL, HansenLM, LamAM, GaddyJA, et al. (2013) Functional plasticity in the type IV secretion system of Helicobacter pylori. PLoS Pathog 9: e1003189.

45. KersulyteD, LeeW, SubramaniamD, AnantS, HerreraP, et al. (2009) Helicobacter Pylori's plasticity zones are novel transposable elements. PLoS One 4: e6859.

46. GelfandMS, KooninEV (1997) Avoidance of palindromic words in bacterial and archaeal genomes: a close connection with restriction enzymes. Nucleic Acids Res 25: 2430–2439.

47. KarlinS, CampbellAM, MrazekJ (1998) Comparative DNA analysis across diverse genomes. Annu Rev Genet 32: 185–225.

48. RochaEP, ViariA, DanchinA (1998) Oligonucleotide bias in Bacillus subtilis: general trends and taxonomic comparisons. Nucleic Acids Res 26: 2971–2980.

49. KatoM, MiuraA, BenderJ, JacobsenSE, KakutaniT (2003) Role of CG and non-CG methylation in immobilization of transposons in Arabidopsis. Curr Biol 13: 421–426.

50. ChinenA, UchiyamaI, KobayashiI (2000) Comparison between Pyrococcus horikoshii and Pyrococcus abyssi genome sequences reveals linkage of restriction-modification genes with large genome polymorphisms. Gene 259: 109–121.

51. HumbertO, SalamaNR (2008) The Helicobacter pylori HpyAXII restriction-modification system limits exogenous DNA uptake by targeting GTAC sites but shows asymmetric conservation of the DNA methyltransferase and restriction endonuclease components. Nucleic Acids Res 36: 6893–6906.

52. OhnoS, HandaN, Watanabe-MatsuiM, TakahashiN, KobayashiI (2008) Maintenance forced by a restriction-modification system can be modulated by a region in its modification enzyme not essential for methyltransferase activity. J Bacteriol 190: 2039–2049.

53. MaloneT, BlumenthalRM, ChengX (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: 618–632.

54. AltschulSF, GishW, MillerW, MyersEW, LipmanDJ (1990) Basic local alignment search tool. J Mol Biol 215: 403–410.

55. MorganRD, LuytenYA (2009) Rational engineering of type II restriction endonuclease DNA binding and cleavage specificity. Nucleic Acids Res 37: 5222–5233.

56. SharmaCM, HoffmannS, DarfeuilleF, ReignierJ, FindeissS, et al. (2010) The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464: 250–255.

57. YaharaK, KawaiM, FurutaY, TakahashiN, HandaN, et al. (2012) Genome-wide survey of mutual homologous recombination in a highly sexual bacterial species. Genome Biol Evol 4: 628–640.

58. SasaiN, DefossezPA (2009) Many paths to one goal? The proteins that recognize methylated DNA in eukaryotes. Int J Dev Biol 53: 323–334.

59. VitorianoI, VítorJMB, OleastroM, Roxo-RosaM, ValeFF (2013) Proteome variability among Helicobacter pylori isolates clustered according to genomic methylation. Journal of Applied Microbiology 114: 1817–1832.

60. PalmerGH, BankheadT, LukehartSa (2009) ‘Nothing is permanent but change’- antigenic variation in persistent bacterial pathogens. Cellular microbiology 11: 1697–1705.

61. HeuermannD, HaasR (1998) A stable shuttle vector system for efficient genetic complementation of Helicobacter pylori strains by transformation and conjugation. Mol Gen Genet 257: 519–528.

62. BereswillS, SchonenbergerR, van VlietAH, KustersJG, KistM (2005) Novel plasmids for gene expression analysis and for genetic manipulation in the gastric pathogen Helicobacter pylori. FEMS Immunol Med Microbiol 44: 157–162.

63. SchadtEE, BanerjeeO, FangG, FengZ, WongWH, et al. (2013) Modeling kinetic rate variation in third generation DNA sequencing data to detect putative modifications to DNA bases. Genome Res 23: 129–141.

64. MachanickP, BaileyTL (2011) MEME-ChIP: motif analysis of large DNA datasets. Bioinformatics 27: 1696–1697.

65. AndersS, HuberW (2010) Differential expression analysis for sequence count data. Genome Biol 11: R106.

66. KrzywinskiM, ScheinJ, BirolI, ConnorsJ, GascoyneR, et al. (2009) Circos: an information aesthetic for comparative genomics. Genome Res 19: 1639–1645.