Genome-wide mapping of methylated adenine residues in pathogenic Escherichia coli using single-molecule real-time sequencing (original) (raw)

Change history

In the version of this article initially published, on p. 1235, line 32, the wrong MTases were given for the motif GATC. Instead of “…GATC (for M.EcoGI and M.EcoGII)…,” it should have read, “…GATC (for M.EcoGV and M.EcoGVII)….” The error has been corrected for the PDF and HTML versions of this article.

References

  1. Kriaucionis, S. & Heintz, N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324, 929–930 (2009).
    Article CAS Google Scholar
  2. Kumar, S. et al. The DNA (cytosine-5) methyltransferases. Nucleic Acids Res. 22, 1–10 (1994).
    Article CAS Google Scholar
  3. Roberts, R.J., Vincze, T., Posfai, J. & Macelis, D. REBASE—a database for DNA restriction and modification: enzymes, genes and genomes. Nucleic Acids Res. 38, D234–D236 (2010).
    Article CAS Google Scholar
  4. Swinton, D. et al. Purification and characterization of the unusual deoxynucleoside, α-_N_-(9-β-D-2′-deoxyribofuranosylpurin-6-yl)glycinamide, specified by the phage Mu modification function. Proc. Natl. Acad. Sci. USA 80, 7400–7404 (1983).
    Article CAS Google Scholar
  5. Tahiliani, M. et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324, 930–935 (2009).
    Article CAS Google Scholar
  6. Warren, R.A. Modified bases in bacteriophage DNAs. Annu. Rev. Microbiol. 34, 137–158 (1980).
    Article CAS Google Scholar
  7. Wyatt, G.R. & Cohen, S.S. A new pyrimidine base from bacteriophage nucleic acids. Nature 170, 1072–1073 (1952).
    Article CAS Google Scholar
  8. Anway, M.D., Cupp, A.S., Uzumcu, M. & Skinner, M.K. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308, 1466–1469 (2005).
    Article CAS Google Scholar
  9. Jirtle, R.L. & Skinner, M.K. Environmental epigenomics and disease susceptibility. Nat. Rev. Genet. 8, 253–262 (2007).
    Article CAS Google Scholar
  10. Kong, A. et al. Parental origin of sequence variants associated with complex diseases. Nature 462, 868–874 (2009).
    Article CAS Google Scholar
  11. Casadesús, J. & Low, D. Epigenetic gene regulation in the bacterial world. Microbiol. Mol. Biol. Rev. 70, 830–856 (2006).
    Article Google Scholar
  12. Collier, J., McAdams, H.H. & Shapiro, L. A DNA methylation ratchet governs progression through a bacterial cell cycle. Proc. Natl. Acad. Sci. USA 104, 17111–17116 (2007).
    Article CAS Google Scholar
  13. Heithoff, D.M., Sinsheimer, R.L., Low, D.A. & Mahan, M.J. An essential role for DNA adenine methylation in bacterial virulence. Science 284, 967–970 (1999).
    Article CAS Google Scholar
  14. Marinus, M.G. & Casadesus, J. Roles of DNA adenine methylation in host-pathogen interactions: mismatch repair, transcriptional regulation, and more. FEMS Microbiol. Rev. 33, 488–503 (2009).
    Article CAS Google Scholar
  15. Stephens, C., Reisenauer, A., Wright, R. & Shapiro, L. A cell cycle-regulated bacterial DNA methyltransferase is essential for viability. Proc. Natl. Acad. Sci. USA 93, 1210–1214 (1996).
    Article CAS Google Scholar
  16. van der Woude, M., Braaten, B. & Low, D. Epigenetic phase variation of the pap operon in Escherichia coli. Trends Microbiol. 4, 5–9 (1996).
    Article CAS Google Scholar
  17. Cokus, S.J. et al. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452, 215–219 (2008).
    Article CAS Google Scholar
  18. Kahramanoglou, C. et al. Genomics of DNA cytosine methylation in Escherichia coli reveals its role in stationary phase transcription. Nat. Commun. 3, 886 (2012).
    Article Google Scholar
  19. Booth, M.J. et al. Quantitative sequencing of 5-methylcytosine and 5-hydroxymethylcytosine at single-base resolution. Science 336, 934–937 (2012).
    Article CAS Google Scholar
  20. Yu, M. et al. Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome. Cell 149, 1368–1380 (2012).
    Article CAS Google Scholar
  21. Schadt, E.E., Turner, S. & Kasarskis, A. A window into third-generation sequencing. Hum. Mol. Genet. 19, R227–R240 (2010).
    Article CAS Google Scholar
  22. Clark, T.A. et al. Characterization of DNA methyltransferase specificities using single-molecule, real-time DNA sequencing. Nucleic Acids Res. 40, e29 (2012).
    Article CAS Google Scholar
  23. Flusberg, B.A. et al. Direct detection of DNA methylation during single-molecule, real-time sequencing. Nat. Methods 7, 461–465 (2010).
    Article CAS Google Scholar
  24. Schadt, E.E. et al. Modeling kinetic rate variation in third generation DNA sequencing data to detect putative modifications to DNA bases. Genome Res. advance online publication, doi:10.1101/gr.136739.111 (23 October 2012).
  25. Roberts, R.J. & Halford, S.E. Type II Restriction Enzymes (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA, 1993).
    Google Scholar
  26. Srikhanta, Y.N. et al. Phasevarions mediate random switching of gene expression in pathogenic Neisseria. PLoS Pathog. 5, e1000400 (2009).
    Article Google Scholar
  27. Reisenauer, A., Kahng, L.S., McCollum, S. & Shapiro, L. Bacterial DNA methylation: a cell cycle regulator? J. Bacteriol. 181, 5135–5139 (1999).
    CAS PubMed PubMed Central Google Scholar
  28. Rasko, D.A. et al. Origins of the E. coli strain causing an outbreak of hemolytic-uremic syndrome in Germany. N. Engl. J. Med. 365, 709–717 (2011).
    Article CAS Google Scholar
  29. Bailey, T.L. et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37, W202–8 (2009).
    Article CAS Google Scholar
  30. Broadbent, S.E., Balbontin, R., Casadesus, J., Marinus, M.G. & van der Woude, M. YhdJ, a nonessential CcrM-like DNA methyltransferase of Escherichia coli and Salmonella enterica. J. Bacteriol. 189, 4325–4327 (2007).
    Article CAS Google Scholar
  31. Wion, D. & Casadesus, J. _N_6-methyl-adenine: an epigenetic signal for DNA-protein interactions. Nat. Rev. Microbiol. 4, 183–192 (2006).
    Article CAS Google Scholar
  32. Low, D.A., Weyand, N.J. & Mahan, M.J. Roles of DNA adenine and methylation in regulating bacterial gene expression and virulence. Infect. Immun. 69, 7197–1204 (2001).
    Article CAS Google Scholar
  33. Camacho, E.M. & Casadesus, J. Regulation of traJ transcription in the Salmonella virulence plasmid by strand-specific DNA adenine hemimethylation. Mol. Microbiol. 57, 1700–1718 (2005).
    Article CAS Google Scholar
  34. Løbner-Olesen, A., Skovgaard, O. & Marinus, M.G. Dam methylation: coordinating cellular processes. Curr. Opin. Microbiol. 8, 154–160 (2005).
    Article Google Scholar
  35. Messer, W. & Noyer-Weidner, M. Timing and targeting: the biological functions of Dam methylation in E. coli. Cell 54, 735–737 (1988).
    Article CAS Google Scholar
  36. Roberts, D., Hoopes, B.C., McClure, W.R. & Kleckner, N. IS10 transposition is regulated by DNA adenine methylation. Cell 43, 117–130 (1985).
    Article CAS Google Scholar
  37. Kaper, J.B., Nataro, J.P. & Mobley, H.L. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2, 123–140 (2004).
    Article CAS Google Scholar
  38. Karam, J.D. & Drake, J.W. Molecular biology of bacteriophage T4 (American Society for Microbiology, Washington, DC, USA, 1994).
  39. Drozdz, M., Piekarowicz, A., Bujnicki, J.M. & Radlinska, M. Novel non-specific DNA adenine methyltransferases. Nucleic Acids Res. 40, 2119–2130 (2012).
    Article CAS Google Scholar
  40. Furuta, Y., Abe, K. & Kobayashi, I. Genome comparison and context analysis reveals putative mobile forms of restriction-modification systems and related rearrangements. Nucleic Acids Res. 38, 2428–2443 (2010).
    Article CAS Google Scholar
  41. Travers, K.J., Chin, C.S., Rank, D.R., Eid, J.S. & Turner, S.W. A flexible and efficient template format for circular consensus sequencing and SNP detection. Nucleic Acids Res. 38, e159 (2010).
    Article Google Scholar
  42. Chin, C.S. et al. The origin of the Haitian cholera outbreak strain. N. Engl. J. Med. 364, 33–42 (2011).
    Article CAS Google Scholar
  43. Korlach, J. et al. Real-time DNA sequencing from single polymerase molecules. Methods Enzymol. 472, 431–455 (2010).
    Article CAS Google Scholar
  44. Bentley, D.R. et al. Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456, 53–59 (2008).
    Article CAS Google Scholar
  45. Robinson, M.D. & Oshlack, A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 11, R25 (2010).
    Article Google Scholar
  46. Huang, W., Sherman, B.T. & Lempicki, R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44–57 (2009).
    Article CAS Google Scholar
  47. Milton, D.L., O'Toole, R., Horstedt, P. & Wolf-Watz, H. Flagellin A is essential for the virulence of Vibrio anguillarum. J. Bacteriol. 178, 1310–1319 (1996).
    Article CAS Google Scholar
  48. Guzman, L.M., Belin, D., Carson, M.J. & Beckwith, J. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177, 4121–4130 (1995).
    Article CAS Google Scholar
  49. Datsenko, K.A. & Wanner, B.L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97, 6640–6645 (2000).
    Article CAS Google Scholar
  50. Kaiser, A.D. & Jacob, F. Recombination between related temperate bacteriophages and the genetic control of immunity and prophage localization. Virology 4, 509–521 (1957).
    Article CAS Google Scholar
  51. Dhillon, T.S. & Dhillon, E.K. Temperate coliphage HK022. Clear plaque mutants and preliminary vegetative map. Jpn. J. Microbiol. 20, 385–396 (1976).
    Article CAS Google Scholar

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Acknowledgements

This study was supported in part by a US National Science Foundation grant IIS0916439 (G.F. and V.K.) and NIH R37 AI-42347 and HHMI (M.K.W.).

Author information

Author notes

  1. Gang Fang and Diana Munera: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Computer Science and Engineering, University of Minnesota, Minneapolis, Minnesota, USA
    Gang Fang & Vipin Kumar
  2. Division of Infectious Diseases, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts, USA
    Diana Munera, Anjali Mandlik, Michael C Chao, Brigid M Davis & Matthew K Waldor
  3. Howard Hughes Medical Institute, Boston, Massachusetts, USA
    Diana Munera, Anjali Mandlik, Michael C Chao, Brigid M Davis & Matthew K Waldor
  4. Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan, USA
    David I Friedman
  5. Pacific Biosciences, Menlo Park, California, USA
    Onureena Banerjee, Tyson A Clark, Khai Luong, Jonas Korlach & Steve W Turner
  6. Department of Statistics, Stanford University, Stanford, California, USA
    Zhixing Feng
  7. Tsinghua National Laboratory for Information Science and Technology, Tsinghua University, Beijing, China
    Zhixing Feng
  8. Department of Automation, Tsinghua University, Beijing, China
    Zhixing Feng
  9. Department of Genetics and Genomic Sciences, Mount Sinai School of Medicine, New York, New York, USA
    Bojan Losic, Milind C Mahajan, Omar J Jabado, Gintaras Deikus, Alona Keren-Paz, Andrew Chess & Eric E Schadt
  10. New England Biolabs, Inc., Ipswich, Massachusetts, USA
    Iain A Murray & Richard J Roberts

Authors

  1. Gang Fang
  2. Diana Munera
  3. David I Friedman
  4. Anjali Mandlik
  5. Michael C Chao
  6. Onureena Banerjee
  7. Zhixing Feng
  8. Bojan Losic
  9. Milind C Mahajan
  10. Omar J Jabado
  11. Gintaras Deikus
  12. Tyson A Clark
  13. Khai Luong
  14. Iain A Murray
  15. Brigid M Davis
  16. Alona Keren-Paz
  17. Andrew Chess
  18. Richard J Roberts
  19. Jonas Korlach
  20. Steve W Turner
  21. Vipin Kumar
  22. Matthew K Waldor
  23. Eric E Schadt

Contributions

G.F., D.M., M.K.W. and E.E.S. designed the experiments; G.F., D.M., D.I.F., A.M., M.C.C., O.B., Z.F., I.A.M., A.K.-P., A.C., R.J.R., J.K., S.W.T., V.K., M.K.W. and E.E.S. designed the methods; D.M., D.I.F., A.M., M.C.C., M.C.M., O.J.J., G.D., T.A.C., K.L., I.A.M., A.K.-P. and A.C. carried out all sample-preparation experiments, all sequencing runs and all validation experiments; G.F., D.M., D.I.F., A.M., M.C.C., O.B., Z.F., B.L., I.A.M., B.M.D., A.K.-P., A.C., R.J.R., V.K., M.K.W. and E.E.S. jointly analyzed the data sets; and G.F., D.M., D.I.F., A.M., M.C.C., M.C.M., O.J.J., T.A.C., B.M.D., A.K.-P., A.C., R.J.R., J.K., M.K.W. and E.E.S. wrote the manuscript.

Corresponding authors

Correspondence toMatthew K Waldor or Eric E Schadt.

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Competing interests

O.B., T.A.C., K.L., J.K., S.W.T. and E.E.S. are employees or consultants for and own stock in Pacific Biosciences.

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Fang, G., Munera, D., Friedman, D. et al. Genome-wide mapping of methylated adenine residues in pathogenic Escherichia coli using single-molecule real-time sequencing.Nat Biotechnol 30, 1232–1239 (2012). https://doi.org/10.1038/nbt.2432

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