Skip to main content
SpringerLink
Log in

Selection againstdam methylation sites in the genomes of DNA of enterobacteriophages

  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Summary

Postreplicative methylation of adenine inEscherichia coli DNA to produce G6m ATC (where6mA is 6-methyladenine) has been associated with preferential daughter-strand repair and possibly regulation of replication. An analysis was undertaken to determine if these, or other, as yet unknown roles of GATC, have had an effect on the frequency of GATC inE. coli or bacteriophage DNA. It was first ascertained that the most accurate predictions of GATC frequency were based on the observed frequencies of GAT and ATC, which would be expected since these predictors take into account preferences in codon usage. The predicted frequencies were compared with observed GATC frequencies in all available bacterial and phage nucleotide sequences. The frequency of GATC was close to the predicted frequency in most genes ofE. coli and its RNA bacteriophages and in the genes of nonenteric bacteria and their bacteriophages. However, for DNA enterobacteriophages the observed frequency of DNA enterobacteriophages the observed frequency of GATC was generally significantly lower than predicted when assessed by the chi square test. No elevation in the rate of mutation of6mA in GATC relative to other bases was found when pairs of DNA sequences from closely related phages or pairs of homologous genes from enterobacteria were compared, nor was any preferred pathway for mutation of6mA evident in theE. coli DNA bacteriophages. This situation contrasts with that of 5-methylcytosine, which is hypermutable, with a preferred pathway to thymine. Thus, the low level of GATC in enterobacteriophages is probably due not to6mA hypermutability, but to selection against GATC in order to bypass a GATC-mediated host function.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bauer J, Krammer G, Knippers R (1981) Asymmetric repair of bacteriophage T7 heteroduplex DNA. Mol Gen Genet 181:541–547

    Article  PubMed  Google Scholar 

  • Brooks JE, Blumenthal RM, Gingeras TR (1983) The isolation and characterization of theE. coli DNA adenine methylase (Dam) gene. Nucleic Acids Res 11:837–851

    PubMed  Google Scholar 

  • Coulondre C, Miller JH, Farabaugh PJ, Gilbert W (1978) Molecular basis of base substitution hot spots inE. coli. Nature 274:775–780

    Article  PubMed  Google Scholar 

  • Dreiseikelmann B, Wackernagel W (1981) Absence inBacillus subtilis andStaphylococcus aureus of the sequence specific DNA methylase that is conferred inE. coli K-12 by thedam anddcm enzymes. J Bacteriol 147:259–261

    PubMed  Google Scholar 

  • Dreiseikelmann B, Eichenlaub R, Wackernagel W (1979) The effect of differential methylation byE. coli of plasmid DNA and phage T7 DNA on the cleavage by restriction endonucleaseMbo I. Biochim Biophys Acta 562:418–428

    PubMed  Google Scholar 

  • Dunn JJ, Studier FW (1983) The complete nucleotide sequence of bacteriophage T7 DNA and the location of the T7 genetic elements. J Mol Biol 166:477–535

    PubMed  Google Scholar 

  • Glickman BW, Radman M (1980)E. coli mutator mutants deficient in methylation instructed DNA mismatch correction. Proc Natl Acad Sci USA 77:1063–1067

    PubMed  Google Scholar 

  • Gomez-Eichelmann MC (1979) DNA adenine and cytosine methylation inSalmonella typhimurium andS. typhi. J Bacteriol 140:574–579

    PubMed  Google Scholar 

  • Gram H, Liebig H-D, Hack A, Niggemann E, Ruger W (1984) The physical map of bacteriophage T4 including the positions of promoters and terminators recognizedin vitro. Mol Gen Genet 194:232–240

    Article  PubMed  Google Scholar 

  • Hansen EB, Hansen FG, Von Meyenberg K (1982) the nucleotide sequence of the DNA A gene and the first part of the DNA N gene ofE. coli. Nucleic Acids Res. 10:7373–7385

    PubMed  Google Scholar 

  • Hattman S (1970) DNA methylation of T-even bacteriophage and of their nonglucosylated mutants—its role in P1 directed restriction. Virology 42:359–367

    Article  PubMed  Google Scholar 

  • Hattman S (1979) Unusual modification of bacteriophage Mu DNA. J Virol 32:468–475

    PubMed  Google Scholar 

  • Hattman S (1982) DNA methyltransferase-dependent transcription of the phage Mumom gene. Proc Natl Acad Sci USA 79:5518–5521

    PubMed  Google Scholar 

  • Hattman S, Brooks JE, Masurekar M (1978) Sequence specificity of the P1-modification methylase (M. Eco PI) and DNA methylase (M.Eco dam) controlled by theE. coli dam gene. J Mol Biol 126:367–380

    Article  PubMed  Google Scholar 

  • Herman GE, Modrich P (1981)E. coli K-12 clones that overproducedam methylase are hypermutable. J Bacteriol 145:644–646

    PubMed  Google Scholar 

  • Ito J, Roberts RJ (1979) Unusual base sequence arrangement in phage phi-29 DNA. Gene 5:1–7

    Article  PubMed  Google Scholar 

  • Korba BE, Hays JB (1982) Novel mutations ofE. coli that produce recombinogenic lesions in DNA. 5. Recombinogenic plasmids fromArl mutants ofE. coli are unusually sensitive to S1 and partially deficient in cytosine methylation at CC(A/T)GG. J Mol Biol 157:213–235

    Article  PubMed  Google Scholar 

  • Lundahl T (1982) DNA repair enzymes. Annu Rev Biochem 51:61–87

    Article  PubMed  Google Scholar 

  • Marinus MG, Konrad B (1976) Hyper-recombinogenicdam mutants ofE. coli K-12. Mol Gen Genet 149:273–277

    Article  PubMed  Google Scholar 

  • Marinus MG, Morris NR (1974) Biological function for 6mA residues in DNA ofE. coli K-12. J Mol Biol 85:309–322

    Article  PubMed  Google Scholar 

  • Marinus MG, Carraway M, Frey AZ, Brown L, Arraj JA (1983) Insertion mutations in thedam gene ofE. coli K-12. Mol Gen Genet 192:288–289

    Article  PubMed  Google Scholar 

  • McClelland M (1983) The effect of site specific methylation on restriction endonuclease cleavage (update). Nucleic Acids Res 11:r169-r173

    PubMed  Google Scholar 

  • Meijer M, Beck E, Hansen FG, Bergmans HEN, Messer W, Von Mayenburg K, Schaller H (1979) Nucleotide sequence of the origin of replication of theE. coli K-12 chromosome. Proc Natl Acad Sci USA 76:580–584

    PubMed  Google Scholar 

  • Plasterk RHA, Vollering M, Brinkman A, van de Putte P (1984) Analysis of the methylation-regulated mumom transcript. Cell 36:189–196

    Article  PubMed  Google Scholar 

  • Pukkila PJ, Peterson J, Herman G, Modrich P, Meselson M (1983) Effects of high levels of DNA adenine methylation on methyl-directed mismatch repair inE. coli. Genetics 104:571–582

    PubMed  Google Scholar 

  • Reeve JN, Amann E, Tailor R, Gunthert U, Scholz K, Trautner TA (1980) Unusual behaviour of SPO1 DNA with respect to restriction and modification enzymes recognizing the sequence GGCC. Mol Gen Genet 178:229–231

    Article  PubMed  Google Scholar 

  • Sechaud J, Strisinger G, Emrich J, Newton H, Langford H, Reinhold H, Stahl M (1965) Chromosome structure and phage T4. II. Terminal redundancies in heterozygotes. Proc Natl Acad Sci USA 54:1333–1339

    PubMed  Google Scholar 

  • Sinha NK, Goodman MF (1983) Fidelity of DNA replication. In: Mattews CK, Kutter EM, Mosig G, Berget PB (eds) Bacteriophage T4. American Society of Microbiology, Washington DC, pp 131–137

    Google Scholar 

  • Smith HO, Kelly SV (1983) Methylases of the type II. Restriction-modification system. In: Razin A, Cedar H, Riggs AD (eds) DNA methylation and its biological significance. Springer-Verlag, New York, pp 39–72

    Google Scholar 

  • Sugimoto K, Oka A, Sugisaki H, Takanami M, Nishimura A, Yasuda S, Hirota A (1979) Nucleotide sequence of theE. coli K-12 replication origin. Proc Natl Acad Sci USA 76:575–579

    PubMed  Google Scholar 

  • Szyf M, Gruenbaum Y, Urieli-Shoval S, Razin A (1982) Studies on the biological role of DNA methylation. 5. The pattern ofE. coli DNA methylation. Nucleic Acids Res 10:7247–7259

    PubMed  Google Scholar 

  • Zyskind JW, Smith DW (1980) Nucleotide sequence of theSalmonella typhimurium origin of DNA replication. Proc Natl Acad Sci USA 77:2460–2464

    PubMed  Google Scholar 

  • Zyskind JW, Cleary JM, Brusilow WS, Harding NE, Smith DW (1983) Chromosomal replication origin from the marine bacteriumVibrio harveyi functions inE. coli-Ori C consensus sequence. Proc Natl Acad Sci USA 80:1164–1168

    PubMed  Google Scholar 

Download references

Author information

Author notes

  1. Michael McClelland

    Present address: Department of Human Genetics and Development, College of Physicians and Surgeons of Columbia University, 701 West 168th St., 10032, New York, New York, USA

Authors and Affiliations

  1. Department of Biochemistry, University of California, 94720, Berkeley, California, USA

    Michael McClelland

Authors
  1. Michael McClelland
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

McClelland, M. Selection againstdam methylation sites in the genomes of DNA of enterobacteriophages. J Mol Evol 21, 317–322 (1985). https://doi.org/10.1007/BF02115649

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02115649

Key words

Search

Navigation