1887

Abstract

The type I restriction–modification () systems of 73 strains were characterized according to their DNA and amino acid sequences, and/or gene organization. A number of new genes were identified which are not present in the sequenced strain NCTC 11168. The closely related organism has three type I systems; however, no evidence was found that strains contain multiple type I systems, although loci are present in at least two different chromosomal locations. Also, unlike , intervening ORFs are present, in some strains, between and and between and . No definitive function can be ascribed to these ORFs, designated here as (-inked RF) and (-inked RF). Based on parsimony analysis of amino acid sequences to assess character relatedness, the type I R–M systems are assigned to one of three families: ‘IAB’, ‘IC’ or ‘IF’. This study confirms that HsdM proteins within a family are highly conserved but share little homology with HsdM proteins from other families. The ‘IC’ loci are >99 % identical at the nucleotide level, as are the ‘IF’ loci. Additionally, whereas the nucleotide sequences of the ‘IAB’ and genes show a high degree of similarity, the nucleotide sequences of the ‘IAB’ and genes vary considerably. This diversity suggests that recombination between ‘IAB’ loci would lead not only to new alleles but also to the exchange of genes; five loci are presumably the result of such recombination. The importance of these findings with regard to the evolution of type I R–M systems is discussed.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27327-0
2005-02-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/151/2/mic1510337.html?itemId=/content/journal/micro/10.1099/mic.0.27327-0&mimeType=html&fmt=ahah

References

  1. Alm R. A., Ling L. S., Moir D. T. 20 other authors 1999; Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori . Nature 397:176–180 [CrossRef]
    [Google Scholar]
  2. Arber W., Wauters-Willems D. 1970; Host specificity of DNA produced by Escherichia coli. XII. The two restriction and modification systems of strain 15T. Mol Gen Genet 108:203–217
    [Google Scholar]
  3. Bickle T. A. 1993; The ATP-dependent restriction enzymes. In Nucleases Cold Spring Harbor Monograph Series no. 25) , 2nd edn. pp 89–109 Edited by Linn S. M. R. S. L., Roberts R. J. Plainview, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  4. Bickle T. A., Kruger D. H. 1993; Biology of DNA restriction. Microbiol Rev 57:434–450
    [Google Scholar]
  5. Black R. E., Levine M. M., Clements M. L., Hughes T. P., Blaser M. J. 1988; Experimental Campylobacter jejuni infection in humans. J Infect Dis 157:472–479 [CrossRef]
    [Google Scholar]
  6. Bullas L. R., Colson C., Van Pel A. 1976; DNA restriction and modification systems in Salmonella. SQ, a new system derived by recombination between the SB system ofSalmonella typhimurium and the SP system of Salmonella potsdam . J Gen Microbiol 95:166–172 [CrossRef]
    [Google Scholar]
  7. Chang N., Taylor D. E. 1990; Use of pulsed-field agarose gel electrophoresis to size genomes of Campylobacter species and to construct a SalI map of Campylobacter jejuni UA580. J Bacteriol 172:5211–5217
    [Google Scholar]
  8. Chen A., Powell L. M., Dryden D. T., Murray N. E., Brown T. 1995; Tyrosine 27 of the specificity polypeptide of EcoKI can be UV crosslinked to a bromodeoxyuridine-substituted DNA target sequence. Nucleic Acids Res 23:1177–1183 [CrossRef]
    [Google Scholar]
  9. Daniel A. S., Fuller-Pace F. V., Legge D. M., Murray N. E. 1988; Distribution and diversity of hsd genes in Escherichia coli and other enteric bacteria. J Bacteriol 170:1775–1782
    [Google Scholar]
  10. de Boer P., Wagenaar J. A., Achterberg R. P., Putten J. P., Schouls L. M., Duim B. 2002; Generation of Campylobacter jejuni genetic diversity in vivo . Mol Microbiol 44:351–359 [CrossRef]
    [Google Scholar]
  11. Deng Y. M., Liu C. Q., Dunn N. W. 1999; Genetic organization and functional analysis of a novel phage abortive infection system, AbiL, from Lactococcus lactis . J Biotechnol 67:135–149 [CrossRef]
    [Google Scholar]
  12. Donahue J. P., Peek R. M. 2001; Restriction and modification systems. In Helicobacter pylori: Physiology and Genetics pp 269–276 Edited by Mobley H. L. T., Mendz G. L., Hazell S. L. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  13. Dybvig K., Yu H. 1994; Regulation of a restriction and modification system via DNA inversion in Mycoplasma pulmonis. Mol Microbiol 12:547–560 [CrossRef]
    [Google Scholar]
  14. Engberg J., Nachamkin I., Fussing V., McKhann G. M., Griffin J. W., Piffaretti J. C., Nielsen E. M., Gerner-Smidt P. 2001; Absence of clonality of Campylobacter jejuni in serotypes other than HS : 19 associated with Guillain-Barré syndrome and gastroenteritis. J Infect Dis 184:215–220 [CrossRef]
    [Google Scholar]
  15. Firman K., Creasey W. A., Watson G., Price C., Glover S. W. 1983; Genetic and physical studies of restriction-deficient mutants of the Inc FIV plasmids R124 and R124/3. Mol Gen Genet 191:145–153 [CrossRef]
    [Google Scholar]
  16. Fuller-Pace F. V., Murray N. E. 1986; Two DNA recognition domains of the specificity polypeptides of a family of type I restriction enzymes. Proc Natl Acad Sci U S A 83:9368–9372 [CrossRef]
    [Google Scholar]
  17. Fuller-Pace F. V., Bullas L. R., Delius H., Murray N. E. 1984; Genetic recombination can generate altered restriction specificity. Proc Natl Acad Sci U S A 81:6095–6099 [CrossRef]
    [Google Scholar]
  18. Fuller-Pace F. V., Cowan G. M., Murray N. E. 1985; EcoA and EcoE: alternatives to the EcoK family of type I restriction and modification systems of Escherichia coli. J Mol Biol 186:65–75 [CrossRef]
    [Google Scholar]
  19. Gann A. A., Campbell A. J., Collins J. F., Coulson A. F., Murray N. E. 1987; Reassortment of DNA recognition domains and the evolution of new specificities. Mol Microbiol 1:13–22 [CrossRef]
    [Google Scholar]
  20. Gubler M., Braguglia D., Meyer J., Piekarowicz A., Bickle T. A. 1992; Recombination of constant and variable modules alters DNA sequence recognition by type IC restriction-modification enzymes. EMBO J 11:233–240
    [Google Scholar]
  21. Kaneko T., Nakamura Y., Wolk C. P. 19 other authors 2001; Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res 8:205–213 227–253
    [Google Scholar]
  22. Kannan P., Cowan G. M., Daniel A. S., Gann A. A., Murray N. E. 1989; Conservation of organization in the specificity polypeptides of two families of type I restriction enzymes. J Mol Biol 209:335–344 [CrossRef]
    [Google Scholar]
  23. Kapatral V., Anderson I., Ivanova N. 22 other authors 2002; Genome sequence and analysis of the oral bacterium Fusobacterium nucleatum strain ATCC 25586. J Bacteriol 184:2005–2018 [CrossRef]
    [Google Scholar]
  24. Kong H., Lin L. F., Porter N., Stickel S., Byrd D., Posfai J., Roberts R. J. 2000; Functional analysis of putative restriction-modification system genes in the Helicobacter pylori J99 genome. Nucleic Acids Res 28:3216–3223 [CrossRef]
    [Google Scholar]
  25. Korlath J. A., Osterholm M. T., Judy L. A., Forfang J. C., Robinson R. A. 1985; A point-source outbreak of campylobacteriosis associated with consumption of raw milk. J Infect Dis 152:592–596 [CrossRef]
    [Google Scholar]
  26. Kumar S., Tamura K., Jakobsen I. B., Nei M. 2001; mega2 - molecular evolutionary genetics analysis software. Bioinformatics 17:1244–1245 [CrossRef]
    [Google Scholar]
  27. Miller W. G., Bates A. H., Horn S. T., Brandl M. T., Wachtel M. R., Mandrell R. E. 2000; Detection on surfaces and in Caco-2 cells of Campylobacter jejunicells transformed with new gfp, yfp, and cfp marker plasmids. Appl Environ Microbiol 66:5426–5436 [CrossRef]
    [Google Scholar]
  28. Murray N. E. 2000; Type I restriction systems: sophisticated molecular machines (a legacy of Bertani and Weigle. Microbiol Mol Biol Rev 64:412–434 [CrossRef]
    [Google Scholar]
  29. Murray N. E., Gough J. A., Suri B., Bickle T. A. 1982; Structural homologies among type I restriction-modification systems. EMBO J 1:535–539
    [Google Scholar]
  30. Nachamkin I., Engberg J., Gutacker M. & 10 other authors; 2001; Molecular population genetic analysis of Campylobacter jejuni HS : 19 associated with Guillain-Barre syndrome and gastroenteritis. J Infect Dis 184:221–226 [CrossRef]
    [Google Scholar]
  31. Nagaraja V., Shepherd J. C., Bickle T. A. 1985; A hybrid recognition sequence in a recombinant restriction enzyme and the evolution of DNA sequence specificity. Nature 316:371–372 [CrossRef]
    [Google Scholar]
  32. Parkhill J., Wren B. W., Mungall K. & 18 other authors; 2000; The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403:665–668 [CrossRef]
    [Google Scholar]
  33. Penner J. L., Hennessy J. N., Congi R. V. 1983; Serotyping of Campylobacter jejuni and Campylobacter coli on the basis of thermostable antigens. Eur J Clin Microbiol 2:378–383 [CrossRef]
    [Google Scholar]
  34. Petersen L., Larsen T. S., Ussery D. W., On S. L., Krogh A. 2003; RpoD promoters in Campylobacter jejuni exhibit a strong periodic signal instead of a −35 box. J Mol Biol 326:1361–1372 [CrossRef]
    [Google Scholar]
  35. Piekarowicz A., Klyz A., Kwiatek A., Stein D. C. 2001; Analysis of type I restriction modification systems in the Neisseriaceae: genetic organization and properties of the gene products. Mol Microbiol 41:1199–1210
    [Google Scholar]
  36. Price C., Pripfl T., Bickle T. A. 1987; EcoR124 and EcoR124/3: the first members of a new family of type I restriction and modification systems. Eur J Biochem 167:111–115 [CrossRef]
    [Google Scholar]
  37. Price C., Lingner J., Bickle T. A., Firman K., Glover S. W. 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 [CrossRef]
    [Google Scholar]
  38. Rasmussen M., Bjorck L. 2001; Unique regulation of SclB – a novel collagen-like surface protein of Streptococcus pyogenes. Mol Microbiol 40:1427–1438 [CrossRef]
    [Google Scholar]
  39. Redaschi N., Bickle T. A. 1996; DNA restriction and modification systems. In Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd edn. pp 773–781 Edited by Neidhardt F. C.others Washington, DC: American Society for Microbiology;
    [Google Scholar]
  40. Roberts R. J., Belfort M., Bestor T. & 44 other authors; 2003a; A nomenclature for restriction enzymes, DNA methyltransferases, homing endonucleases and their genes. Nucleic Acids Res 31:1805–1812 [CrossRef]
    [Google Scholar]
  41. Roberts R. J., Vincze T., Posfai J., Macelis D. 2003b; REBASE: restriction enzymes and methyltransferases. Nucleic Acids Res 31:418–420 [CrossRef]
    [Google Scholar]
  42. Schouler C., Clier F., Lerayer A. L., Ehrlich S. D., Chopin M. C. 1998; A type IC restriction-modification system in Lactococcus lactis. J Bacteriol 180:407–411
    [Google Scholar]
  43. Sharp P. M., Kelleher J. E., Daniel A. S., Cowan G. M., Murray N. E. 1992; Roles of selection and recombination in the evolution of type I restriction-modification systems in enterobacteria. Proc Natl Acad Sci U S A 89:9836–9840 [CrossRef]
    [Google Scholar]
  44. Simpson A. J., Reinach F. C., Arruda P. 113 other authors 2000; The genome sequence of the plant pathogen Xylella fastidiosa. The Xylella fastidiosa Consortium of the Organization for Nucleotide Sequencing and Analysis. Nature 406:151–157 [CrossRef]
    [Google Scholar]
  45. Skrzypek E., Piekarowicz A. 1989; The EcoDXX1 restriction and modification system: cloning the genes and homology to type I restriction and modification systems. Plasmid 21:195–204 [CrossRef]
    [Google Scholar]
  46. Suri B., Bickle T. A. 1985; EcoA: the first member of a new family of type I restriction-modification systems. Gene organization and enzymatic activities. J Mol Biol 186:77–85 [CrossRef]
    [Google Scholar]
  47. Titheradge A. J., Ternent D., Murray N. E. 1996; A third family of allelic hsd genes in Salmonella enterica: sequence comparisons with related proteins identify conserved regions implicated in restriction of DNA. Mol Microbiol 22:437–447 [CrossRef]
    [Google Scholar]
  48. Titheradge A. J., King J., Ryu J., Murray N. E. 2001; Families of restriction enzymes: an analysis prompted by molecular and genetic data for type ID restriction and modification systems. Nucleic Acids Res 29:4195–4205 [CrossRef]
    [Google Scholar]
  49. Tomb J. F., White O., Kerlavage A. R. 22 other authors 1997; The complete genome sequence of the gastric pathogen Helicobacter pylori . Nature 388:539–547 [CrossRef]
    [Google Scholar]
  50. Tyndall C., Meister J., Bickle T. A. 1994; The Escherichia coli prr region encodes a functional type IC DNA restriction system closely integrated with an anticodon nuclease gene. J Mol Biol 237:266–274 [CrossRef]
    [Google Scholar]
  51. Wang Y., Taylor D. E. 1990; Natural transformation in Campylobacter species. J Bacteriol 172:949–955
    [Google Scholar]
  52. Wassenaar T. M., Wagenaar J. A., Rigter A., Fearnley C., Newell D. G., Duim B. 2002; Homonucleotide stretches in chromosomal DNA of Campylobacter jejuni display high frequency polymorphism as detected by direct PCR analysis. FEMS Microbiol Lett 212:77–85 [CrossRef]
    [Google Scholar]
  53. Weiserova M., Firman K. 1998; Isolation of a non-classical mutant of the DNA recognition subunit of the type I restriction endonuclease R.EcoRI24I. Biol Chem 379:585–589
    [Google Scholar]
  54. Weiserova M., Dutta C. F., Firman K. 2000; A novel mutant of the type I restriction-modification enzyme EcoRI24I is altered at a key stage of the subunit assembly pathway. J Mol Biol 304:301–310 [CrossRef]
    [Google Scholar]
  55. Wenman W. M., Chai J., Louie T. J., Goudreau C., Lior H., Newell D. G., Pearson A. D., Taylor D. E. 1985; Antigenic analysis of Campylobacter flagellar protein and other proteins. J Clin Microbiol 21:108–112
    [Google Scholar]
  56. Wilson G. G., Murray N. E. 1992; Restriction and modification systems. Annu Rev Genet 25:585–628
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27327-0
Loading
/content/journal/micro/10.1099/mic.0.27327-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error