Skip to content
1887

Microbiology Society logo Microbiology

Volume 140, Issue 11

Conservation of gene arrangement and an unusual organization of rRNA genes in the linear chromosomes of the Lyme disease spirochaetes and Free

Abstract

Physical maps of the chromosomes of the Lyme disease spirochaetes and have been elucidated for the enzymes l, AI, I-I, I, I, HII, I and l by two-dimensional pulsed-field gel electrophoresis techniques. The maps contain 42 sites for and 32 for The mapping studies showed that the two chromosomes are linear DNA molecules of 953 and 948 kbp, respectively. A comparison of the physical maps of and and the published map of the other Lyme disease spirochaete, [Davidson, B. E., MacDougall, J. & Saint Girons, I. (1992) 174, 3766-3774] revealed that the three chromosomes have few endonuclease sites in common, apart from a cluster in (encoding 23S rRNA) and (encoding 16S rRNA). Cloned borrelial genes were used as specific hybridization probes to construct genetic maps, using the physical maps as a basis. The resulting maps contain 41 genetic loci for , 39 for , and 33 for In contrast to the physical maps, the three genetic maps are closely related, with no detectable differences in gene order along the entire length of the chromosome. It is concluded that the chromosomes of these three borrelial species have undergone no major rearrangements, deletions or insertions during their evolution from a common ancestor. Detailed mapping of the region of the and chromosomes that encodes rRNA revealed that each chromosome contains one copy of separated by 5 kbp from two copies each of and (encoding 5S rRNA). The gene order is is the only other member of the eubacteria for which this particular rRNA gene arrangement has been observed. A DNA length polymorphism in the region of the borrelial rRNA genes was shown to be due to the presence of 2.2 kbp more DNA between and in and than in

  • Published Online:
Keyword(s): Borrelia , DNA length polymorphism , genetic map , linear bacterial chromosome and rRNA operon
© Society for General Microbiology 1994
Loading

Article metrics loading...

/content/journal/micro/10.1099/13500872-140-11-2931
1994-11-01
2025-01-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/140/11/mic-140-11-2931.html?itemId=/content/journal/micro/10.1099/13500872-140-11-2931&mimeType=html&fmt=ahah

References

  1. Assous M.V., Postic D., Paul G., Nevot O., Baranton G. Western blot analysis of sera from Lyme borreliosis patients according to the genomic species of the Borrelia strains used as antigens. Eur J Clin Microbiol & Infect Dis 1993; 12:261–268
     [Google Scholar]
  2. Baranton G., Postic D., Saint Girons I., Boerlin P., Piffaretti J.-C., Assous M., Grimont P.A.D. Delineation of Borrelia burgdorferi sensu stricto, Borrelia garinii sp. nov., and group VS461 associated with Lyme borreliosis. Int J Syst Bacteriol 1992; 42:378–383
     [Google Scholar]
  3. Barbour A.G. Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med 1984; 57:521–525
     [Google Scholar]
  4. Baril C., Richaud C., Baranton G., Saint Girons I. Linear chromosome of Borrelia burgdorferi. Rex Microbiol 1989; 140:507–516
     [Google Scholar]
  5. Burgdorfer W., Barbour A.G., Hayes S.F., Benach J.L., Grunwaldt E., Davis J.P. Lyme disease - a tick-borne spirochetosis. Science 1982; 216:1317–1319
     [Google Scholar]
  6. Canard B., Saint-Joanis B., Cole S.T. Genomic diversity and organization of virulence genes in the pathogenic anaerobe Clostridium perfringens. Mol Microbiol 1992; 6:1421–1429
     [Google Scholar]
  7. Canica M.M., Nato F., du Merle L., Mazie J.C., Baranton G., Postic D. Monoclonal antibodies for identification of Borrelia afzelii sp. nov. associated with late cutaneous manifestations of Lyme borreliosis. Scand J Infect Dis 1993; 25:441–448
     [Google Scholar]
  8. Carlson C.R., Gronstad A., Kolsto A.-B. Physical maps of the genomes of three Bacillus cereus strains. J Bacteriol 1992; 174:3750–3756
     [Google Scholar]
  9. Carniel E., Mercereau-Puijalon O., Bonnefoy S. The gene coding for the 190,000-dalton iron-regulated protein of Yersinia species is present only in the highly pathogenic strains. Infect Immun 1989; 57:1211–1217
     [Google Scholar]
  10. Casjens S., Huang W.M. Linear chromosomal physical and genetic map of Borrelia burgdorferi, the Lyme disease agent. Mol Microbiol 1993; 8:967–980
     [Google Scholar]
  11. Davidson B.E., MacDougall J., Saint Girons I. Physical map of the linear chromosome of the bacterium Borrelia burgdorferi 212, a causative agent of Lyme disease, and localization of rRNA genes. J Bacteriol 1992; 174:3766–3774
     [Google Scholar]
  12. Dykhuizen D.E., Polin D.S., Dunn J.J., Wilske B., Preac-Mursic V., Dattwyler R.J., Luft B.J. Borrelia burgdorferi is clonal: implications for taxonomy and vaccine development. Proc Natl AcadSci USA 1993; 90:10163–10167
     [Google Scholar]
  13. Feinberg A.P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 1984; 137:266–267
     [Google Scholar]
  14. Ferdows M.S., Barbour A.G. Megabase-sized linear DNA in the bacterium Borrelia burgdorferi, the Lyme disease agent. Proc Natl Acad Sci USA 1989; 86:5969–5973
     [Google Scholar]
  15. Fukunaga M., Sohnaka M. Tandem repeat of the 23S and 5S ribosomal RNA genes in Borrelia burgdorferi, the etiological agent of Lyme disease. Biochem Biophys Res Commun 1992; 183:952–957
     [Google Scholar]
  16. Fukunaga M., Sohnaka M., Yanagihara Y. Analysis of Borrelia species associated with Lyme disease by rRNA gene restriction fragment length polymorphism. J Gen Microbiol 1993; 139:1141–1146
     [Google Scholar]
  17. Gassmann G.S., Jacobs E., Deutzmann R., Gobel U.B. Analysis of the Borrelia burgdorferi GeHo fla gene and antigenic characterization of its gene product. J Bacteriol 1991; 173:1452–1459
     [Google Scholar]
  18. Gazumyan A., Schwartz J.J., Liveris D., Schwartz I. Sequence analysis of the ribosomal RNA operon of the Lyme disease spirochete Borrelia burgdorferi. Gene 1994 (in press)
    [Google Scholar]
  19. Hansen K., Bangsborg J.M., Fjordvang H., Pedersen N.S., Hindersson P. Immunochemical characterization of and isolation of the gene for a Borrelia burgdorferi immunodominant 60- kilodalton antigen common to a wide range of bacteria. Infect Immun 1988; 56:2047–2053
     [Google Scholar]
  20. Hill C.W., Harnish B.W. Inversions between ribosomal RNA genes of Escherichia coli. Proc Natl Acad Sci USA 1981; 78:7069–7072
     [Google Scholar]
  21. Hinnebusch J., Barbour A.G. Linear plasmids of Borrelia burgdorferi have a telomeric structure and sequence similar to those of a eukaryotic virus. J Bacteriol 1991; 173:7233–7239
     [Google Scholar]
  22. Hinnebusch J., Tilly K. Linear plasmids and chromosomes in bacteria. Mol Microbiol 1993; 10:917–922
     [Google Scholar]
  23. Hinnebusch J., Bergstrom S., Barbour A.G. Cloning and sequence analysis of linear plasmid telomeres of the bacterium Borrelia burgdorferi. Mol Microbiol 1990; 4:811–820
     [Google Scholar]
  24. Howe T.R., Mayer L.W., Barbour A.G. A single recombinant plasmid expressing two major outer surface proteins of the Lyme disease spirochete. Science 1985; 227:645–646
     [Google Scholar]
  25. Jauris-Heipke S., Fuchs R., Hofmann A., Lottspeich F., Preac-Mursic V., Soutschek E., Will G., Wilske B. Molecular characterization of the p100 gene of Borrelia burgdorferi strain PKo. FEMS Microbiol Lett 1993; 114:235–242
     [Google Scholar]
  26. Johnson R.C., Schmid G.P., Hyde F.W., Steigerwalt A.G., Brenner D.J. Borrelia burgdorferi sp nov: etiologic agent of Lyme disease. Int J Syst Bacteriol 1984; 34:496–497
     [Google Scholar]
  27. Krawiec S., Riley M. Organization of the bacterial chromosome. Microbiol Rev 1990; 54:502–539
     [Google Scholar]
  28. Ladefoged S.A., Christiansen G. Physical and genetic mapping of the genomes of five Mycoplasma hominis strains by pulsed-field gel electrophoresis. J Bacteriol 1992; 174:2199–2207
     [Google Scholar]
  29. Lin Y.-S., Kieser H.M., Hopwood D.A., Chen C.W. The chromosomal DNA of Streptomyces lividans 66 is linear. Mol Microbiol 1993; 10:923–933
     [Google Scholar]
  30. Marconi R.T., Garon C.F. Phylogenetic analysis of the genus Borrelia: a comparison of North American and European isolates of Borrelia burgdorferi. J Bacteriol 1992a; 174:241–244
     [Google Scholar]
  31. Marconi R.T., Garon C.F. Identification of a third genomic group of Borrelia burgdorferi through signature nucleotide analysis and 16S rRNA sequence determination. J Gen Microbiol 1992b; 138:533–536
     [Google Scholar]
  32. Okada N., Sasakawa C., Tobe T., Talukder K.A., Komatsu K., Yoshikawa M. Construction of a physical map of the chromosome of Shigella flexneri 2a and the direct assignment of nine virulence-associated loci identified by Tn5 insertions. Mol Microbiol 1991; 5:2171–2180
     [Google Scholar]
  33. Old I.G., MacDougall J., Saint Girons I., Davidson B.E. Mapping of genes on the linear chromosome of the bacterium Borrelia burgdorferi: possible locations for its origin of replication. FEMS Microbiol Eett 1992a; 99:245–250
     [Google Scholar]
  34. Old I.G., Margarita D., Saint Girons I. Nucleotide sequence of the Borrelia burgdorferi rpmH gene encoding ribosomal protein L34. Nucleic Acids Res 1992b; 20:6097
     [Google Scholar]
  35. Old I.G., Margarita D., Saint Girons I. Unique genetic arrangement in the dnaA region of the Borrelia burgdorferi linear chromosome: nucleotide sequence of the dnaA gene. FEMS Microbiol Eett 1993a; 111:109–114
     [Google Scholar]
  36. Old I.G., Margarita D., Saint Girons I. Nucleotide sequence of the Borrelia burgdorferi dnaN gene encoding the βsubunit of DNA polymerase III. Nucleic Acids Res 1993b; 21:3323
     [Google Scholar]
  37. Pyle L.E., Taylor T., Finch L.R. Genomic maps of some strains within the Mycoplasma mycoides cluster. J Bacteriol 1990; 172:7265–7268
     [Google Scholar]
  38. Reed K.C., Mann D.A. Rapid transfer of DNA from agarose gels to nylon membranes. Nucleic Acids Res 1985; 13:7207–7221
     [Google Scholar]
  39. Riley M., Krawiec S. Genome organization. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology 1987 Edited by Neidhardt F.C., Ingraham J.L., Low K.B., Magasanik B., Schaechter M., Umbarger H.E. Washington, DC: American Society for Microbiology; pp 967–981
     [Google Scholar]
  40. Rosa P.A., Hogan D., Schwan T.G. Polymerase chain reaction analyses identify two distinct classes of Borrelia burgdorferi. J Clin Microbiol 1991; 29:524–532
     [Google Scholar]
  41. Rosa P.A., Schwan T., Hogan D. Recombination between genes encoding major outer surface proteins A and B of Borrelia burgdorferi. Mol Microbiol 1992; 6:3031–3040
     [Google Scholar]
  42. Saint Girons I., Old I.G., Davidson B.E. Molecular biology of the Borrelia, bacteria with linear replicons. Microbiology 1994; 140:1803–1816
     [Google Scholar]
  43. Schwartz J.J., Gazumyan A., Schwartz I. rRNA gene organization in the Lyme disease spirochaete, Borrelia burgdorferi. J Bacteriol 1992; 174:3757–3765
     [Google Scholar]
  44. Tilly K., Campbell J. A Borrelia burgdorferi homolog of the Escherichia coli rho gene. Nucleic Acids Res 1993; 21:1040
     [Google Scholar]
  45. Tilly K., Hauser R., Campbell J., Ostheimer G.J. Isolation of dnaj, dnaK and grpE homologues from Borrelia burgdorferi and complementation of Escherichia coli mutants. Mol Microbiol 1993; 7:359–369
     [Google Scholar]
  46. Tulloch D.L., Finch L.R., Hillier A.J., Davidson B.E. Physical map of the chromosome of Eactococcus lactis subsp. lactis DL11 and localization of six putative rRNA operons. J Bacteriol 1991; 173:2768–2775
     [Google Scholar]
  47. Zuerner R.L., Herrmann J.L., Saint Girons I. Comparison of genetic maps for two Eeptospira interrogans serovars provides evidence for two chromosomes and intraspecies heterogeneity. J Bacteriol 1993; 175:5445–5451
     [Google Scholar]
/content/journal/micro/10.1099/13500872-140-11-2931
Loading
Conservation of gene arrangement and an unusual organization of rRNA genes in the linear chromosomes of the Lyme disease spirochaetes Borrelia burgdorferi, B. gariniiand B. afzelii
Microbiology 140, 2931 (1994); https://doi.org/10.1099/13500872-140-11-2931
/content/journal/micro/10.1099/13500872-140-11-2931
/content/journal/micro/10.1099/13500872-140-11-2931
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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