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. 1995 May;177(10):2769–2780. doi: 10.1128/jb.177.10.2769-2780.1995

Linear chromosomes of Lyme disease agent spirochetes: genetic diversity and conservation of gene order.

S Casjens 1, M Delange 1, H L Ley 3rd 1, P Rosa 1, W M Huang 1
PMCID: PMC176948  PMID: 7751287

Abstract

We have constructed physical and genetic maps of the chromosomes of 21 Lyme disease agent spirochetes from geographically diverse locations. All have linear chromosomes whose lengths range from 935 to 955 kbp, and all contain multiple linear plasmids in the 16- to 175-kbp size range. The locations of 11 gene clusters on the chromosomes of these different isolates are indistinguishable at the resolution achieved in this study, indicating that the members of this related group of species have highly conserved chromosomal gene orders. However, chromosomal restriction endonuclease cleavage site maps are unique for nearly all isolates. The 22 chromosomal maps currently available define eight classes of Lyme disease agents. Four of these correspond to the previously proposed species Borrelia burgdorferi, Borrelia garinii, Borrelia afzelii, and Borrelia japonica. In addition, the North American isolates 21038, DN127 c19-2, 25015, and CA55 typify four additional chromosomal types that are as phylogenetically distinct as the species listed above. These findings support the idea that comparison of restriction maps is currently the most robust and definitive method for determining overall chromosomal relationships among closely related bacteria. In the course of this work, we located on the chromosome the previously unmapped outer surface protein-encoding LA7 gene and genes homologous to the Escherichia coli priA, plsC, parE, and parC genes, and we have substantially refined the locations of the recA, fla, p22A, and flgE genes.

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Selected References

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  1. Anderson J. F., Barthold S. W., Magnarelli L. A. Infectious but nonpathogenic isolate of Borrelia burgdorferi. J Clin Microbiol. 1990 Dec;28(12):2693–2699. doi: 10.1128/jcm.28.12.2693-2699.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anderson J. F., Magnarelli L. A., LeFebvre R. B., Andreadis T. G., McAninch J. B., Perng G. C., Johnson R. C. Antigenically variable Borrelia burgdorferi isolated from cottontail rabbits and Ixodes dentatus in rural and urban areas. J Clin Microbiol. 1989 Jan;27(1):13–20. doi: 10.1128/jcm.27.1.13-20.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Baranton G., Postic D., Saint Girons I., Boerlin P., Piffaretti J. C., Assous M., Grimont P. A. Delineation of Borrelia burgdorferi sensu stricto, Borrelia garinii sp. nov., and group VS461 associated with Lyme borreliosis. Int J Syst Bacteriol. 1992 Jul;42(3):378–383. doi: 10.1099/00207713-42-3-378. [DOI] [PubMed] [Google Scholar]
  4. Barbour A. G., Fish D. The biological and social phenomenon of Lyme disease. Science. 1993 Jun 11;260(5114):1610–1616. doi: 10.1126/science.8503006. [DOI] [PubMed] [Google Scholar]
  5. Barbour A. G. Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med. 1984 Jul-Aug;57(4):521–525. [PMC free article] [PubMed] [Google Scholar]
  6. Barbour A. G. Plasmid analysis of Borrelia burgdorferi, the Lyme disease agent. J Clin Microbiol. 1988 Mar;26(3):475–478. doi: 10.1128/jcm.26.3.475-478.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Barbour A. G., Tessier S. L., Todd W. J. Lyme disease spirochetes and ixodid tick spirochetes share a common surface antigenic determinant defined by a monoclonal antibody. Infect Immun. 1983 Aug;41(2):795–804. doi: 10.1128/iai.41.2.795-804.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bissett M. L., Hill W. Characterization of Borrelia burgdorferi strains isolated from Ixodes pacificus ticks in California. J Clin Microbiol. 1987 Dec;25(12):2296–2301. doi: 10.1128/jcm.25.12.2296-2301.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brown W. M., George M., Jr, Wilson A. C. Rapid evolution of animal mitochondrial DNA. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1967–1971. doi: 10.1073/pnas.76.4.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Burgdorfer W., Barbour A. G., Hayes S. F., Benach J. L., Grunwaldt E., Davis J. P. Lyme disease-a tick-borne spirochetosis? Science. 1982 Jun 18;216(4552):1317–1319. doi: 10.1126/science.7043737. [DOI] [PubMed] [Google Scholar]
  11. Canard B., Saint-Joanis B., Cole S. T. Genomic diversity and organization of virulence genes in the pathogenic anaerobe Clostridium perfringens. Mol Microbiol. 1992 Jun;6(11):1421–1429. doi: 10.1111/j.1365-2958.1992.tb00862.x. [DOI] [PubMed] [Google Scholar]
  12. 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(4):441–448. doi: 10.3109/00365549309008525. [DOI] [PubMed] [Google Scholar]
  13. Carlson C. R., Grønstad A., Kolstø A. B. Physical maps of the genomes of three Bacillus cereus strains. J Bacteriol. 1992 Jun;174(11):3750–3756. doi: 10.1128/jb.174.11.3750-3756.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Casjens S., Huang W. M. Linear chromosomal physical and genetic map of Borrelia burgdorferi, the Lyme disease agent. Mol Microbiol. 1993 May;8(5):967–980. doi: 10.1111/j.1365-2958.1993.tb01641.x. [DOI] [PubMed] [Google Scholar]
  15. Clark-Curtiss J. E., Walsh G. P. Conservation of genomic sequences among isolates of Mycobacterium leprae. J Bacteriol. 1989 Sep;171(9):4844–4851. doi: 10.1128/jb.171.9.4844-4851.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Daniels D. L. The complete AvrII restriction map of the Escherichia coli genome and comparisons of several laboratory strains. Nucleic Acids Res. 1990 May 11;18(9):2649–2651. doi: 10.1093/nar/18.9.2649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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 Jun;174(11):3766–3774. doi: 10.1128/jb.174.11.3766-3774.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Dykhuizen D. E., Green L. Recombination in Escherichia coli and the definition of biological species. J Bacteriol. 1991 Nov;173(22):7257–7268. doi: 10.1128/jb.173.22.7257-7268.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. 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 Acad Sci U S A. 1993 Nov 1;90(21):10163–10167. doi: 10.1073/pnas.90.21.10163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ferdows M. S., Barbour A. G. Megabase-sized linear DNA in the bacterium Borrelia burgdorferi, the Lyme disease agent. Proc Natl Acad Sci U S A. 1989 Aug;86(15):5969–5973. doi: 10.1073/pnas.86.15.5969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Fukunaga M., Sohnaka M., Takahashi Y., Nakao M., Miyamoto K. Antigenic and genetic characterization of Borrelia species isolated from Ixodes persulcatus in Hokkaido, Japan. J Clin Microbiol. 1993 May;31(5):1388–1391. doi: 10.1128/jcm.31.5.1388-1391.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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 Mar 31;183(3):952–957. doi: 10.1016/s0006-291x(05)80282-7. [DOI] [PubMed] [Google Scholar]
  23. Hinnebusch J., Barbour A. G. Linear- and circular-plasmid copy numbers in Borrelia burgdorferi. J Bacteriol. 1992 Aug;174(16):5251–5257. doi: 10.1128/jb.174.16.5251-5257.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Huppertz H. I., Sticht-Groh V., Schwan T. Borderline antibody response in initial stages of lymphocytic meningitis does not rule out borreliosis. Lancet. 1986 Dec 20;2(8521-22):1468–1469. doi: 10.1016/s0140-6736(86)92789-3. [DOI] [PubMed] [Google Scholar]
  25. Kitten T., Barbour A. G. The relapsing fever agent Borrelia hermsii has multiple copies of its chromosome and linear plasmids. Genetics. 1992 Oct;132(2):311–324. doi: 10.1093/genetics/132.2.311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Krawiec S., Riley M. Organization of the bacterial chromosome. Microbiol Rev. 1990 Dec;54(4):502–539. doi: 10.1128/mr.54.4.502-539.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kriuchechnikov V. N., Korenberg E. I., Shcherbakov S. V., Kovalevskii Iu V., Levin M. L. Identifikatsiia borrelii, izolirovannykh v SSSR ot kleshchei Ixodes persulcatus Schulze. Zh Mikrobiol Epidemiol Immunobiol. 1988 Dec;(12):41–44. [PubMed] [Google Scholar]
  28. Kurashige S., Bissett M., Oshiro L. Characterization of a tick isolate of Borrelia burgdorferi that possesses a major low-molecular-weight surface protein. J Clin Microbiol. 1990 Jun;28(6):1362–1366. doi: 10.1128/jcm.28.6.1362-1366.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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 Apr;174(7):2199–2207. doi: 10.1128/jb.174.7.2199-2207.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lee J. J., Smith H. O., Redfield R. J. Organization of the Haemophilus influenzae Rd genome. J Bacteriol. 1989 Jun;171(6):3016–3024. doi: 10.1128/jb.171.6.3016-3024.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Li J., Nelson K., McWhorter A. C., Whittam T. S., Selander R. K. Recombinational basis of serovar diversity in Salmonella enterica. Proc Natl Acad Sci U S A. 1994 Mar 29;91(7):2552–2556. doi: 10.1073/pnas.91.7.2552. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Livesley M. A., Thompson I. P., Gern L., Nuttall P. A. Analysis of intra-specific variation in the fatty acid profiles of Borrelia burgdorferi. J Gen Microbiol. 1993 Sep;139(9):2197–2201. doi: 10.1099/00221287-139-9-2197. [DOI] [PubMed] [Google Scholar]
  33. Lovrich S. D., Callister S. M., Lim L. C., Schell R. F. Seroprotective groups among isolates of Borrelia burgdorferi. Infect Immun. 1993 Oct;61(10):4367–4374. doi: 10.1128/iai.61.10.4367-4374.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Marconi R. T., Garon C. F. Development of polymerase chain reaction primer sets for diagnosis of Lyme disease and for species-specific identification of Lyme disease isolates by 16S rRNA signature nucleotide analysis. J Clin Microbiol. 1992 Nov;30(11):2830–2834. doi: 10.1128/jcm.30.11.2830-2834.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. 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. 1992 Mar;138(3):533–536. doi: 10.1099/00221287-138-3-533. [DOI] [PubMed] [Google Scholar]
  36. Marconi R. T., Konkel M. E., Garon C. F. Variability of osp genes and gene products among species of Lyme disease spirochetes. Infect Immun. 1993 Jun;61(6):2611–2617. doi: 10.1128/iai.61.6.2611-2617.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Margolis N., Rosa P. A. Regulation of expression of major outer surface proteins in Borrelia burgdorferi. Infect Immun. 1993 May;61(5):2207–2210. doi: 10.1128/iai.61.5.2207-2210.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Masuzawa T., Okada Y., Beppu Y., Oku T., Kawamori F., Yanagihara Y. Immunological properties of Borrelia burgdorferi isolated from the Ixodes ovatus in Shizuoka, Japan. Microbiol Immunol. 1991;35(10):913–919. doi: 10.1111/j.1348-0421.1991.tb02030.x. [DOI] [PubMed] [Google Scholar]
  39. Masuzawa T., Okada Y., Yanagihara Y., Sato N. Antigenic properties of Borrelia burgdorferi isolated from Ixodes ovatus and Ixodes persulcatus in Hokkaido, Japan. J Clin Microbiol. 1991 Aug;29(8):1568–1573. doi: 10.1128/jcm.29.8.1568-1573.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. McLean R. G., Ubico S. R., Hughes C. A., Engstrom S. M., Johnson R. C. Isolation and characterization of Borrelia burgdorferi from blood of a bird captured in the Saint Croix River Valley. J Clin Microbiol. 1993 Aug;31(8):2038–2043. doi: 10.1128/jcm.31.8.2038-2043.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Milkman R., Bridges M. M. Molecular evolution of the Escherichia coli chromosome. IV. Sequence comparisons. Genetics. 1993 Mar;133(3):455–468. doi: 10.1093/genetics/133.3.455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Miyamoto K., Nakao M., Sato N., Mori M. Isolation of Lyme disease spirochetes from an ixodid tick in Hokkaido, Japan. Acta Trop. 1991 Apr;49(1):65–68. doi: 10.1016/0001-706x(91)90031-e. [DOI] [PubMed] [Google Scholar]
  43. Nei M., Li W. H. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci U S A. 1979 Oct;76(10):5269–5273. doi: 10.1073/pnas.76.10.5269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Nelson K., Whittam T. S., Selander R. K. Nucleotide polymorphism and evolution in the glyceraldehyde-3-phosphate dehydrogenase gene (gapA) in natural populations of Salmonella and Escherichia coli. Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6667–6671. doi: 10.1073/pnas.88.15.6667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Ojaimi C., Davidson B. E., Saint Girons I., Old I. G. Conservation of gene arrangement and an unusual organization of rRNA genes in the linear chromosomes of the Lyme disease spirochaetes Borrelia burgdorferi, B. garinii and B. afzelii. Microbiology. 1994 Nov;140(Pt 11):2931–2940. doi: 10.1099/13500872-140-11-2931. [DOI] [PubMed] [Google Scholar]
  46. 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 Lett. 1992 Dec 1;78(2-3):245–250. doi: 10.1016/0378-1097(92)90034-l. [DOI] [PubMed] [Google Scholar]
  47. Perng G. C., LeFebvre R. B., Johnson R. C. Further characterization of a potent immunogen and the chromosomal gene encoding it in the Lyme disease agent, Borrelia burgdorferi. Infect Immun. 1991 Jun;59(6):2070–2074. doi: 10.1128/iai.59.6.2070-2074.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Picken R. N. Polymerase chain reaction primers and probes derived from flagellin gene sequences for specific detection of the agents of Lyme disease and North American relapsing fever. J Clin Microbiol. 1992 Jan;30(1):99–114. doi: 10.1128/jcm.30.1.99-114.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Piesman J., Mather T. N., Sinsky R. J., Spielman A. Duration of tick attachment and Borrelia burgdorferi transmission. J Clin Microbiol. 1987 Mar;25(3):557–558. doi: 10.1128/jcm.25.3.557-558.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Péter O., Bretz A. G. Polymorphism of outer surface proteins of Borrelia burgdorferi as a tool for classification. Zentralbl Bakteriol. 1992 Jun;277(1):28–33. doi: 10.1016/s0934-8840(11)80867-4. [DOI] [PubMed] [Google Scholar]
  51. Rosa P. A., Hogan D., Schwan T. G. Polymerase chain reaction analyses identify two distinct classes of Borrelia burgdorferi. J Clin Microbiol. 1991 Mar;29(3):524–532. doi: 10.1128/jcm.29.3.524-532.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Rosa P. A., Schwan T., Hogan D. Recombination between genes encoding major outer surface proteins A and B of Borrelia burgdorferi. Mol Microbiol. 1992 Oct;6(20):3031–3040. doi: 10.1111/j.1365-2958.1992.tb01761.x. [DOI] [PubMed] [Google Scholar]
  53. Samuels D. S., Marconi R. T., Garon C. F. Variation in the size of the ospA-containing linear plasmid, but not the linear chromosome, among the three Borrelia species associated with Lyme disease. J Gen Microbiol. 1993 Oct;139(10):2445–2449. doi: 10.1099/00221287-139-10-2445. [DOI] [PubMed] [Google Scholar]
  54. Schmid G. P., Steigerwalt A. G., Johnson S. E., Barbour A. G., Steere A. C., Robinson I. M., Brenner D. J. DNA characterization of the spirochete that causes Lyme disease. J Clin Microbiol. 1984 Aug;20(2):155–158. doi: 10.1128/jcm.20.2.155-158.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Schwan T. G., Burgdorfer W., Garon C. F. Changes in infectivity and plasmid profile of the Lyme disease spirochete, Borrelia burgdorferi, as a result of in vitro cultivation. Infect Immun. 1988 Aug;56(8):1831–1836. doi: 10.1128/iai.56.8.1831-1836.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Schwan T. G., Schrumpf M. E., Karstens R. H., Clover J. R., Wong J., Daugherty M., Struthers M., Rosa P. A. Distribution and molecular analysis of Lyme disease spirochetes, Borrelia burgdorferi, isolated from ticks throughout California. J Clin Microbiol. 1993 Dec;31(12):3096–3108. doi: 10.1128/jcm.31.12.3096-3108.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Schwartz I., Wormser G. P., Schwartz J. J., Cooper D., Weissensee P., Gazumyan A., Zimmermann E., Goldberg N. S., Bittker S., Campbell G. L. Diagnosis of early Lyme disease by polymerase chain reaction amplification and culture of skin biopsies from erythema migrans lesions. J Clin Microbiol. 1992 Dec;30(12):3082–3088. doi: 10.1128/jcm.30.12.3082-3088.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Schwartz J. J., Gazumyan A., Schwartz I. rRNA gene organization in the Lyme disease spirochete, Borrelia burgdorferi. J Bacteriol. 1992 Jun;174(11):3757–3765. doi: 10.1128/jb.174.11.3757-3765.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Simpson W. J., Schrumpf M. E., Hayes S. F., Schwan T. G. Molecular and immunological analysis of a polymorphic periplasmic protein of Borrelia burgdorferi. J Clin Microbiol. 1991 Sep;29(9):1940–1948. doi: 10.1128/jcm.29.9.1940-1948.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  61. Steere A. C., Grodzicki R. L., Kornblatt A. N., Craft J. E., Barbour A. G., Burgdorfer W., Schmid G. P., Johnson E., Malawista S. E. The spirochetal etiology of Lyme disease. N Engl J Med. 1983 Mar 31;308(13):733–740. doi: 10.1056/NEJM198303313081301. [DOI] [PubMed] [Google Scholar]
  62. Steere A. C. Lyme disease. N Engl J Med. 1989 Aug 31;321(9):586–596. doi: 10.1056/NEJM198908313210906. [DOI] [PubMed] [Google Scholar]
  63. Sădziene A., Rosa P. A., Thompson P. A., Hogan D. M., Barbour A. G. Antibody-resistant mutants of Borrelia burgdorferi: in vitro selection and characterization. J Exp Med. 1992 Sep 1;176(3):799–809. doi: 10.1084/jem.176.3.799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Taylor D. E., Eaton M., Chang N., Salama S. M. Construction of a Helicobacter pylori genome map and demonstration of diversity at the genome level. J Bacteriol. 1992 Nov;174(21):6800–6806. doi: 10.1128/jb.174.21.6800-6806.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Tilly K., Campbell J. A Borrelia burgdorferi homolog of the Escherichia coli rho gene. Nucleic Acids Res. 1993 Feb 25;21(4):1040–1040. doi: 10.1093/nar/21.4.1040. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. 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 Feb;7(3):359–369. doi: 10.1111/j.1365-2958.1993.tb01128.x. [DOI] [PubMed] [Google Scholar]
  67. Wallich R., Helmes C., Schaible U. E., Lobet Y., Moter S. E., Kramer M. D., Simon M. M. Evaluation of genetic divergence among Borrelia burgdorferi isolates by use of OspA, fla, HSP60, and HSP70 gene probes. Infect Immun. 1992 Nov;60(11):4856–4866. doi: 10.1128/iai.60.11.4856-4866.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Wallich R., Simon M. M., Hofmann H., Moter S. E., Schaible U. E., Kramer M. D. Molecular and immunological characterization of a novel polymorphic lipoprotein of Borrelia burgdorferi. Infect Immun. 1993 Oct;61(10):4158–4166. doi: 10.1128/iai.61.10.4158-4166.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Welsh J., Pretzman C., Postic D., Saint Girons I., Baranton G., McClelland M. Genomic fingerprinting by arbitrarily primed polymerase chain reaction resolves Borrelia burgdorferi into three distinct phyletic groups. Int J Syst Bacteriol. 1992 Jul;42(3):370–377. doi: 10.1099/00207713-42-3-370. [DOI] [PubMed] [Google Scholar]
  70. Woese C. R. Bacterial evolution. Microbiol Rev. 1987 Jun;51(2):221–271. doi: 10.1128/mr.51.2.221-271.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]

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