Sequence typing reveals extensive strain diversity of the Lyme borreliosis agents Borrelia burgdorferi in North America and Borrelia afzelii in Europe

Microbiology

Volumn 150, Issue 6, 2004, Pages 1741-1755

  Bunikis, Jonas ^a   Garpmo, Ulf ^b   Tsao, Jean ^c,d   Berglund, Johan ^e   Fish, Durland ^c   Barbour, Alan G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b KALMAR COUNTY HOSPITAL   (Sweden)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d MICHIGAN STATE UNIVERSITY   (United States)

^e LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; OUTER MEMBRANE PROTEIN; PROTEIN P66; SPACER DNA;

ALLELE; ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL STRAIN; BACTERIUM ISOLATION; BORRELIA AFZELII; BORRELIA BURGDORFERI; CLADISTICS; CONTROLLED STUDY; EUROPE; GENE AMPLIFICATION; GENE LOCUS; GENE VECTOR; GENETIC LINKAGE; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENOTYPE; HUMAN; HUMAN CELL; IXODES RICINUS; IXODES SCAPULARIS; LYME DISEASE; MAXIMUM LIKELIHOOD METHOD; MONOPHYLY; NONHUMAN; NORTH AMERICA; NUCLEOTIDE SEQUENCE; PARSIMONY ANALYSIS; PHYLOGENY; PLASMID; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SKIN BIOPSY; SPECIES DIFFERENCE; SWEDEN; UNINDEXED SEQUENCE; UNITED STATES;

ACARI; BORRELIA; BORRELIA AFZELII; BORRELIA BURGDORFERI; IXODES; IXODES RICINUS; IXODES SCAPULARIS;

EID: 3142735095     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.26944-0     Document Type: Article

References (67)

1. Anderson, J. F. & Magnarelli, L. A. (1992). Epizootiology of Lyme disease and methods of cultivating Borrelia burgdorferi. Ann N Y Acad Sci 653, 52-63.
2. Anderson, J. F., Johnson, R. C., Magnarelli, L. A. & Hyde, F. W. (1986). Involvement of birds in the epidemiology of the Lyme disease agent Borrelia burgdorferi. Infect Immun 51, 394-396.
3. Åsbrink, E. & Hovmark, A. (1985). The spirochetal etiology of erythema chronicum migrans Afzelius. Acta Pathol Microbiol Immunol Scand Sect B 93, 161-163.
4. Barbour, A. G. (1984). Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med 57, 521-525.
5. Barbour, A. G. & Fish, D. (1993). The biological and social phenomenon of Lyme disease. Science 260, 1610-1616.
6. Barbour, A. G. & Schrumpf, M. E. (1986). Polymorphisms of major surface proteins of Borrelia burgdorferi. Zentbl Bakteriol Mikrobiol Hyg [A] 263, 83-91.
7. Barbour, A. G., Burgdorfer, W., Hayes, S. F., Peter, O. & Aeschlimann, A. (1983). Isolation of a cultivable spirochete from Ixodes ricinus ticks of Switzerland. Curr Microbiol 8, 123-126.
8. Barbour, A. G., Heiland, R. A. & Howe, T. R. (1985). Heterogeneity of major proteins in Lyme disease borreliae: a molecular analysis of North American and European isolates. J Infect Dis 152, 478-484.
9. Barbour, A. G., Maupin, G. O., Teltow, G. J., Carter, C. J. & Piesman, J. (1996). Identification of an uncultivable Borrelia species in the hard tick Amblyomma americanum: possible agent of a Lyme disease-like illness. J Infect Dis 173, 403-409.
10. Barthold, S. W., Moody, K. D., Terwilliger, G. A., Jacoby, R. O. & Steere, A. C. (1988). An animal model for Lyme arthritis. Ann N Y Acad Sci 539, 264-273.
11. Beati, L. & Keirans, J. E. (2001). Analysis of the systematic relationships among ticks of the genera Rhipicephalus and Boophilus (Acari: Ixodidae) based on mitochondrial 12S ribosomal DNA gene sequences and morphological characters. J Parasitol 87, 32-48.
12. Berger, B. W., Kaplan, M. H., Rothenberg, I. R. & Barbour, A. G. (1985). Isolation and characterization of the Lyme disease spirochete from the skin of patients with erythema chronicum migrans. J Am Acad Dermatol 13, 444-449.
13. Berglund, J., Eitrem, R., Ornstein, K. & 7 other authors (1995). An epidemiologic study of Lyme disease in southern Sweden. N Engl J Med 333, 1319-1327.
14. Bunikis, J., Luke, C. J., Bunikiene, E., Bergstrom, S. & Barbour, A. G. (1998). A surface-exposed region of a novel outer membrane protein (P66) of Borrelia spp. is variable in size and sequence. J Bacteriol 180, 1618-1623.
15. Busch, U., Hizo-Teufel, C., Boehmer, R., Fingerle, V., Nitschko, H., Wilske, B. & Preac-Mursic, V. (1996a). Three species of Borrelia burgdorferi sensu lato (B. burgdorferi sensu stricto, B. afzelii, and B. garinii) identified from cerebrospinal fluid isolates by pulsed-field gel electrophoresis and PCR. J Clin Microbiol 34, 1072-1078.
16. Busch, U., Hizo-Teufel, C., Bohmer, R., Fingerle, V., Rossler, D., Wilske, B. & Preac-Mursic, V. (1996b). Borrelia burgdorferi sensu lato strains isolated from cutaneous Lyme borreliosis biopsies differentiated by pulsed-field gel electrophoresis. Scand J Infect Dis 28, 583-589.
17. C. D. C. (1997). Lyme disease - United States, 1996. Morb Mortal Wkly Rep 46, 531-535.
18. Ding, W., Huang, X., Yang, X., Dunn, J. J., Luft, B. J., Koide, S. & Lawson, C. L. (2000). Structural identification of a key protective B-cell epitope in Lyme disease antigen OspA. J Mol Biol 302, 1153-1164.
19. Dressler, F., Whalen, J. A., Reinhardt, B. N. & Steere, A. C. (1993). Western blotting in the serodiagnosis of Lyme disease. J Infect Dis 167, 392-400.
20. Dykhuizen, D. E. & Baranton, G. (2001). The implications of a low rate of horizontal transfer in Borrelia. Trends Microbiol 9, 344-350.
21. Dykhuizen, D. E., Polin, D. S., Dunn, J. J., Wilske, B., Preac-Mursic, V., Dattwyler, R. J. & Luft, B. J. (1993). Borrelia burgdorferi is clonal: implications for taxonomy and vaccine development. Proc Natl Acad Sci U S A 90, 10163-10167.
22. Falco, R. C. & Fish, D. (1992). A comparison of methods for sampling the deer tick, Ixodes dammini, in a Lyme disease endemic area. Exp Appl Acarol 14, 165-173.
23. Farlow, J., Postic, D., Smith, K. L., Jay, Z., Baranton, G. & Keim, P. (2002). Strain typing of Borrelia burgdorferi, Borrelia afzelii, and Borrelia garinii by using multiple-locus variable-number tandem repeat analysis. J Clin Microbiol 40, 4612-4618.
24. Feavers, I. M., Gray, S. J., Urwin, R., Russell, J. E., Bygraves, J. A., Kaczmarski, E. B. & Maiden, M. C. (1999). Multilocus sequence typing and antigen gene sequencing in the investigation of a meningococcal disease outbreak. J Clin Microbiol 37, 3883-3887.
25. Fraser, C. M., Casjens, S., Huang, W. M. & 35 other authors (1997). Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390, 580-586.
26. Gern, L., Estrada-Pena, A., Frandsen, F. & 7 other authors (1998). European reservoir hosts of Borrelia burgdorferi sensu lato. Zentbl Bakteriol 287, 196-204.
27. Guttman, D. S., Wang, P. W., Wang, I. N., Bosler, E. M., Luft, B. J. & Dykhuizen, D. E. (1996). Multiple infections of Ixodes scapularis ticks by Borrelia burgdorferi as revealed by single-strand conformation polymorphism analysis. J Clin Microbiol 34, 652-656.
28. Hengge, U. R., Tannapfel, A., Tyring, S. K., Erbel, R., Arendt, G. & Ruzicka, T. (2003). Lyme borreliosis. Lancet Infect Dis 3, 489-500.
29. Hill, W. G. & Roberts, A. (1968). Linkage disequilibrium in finite populations. Theor Appl Genet 38, 226-231.
30. Jauris-Heipke, S., Liegl, G., Preac-Mursic, V., Rossler, D., Schwab, E., Soutschek, E., Will, G. & Wilske, B. (1995). Molecular analysis of genes encoding outer surface protein C (OspC) of Borrelia burgdorferi sensu lato: relationship to ospA genotype and evidence of lateral gene exchange of ospC. J Clin Microbiol 33, 1860-1866.
31. Jolley, K. A., Feil, E. J., Chan, M.-S. & Maiden, M. C. J. (2001). Sequence type analysis and recombinational tests (START). Bioinformatics 17, 1230-1231.
32. Kurtenbach, K., De Michelis, S., Sewell, H. S. & 10 other authors (2002). The key roles of selection and migration in the ecology of Lyme borreliosis. Int J Med Microbiol 291 Suppl 33, 152-154.
33. Lagal, V., Postic, D., Ruzic-Sabljic, E. & Baranton, G. (2003). Genetic diversity among Borrelia strains determined by single-strand conformation polymorphism analysis of the ospC gene and its association with invasiveness. J Clin Microbiol 41, 5059-5065.
34. Lee, S. H., Kim, B. J., Kim, J. H., Park, K. H., Yeo, S. J., Kim, S. J. & Kook, Y. H. (2000). Characterization of Borrelia burgdorferi strains isolated from Korea by 16S rDNA sequence analysis and PCR-RFLP analysis of rrf (5S)-rrl (23S) intergenic spacer amplicons. Int J Syst Evol Microbiol 50, 857-863.
35. Liveris, D., Gazumyan, A. & Schwartz, I. (1995). Molecular typing of Borrelia burgdorferi sensu lato by PCR-restriction fragment length polymorphism analysis. J Clin Microbiol 33, 589-595.
36. Liveris, D., Varde, S., Iyer, R. & 8 other authors (1999). Genetic diversity of Borrelia burgdorferi in Lyme disease patients as determined by culture versus direct PCR with clinical specimens. J Clin Microbiol 37, 565-569.
37. Livey, I., Gibbs, C. P., Schuster, R. & Dorner, F. (1995). Evidence for lateral transfer and recombination in OspC variation in Lyme disease Borrelia. Mol Microbiol 18, 257-269.
38. Maddison, D. R. & Maddison, W. P. (2002). MacClade 4: Analysis of Phylogeny and Character Evolution, version 4.04. Sunderland, MA: Sinauer Associates.
39. Maiden, M. C., Bygraves, J. A., Feil, E. & 10 other authors (1998). Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci U S A 95, 3140-3145.
40. Mathiesen, D. A., Oliver, J. H., Jr, Kolbert C. P. & 9 other authors (1997). Genetic heterogeneity of Borrelia burgdorferi in the United States. J Infect Dis 175, 98-107.
41. Maynard Smith, J. (1992). Analysing the mosaic structure of genes. J Mol Evol 34, 126-129.
42. Norris, D. E., Johnson, B. J., Piesman, J., Maupin, G. O., Clark, J. L. & Black, W. C., IV (1997). Culturing selects for specific genotypes of Borrelia burgdorferi in an enzootic cycle in Colorado. J Clin Microbiol 35, 2359-2364.
43. Norris, D. E., Johnson, B. J., Piesman, J., Maupin, G. O., Clark, J. L. & Black, W. C., IV (1999). Population genetics and phylogenetic analysis of Colorado Borrelia burgdorferi. Am J Trop Med Hyg 60, 699-707.
44. Ochman, H., Lawrence, J. G. & Groisman, E. A. (2000). Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299-304.
45. Ornstein, K., Berglund, J., Nilsson, I., Norrby, R. & Bergstrom, S. (2001). Characterization of Lyme borreliosis isolates from patients with erythema migrans and neuroborreliosis in southern Sweden. J Clin Microbiol 39, 1294-1298.
46. Posada, D. & Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817-818.
47. Posada, D. & Crandall, K. A. (2002). The effect of recombination on the accuracy of phylogeny estimation. J Mol Evol 54, 396-402.
48. Postic, D., Assous, M. V., Grimont, P. A. & Baranton, G. (1994). Diversity of Borrelia burgdorferi sensu lato evidenced by restriction fragment length polymorphism of rrf (5S)-rrl (23S) intergenic spacer amplicons. Int J Syst Bacteriol 44, 743-752.
49. Qiu, W. G., Bosler, E. M., Campbell, J. R., Ugine, G. D., Wang, I. N., Luft, B. J. & Dykhuizen, D. E. (1997). A population genetic study of Borrelia burgdorferi sensu stricto from eastern Long Island, New York, suggested frequency-dependent selection, gene flow and host adaptation. Hereditas 127, 203-216.
50. Qiu, W. G., Dykhuizen, D. E., Acosta, M. S. & Luft, B. J. (2002). Geographic uniformity of the Lyme disease spirochete (Borrelia burgdorferi) and its shared history with tick vector (Ixodes scapularis) in the Northeastern United States. Genetics 160, 833-849.
51. Rozas, J. & Rozas, R. (1999). DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15, 174-175.
52. Sawyer, S. (1989). Statistical tests for detecting gene conversion. Mol Biol Evol 6, 526-538.
53. Schwan, T. G., Piesman, J., Golde, W. T., Dolan, M. C. & Rosa, P. A. (1995). Induction of an outer surface protein on Borrelia burgdorferi during tick feeding. Proc Natl Acad Sci U S A 92, 2909-2913.
54. Scoles, G. A., Papero, M., Beati, L. & Fish, D. (2001). A relapsing fever group spirochete transmitted by Ixodes scapularis ticks. Vector Borne Zoonotic Dis 1, 21-34.
55. Seinost, G., Dykhuizen, D. E., Dattwyler, R. J., Golde, W. T., Dunn, J. J., Wang, I. N., Wormser, G. P., Schriefer, M. E. & Luft, B. J. (1999a). Four clones of Borrelia burgdorferi sensu stricto cause invasive infection in humans. Infect Immun 67, 3518-3524.
56. Seinost, G., Golde, W. T., Berger, B. W., Dunn, J. J., Qiu, D., Dunkin, D. S., Dykhuizen, D. E., Luft, B. J. & Dattwyler, R. J. (1999b). Infection with multiple strains of Borrelia burgdorferi sensu stricto in patients with Lyme disease. Arch Dermatol 135, 1329-1333.
57. Steere, A. C. (2001). Lyme disease. N Engl J Med 345, 115-125.
58. 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. (1983). The spirochetal etiology of Lyme disease. N Engl J Med 308, 733-740.
59. Swofford, D. L. (2001). PAUP. Phylogenetic Analysis Using Parsimony (* and other methods). Beta, version 4.0b6. Sunderland, MA: Sinauer Associates.
60. Theisen, M., Borre, M., Mathiesen, M. J., Mikkelsen, B., Lebech, A. M. & Hansen, K. (1995). Evolution of the Borrelia burgdorferi outer surface protein OspC. J Bacteriol 177, 3036-3044.
61. Thompson, J. D., Higgins, D. G. & Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680.
62. Tsao, J. (2000). Vertebrate host community composition and the dynamics of Borrelia burgdorferi, the etiologic agent of Lyme disease: theory and experiments. In Department of Ecology and Evolution, p. 90. Chicago: University of Chicago.
63. Wang, I. N., Dykhuizen, D. E., Qiu, W., Dunn, J. J., Bosler, E. M. & Luft, B. J. (1999). Genetic diversity of ospC in a local population of Borrelia burgdorferi sensu stricto. Genetics 151, 15-30.
64. Wilske, B., Preac-Mursic, V., Schierz, G. & Busch, K. V. (1986). Immunochemical and immunological analysis of European Borrelia burgdorferi strains. Zentbl Bakteriol Mikrobiol Hyg [A] 263, 92-102.
65. Wilske, B., Preac-Mursic, V., Gobel, U. B., Graf, B., Jauris, S., Soutschek, E., Schwab, E. & Zumstein, G. (1993). An OspA serotyping system for Borrelia burgdorferi based on reactivity with monoclonal antibodies and OspA sequence analysis. J Clin Microbiol 31, 340-350.
66. Wilske, B., Jauris-Heipke, S., Lobentanzer, R., Pradel, I., Preac-Mursic, V., Rossler, D., Soutschek, E. & Johnson, R. C. (1995). Phenotypic analysis of outer surface protein C (OspC) of Borrelia burgdorferi sensu lato by monoclonal antibodies: relationship to genospecies and OspA serotype. J Clin Microbiol 33, 103-109.
67. Wormser, G. P., Liveris, D., Nowakowski, J., Nadelman, R. B., Cavaliere, L. F., McKenna, D., Holmgren, D. & Schwartz, I. (1999). Association of specific subtypes of Borrelia burgdorferi with hematogenous dissemination in early Lyme disease. J Infect Dis 180, 720-725.