Genetic basis for retention of a critical virulence plasmid of Borrelia burgdorferi

Molecular Microbiology

Volumn 66, Issue 4, 2007, Pages 975-990

  Jewett, Mollie W ^a   Byram, Rebecca ^a,b,c   Bestor, Aaron ^a   Tilly, Kit ^a   Lawrence, Kevin ^a   Burtnick, Mary N ^a   Gherardini, Frank ^a   Rosa, Patricia A ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b UNIVERSITY OF WYOMING   (United States)

^c Western Range and Water LLC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; RESOLVASE;

ALLELE; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; BBB26 GENE; BBB27 GENE; BORRELIA BURGDORFERI; CP26 GENE; GENETIC LINKAGE; NONHUMAN; OPEN READING FRAME; OSPC GENE; PLASMID; PRIORITY JOURNAL; REST GENE; TELOMERE;

BACTERIAL PROTEINS; BORRELIA BURGDORFERI; DNA, BACTERIAL; DNA, CIRCULAR; ELECTROPORATION; GENE SILENCING; GENES, ESSENTIAL; GENETIC VECTORS; PLASMIDS; RECOMBINATION, GENETIC; TRANSFORMATION, BACTERIAL; VIRULENCE;

BACTERIA (MICROORGANISMS); BORRELIA BURGDORFERI; MAMMALIA;

EID: 35748954029     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2007.05969.x     Document Type: Article

References (66)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. Lipman, D.J. (1990) Basic local alignment search tool. J Mol Biol 215 : 403 410.
2. Austin, S. Nordström, K. (1990) Partition-mediated incompatibility of bacterial plasmids. Cell 60 : 351 354.
3. Barbour, A.G., Hayes, S.F., Heiland, R.A., Schrumpf, M.E. Tessier, S.L. (1986) A Borrelia-specific monoclonal antibody binds to a flagellar epitope. Infect Immun 52 : 549 554.
4. Bergström, S., Bundoc, V.G. Barbour, A.G. (1989) Molecular analysis of linear plasmid-encoded major surface proteins, OspA and OspB, of the Lyme disease spirochete Borrelia burgdorferi. Mol Microbiol 3 : 479 486.
5. Bono, J.L., Tilly, K., Stevenson, B., Hogan, D. Rosa, P. (1998) Oligopeptide permease in Borrelia burgdorferi: putative peptide-binding components encoded by both chromosomal and plasmid loci. Microbiol 144 : 1033 1044.
6. Bono, J.L., Elias, A.F., Kupko, J.J., III. Stevenson, B. Tilly, K. Rosa, P. (2000) Efficient targeted mutagenesis in Borrelia burgdorferi. J Bacteriol 182 : 2445 2452.
7. Botkin, D.J. Abbott, A. Stewart, P.E. Rosa, P.A. Kawabata, H. Watanabe, H., et al. (2006) Identification of potential virulence determinants by HimarI transposition of infectious Borrelia burgdorferi B31. Infect Immun 74 : 6690 6699.
8. Bunikis, J. Barbour, A.G. (1999) Access of antibody or trypsin to an integral outer membrane protein (P66) of Borrelia burgdorferi is hindered by Osp lipoproteins. Infect Immun 67 : 2874 2883.
9. Burgdorfer, W., Barbour, A.G., Hayes, S.F., Benach, J.L., Grunwaldt, E. Davis, J.P. (1982) Lyme disease - a tick-borne spirochetosis? Science 216 : 1317 1319.
10. Byram, R., Stewart, P.E. Rosa, P.A. (2004) The essential nature of the ubiquitous 26 kb circular replicon of Borrelia burgdorferi. J Bacteriol 186 : 3561 3569.
11. Casjens, S., Palmer, N., van Vugt, R., Huang, W.M., Stevenson, B., Rosa, P., et al. (2000) A bacterial genome in flux: the twelve linear and nine circular extrachromosomal DNAs in an infectious isolate of the Lyme disease spirochete Borrelia burgdorferi. Mol Microbiol 35 : 490 516.
12. Chaconas, G. (2005) Hairpin telomeres and genome plasticity in Borrelia: all mixed up in the end. Mol Microbiol 58 : 625 635.
13. Eggers, C.H., Caimano, M.J., Clawson, M.L., Miller, W.G., Samuels, D.S. Radolf, J.D. (2002) Identification of loci critical for replication and compatibility of a Borrelia burgdorferi cp32 plasmid and use of a cp32-based shuttle vector for expression of fluorescent reporters in the Lyme disease spirochaete. Mol Microbiol 43 : 281 295.
14. Elias, A.F., Stewart, P.E., Grimm, D., Caimano, M.J., Eggers, C.H., Tilly, K., et al. (2002) Clonal polymorphism of Borrelia burgdorferi strain B31 MI: implications for mutagenesis in an infectious strain background. Infect Immun 70 : 2139 2150.
15. Elias, A.F., Bono, J.L., Kupko, J.J., III, Stewart, P.E., Krum, J.G. Rosa, P.A. (2003) New antibiotic resistance cassettes suitable for genetic studies in Borrelia burgdorferi. J Mol Microbiol Biotechnol 6 : 29 40.
16. Frank, K.L., Bundle, S.F., Kresge, M.E., Eggers, C.H. Samuels, D.S. (2003) aadA confers streptomycin resistance in Borrelia burgdorferi. J Bacteriol 185 : 6723 6727.
17. Fraser, C.M., Casjens, S., Huang, W.M., Sutton, G.G., Clayton, R., Lathigra, R., et al. (1997) Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390 : 580 586.
18. Glöckner, G., Lehmann, R., Romualdi, A., Pradella, S., Schulte-Spechtel, U., Schilhabel, M., et al. (2004) Comparative analysis of the Borrelia garinii genome. Nucleic Acids Res 32 : 6038 6046.
19. Grimm, D., Elias, A.F., Tilly, K. Rosa, P.A. (2003) Plasmid stability during in vitro propagation of Borrelia burgdorferi assessed at a clonal level. Infect Immun 71 : 3138 3145.
20. Grimm, D., Tilly, K., Byram, R., Stewart, P.E., Krum, J.G., Bueschel, D.M., et al. (2004a) Outer-surface protein C of the Lyme disease spirochete: a protein induced in ticks for infection of mammals. Proc Natl Acad Sci USA 101 : 3142 3147.
21. Grimm, D., Eggers, C.H., Caimano, M.J., Tilly, K., Stewart, P.E., Elias, A.F., et al. (2004b) Experimental assessment of the roles of linear plasmids lp25 and lp28-1 of Borrelia burgdorferi throughout the infectious cycle. Infect Immun 72 : 5938 5946.
22. Grimm, D., Tilly, K., Bueschel, D.M., Fisher, M.A., Policastro, P.F., Gherardini, F.C., et al. (2005) Defining plasmids required by Borrelia burgdorferi for colonization of tick vector Ixodes scapularis (Acari: Ixodidae). J Med Entomol 42 : 676 684.
23. Guyard, C., Battisti, J., Raffel, S., Schrumpf, M., Whitney, A., Krum, J.G., et al. (2006) Relapsing fever spirochetes produce a serine protease that provides resistance to oxidative stress and killing by neutrophils. Mol Microbiol 60 : 710 722.
24. Hopp, T.P., Prickett, K.S., Price, V.L., Libby, R.T., March, C.J., Cerretti, D.P., et al. (1988) A short polypeptide tag sequence useful for recombinant protein identification and purification. Biotechnol J 6 : 1204 1210.
25. Jewett, M.W., Lawrence, K., Bestor, A.C., Tilly, K., Grimm, D., Shaw, P., et al. (2007) The critical role of the linear plasmid lp36 in the infectious cycle of Borrelia burgdorferi. Mol Microbiol 64 : 1358 1374.
26. Juncker, A.S., Willenbrock, H., Von Heijne, G., Burnak, S., Nielsen, H. Krogh, A. (2003) Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci 12 : 1652 1662.
27. Kobryn, K. Chaconas, G. (2002) ResT, a telomere resolvase encoded by the Lyme disease spirochete. Mol Cell 9 : 195 201.
28. Labandeira-Rey, M. Skare, J.T. (2001) Decreased infectivity in Borrelia burgdorferi strain B31 is associated with loss of linear plasmid 25 or 28-1. Infect Immun 69 : 446 455.
29. Marchler-Bauer, A., Anderson, J.B., Cherukuri, P.F., DeWeese-Scott, C., Geer, L.Y., Gwadz, M., et al. (2005) CDD: a conserved domain database for protein classification. Nucleic Acids Res 33 : D192 D196.
30. Marconi, R.T., Konkel, M.E. Garon, C.F. (1993) Variability of osp genes and gene products among species of Lyme disease spirochetes. Infect Immun 61 : 2611 2617.
31. Margolis, N., Hogan, D., Tilly, K. Rosa, P.A. (1994) Plasmid location of Borrelia purine biosynthesis gene homologs. J Bacteriol 176 : 6427 6432.
32. Miller, J.C., Bono, J.L., Babb, K., El-Hage, N., Casjens, S. Stevenson, B. (2000) A second allele of eppA. Borrelia burgdorferi strain B31 is located on the previously undetected circular plasmid cp9-2. J Bacteriol 182 : 6254 6258.
33. Molloy, S.S., Thomas, L., VanSlyke, J.K., Stenberg, P.E. Thomas, G. (1994) Intracellular trafficking and activation of the furin proprotein convertase: localization to the TGN and recycling from the cell surface. EMBO J 13 : 18 33.
34. Mura, C.V., Cosmelli, D., Munoz, F. Delgado, R. (2004) Orientation of Arabidopsis thaliana KAT1 channel in the plasma membrane. J Membr Biol 201 : 157 165.
35. Nakai, K. Horton, P. (1999) Psort: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem Sci 24 : 34 36.
36. Ojaimi, C., Brooks, C., Casjens, S., Rosa, P., Elias, A., Barbour, A.G., et al. (2003) Profiling temperature-induced changes in Borrelia burgdorferi gene expression using whole genome arrays. Infect Immun 71 : 1689 1705.
37. Pal, U., Yang, X., Chen, M., Bockenstedt, L.K., Anderson, J.F., Flavell, R.A., et al. (2004) OspC facilitates Borrelia burgdorferi invasion of Ixodes scapularis salivary glands. J Clin Invest 113 : 220 230.
38. Purser, J.E. Norris, S.J. (2000) Correlation between plasmid content and infectivity in Borrelia burgdorferi. Proc Natl Acad Sci USA 97 : 13865 13870.
39. Purser, J.E., Lawrenz, M.B., Caimano, M.J., Radolf, J.D. Norris, S.J. (2003) A plasmid-encoded nicotinamidase (PncA) is essential for infectivity of Borrelia burgdorferi in a mammalian host. Mol Microbiol 48 : 753 764.
40. Revel, A.T., Blevins, J.S., Almazan, C., Neil, L., Kocan, K.M., de la Fuente, J., et al. (2005) bptA (bbe16) is essential for the persistence of the Lyme disease spirochete, Borrelia burgdorferi, in its natural tick vector. Proc Natl Acad Sci USA 102 : 6972 6977.
41. Rosa, P., Samuels, D.S., Hogan, D., Stevenson, B., Casjens, S. Tilly, K. (1996) Directed insertion of a selectable marker into a circular plasmid of Borrelia burgdorferi. J Bacteriol 178 : 5946 5953.
42. Rosa, P.A., Schwan, T. Hogan, D. (1992) Recombination between genes encoding major outer surface proteins A and B of Borrelia burgdorferi. Mol Microbiol 6 : 3031 3040.
43. Sadziene, A., Wilske, B., Ferdows, M.S. Barbour, A.G. (1993) The cryptic ospC gene of Borrelia burgdorferi B31 is located on a circular plasmid. Infect Immun 61 : 2192 2195.
44. Schulze, R.J. Zuckert, W.R. (2006) Borrelia burgdorferi lipoproteins are secreted to the outer surface by default. Mol Microbiol 59 : 1473 1484.
45. Schwan, T.G., Burgdorfer, W. Garon, C.F. (1988) Changes in infectivity and plasmid profile of the Lyme disease spirochete, Borrelia burgdorferi, as a result of in vitro cultivation. Infect Immun 56 : 1831 1836.
46. Setubal, J.C., Reis, M., Matsunaga, J. Haake, D.A. (2006) Lipoprotein computational prediction in spirochaetal genomes. Microbiol 152 : 113 121.
47. Stevenson, B., Tilly, K. Rosa, P.A. (1996) A family of genes located on four separate 32-kilobase circular plasmids in Borrelia burgdorferi B31. J Bacteriol 178 : 3508 3516.
48. Stevenson, B., Casjens, S., van Vugt, R., Porcella, S.F., Tilly, K., Bono, J.L., et al. (1997) Characterization of cp18, a naturally truncated member of the cp32 family of Borrelia burgdorferi plasmids. J Bacteriol 179 : 4285 4291.
49. Stevenson, B., Casjens, S. Rosa, P. (1998) Evidence of past recombination events among the genes encoding the Erp antigens of Borrelia burgdorferi. Microbiol 144 : 1869 1879.
50. Stewart, P.E., Thalken, R., Bono, J.L. Rosa, P. (2001) Isolation of a circular plasmid region sufficient for autonomous replication and transformation of infectious Borrelia burgdorferi. Mol Microbiol 39 : 714 721.
51. Stewart, P.E., Chaconas, G. Rosa, P. (2003) Conservation of plasmid maintenance functions between linear and circular plasmids in Borrelia burgdorferi. J Bacteriol 185 : 3202 3209.
52. Stewart, P.E., Wang, X., Bueschel, D.M., Clifton, D.R., Grimm, D., Tilly, K., et al. (2006) Delineating the requirement for the Borrelia burgdorferi virulence factor OspC in the mammalian host. Infect Immun 74 : 3547 3553.
53. Strother, K.O., Broadwater, A. De Silva, A. (2005) Plasmid requirements for infection of ticks by Borrelia burgdorferi. Vector Borne Zoonotic Dis 5 : 237 245.
54. Terekhova, D., Iyer, R., Wormser, G.P. Schwartz, I. (2006) Comparative genome hybridization reveals substantial variation among clinical isolates of Borrelia burgdorferi sensu stricto with different pathogenic properties. J Bacteriol 188 : 6124 6134.
55. Tilly, K., Casjens, S., Stevenson, B., Bono, J.L., Samuels, D.S., Hogan, D., et al. (1997) The Borrelia burgdorferi circular plasmid cp26: conservation of plasmid structure and targeted inactivation of the ospC gene. Mol Microbiol 25 : 361 373.
56. Tilly, K., Lubke, L. Rosa, P. (1998) Characterization of circular plasmid dimers in Borrelia burgdorferi. J Bacteriol 180 : 5676 5681.
57. Tilly, K., Elias, A.F., Errett, J., Fischer, E., Iyer, R., Schwartz, I., et al. (2001) Genetics and regulation of chitobiose utilization in Borrelia burgdorferi. J Bacteriol 183 : 5544 5553.
58. Tilly, K., Krum, J.G., Bestor, A., Jewett, M.W., Grimm, D., Bueschel, D., et al. (2006) Borrelia burgdorferi OspC protein required exclusively in a crucial early stage of mammalian infection. Infect Immun 74 : 3554 3564.
59. Tilly, K., Bestor, A., Jewett, M.W. Rosa, P. (2007) Rapid clearance of Lyme disease spirochetes lacking OspC from skin. Infect Immun 75 : 1517 1519.
60. Tourand, Y., Bankhead, T., Wilson, S.L., Putteet-Driver, A.D., Barbour, A.G., Byram, R., et al. (2006) Differential telomere processing by Borrelia telomere resolvases in vitro but not in vivo. J Bacteriol 188 : 7378 7386.
61. Whitehouse, C.A., Williams, L.R. Austin, F.E. (1997) Identification of superoxide dismutase activity in Borrelia burgdorferi. Infect Immun 65 : 4865 4868.
62. Xu, Q., McShan, K. Liang, F.T. (2007) Identification of an ospC operator critical for immune evasion of Borrelia burgdorferi. Mol Microbiol 64 : 220 231.
63. Xu, Y., Kodner, C., Coleman, L. Johnson, R.C. (1996) Correlation of plasmids with infectivity of Borrelia burgdorferi sensu stricto type strain B31. Infect Immun 64 : 3870 3876.
64. Yamamoto, H., Kurosawa, S. Sekiguchi, J. (2003) Localization of the vegetative cell wall hydrolases LytC, LytE, and LytF on the Bacillus subtilis cell surface and stability of these enzymes to cell wall-bound or extracellular proteases. J Bacteriol 185 : 6666 6677.
65. Yang, X.F., Pal, U., Alani, S.M., Fikrig, E. Norgard, M.V. (2004) Essential role for OspA/B in the life cycle of the Lyme disease spirochete. J Exp Med 199 : 641 648.
66. Zhou, X., Cahoon, M., Rosa, P. Hedstrom, L. (1997) Expression, purification, and characterization of inosine 5′-monophosphate dehydrogenase from Borrelia burgdorferi. J Biol Chem 272 : 21977 21981.