Borrelia burgdorferi linear plasmid 38 is dispensable for completion of the mouse-tick infectious cycle

Infection and Immunity

Volumn 79, Issue 9, 2011, Pages 3510-3517

  Dulebohn, Daniel P ^a   Bestor, Aaron ^a   Rego, Ryan O M ^a   Stewart, Philip E ^a   Rosa, Patricia A ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BORRELIA BURGDORFERI; FEMALE; IXODES; LINEAR PLASMID 38; MOUSE; NONHUMAN; PHENOTYPE; PLASMID; PRIORITY JOURNAL; SOUTHERN BLOTTING;

ANIMALS; ARACHNID VECTORS; BORRELIA BURGDORFERI; FEMALE; GENETIC VECTORS; IXODES; LYME DISEASE; MICE; PLASMIDS; VIRULENCE FACTORS;

EID: 80052325574     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05014-11     Document Type: Article

References (66)

1. Ausubel, F. M., et al. (ed.). 1989. Current protocols in molecular biology, vol. 1. Greene Publishing Associates and Wiley-Interscience, New York, NY.
2. Barbour, A. G. 1989. The molecular biology of Borrelia. Rev. Infect. Dis. 11(Suppl. 6):S1470-S1474.
3. Barbour, A. G., C. J. Carter, V. Bundoc, and J. Hinnebusch. 1996. The nucleotide sequence of a linear plasmid of Borrelia burgdorferi reveals similarities to those of circular plasmids of other prokaryotes. J. Bacteriol. 178: 6635-6639.
4. Barbour, A. G., S. F. Hayes, R. A. Heiland, M. E. Schrumpf, and S. L. Tessier. 1986. A Borrelia-specific monoclonal antibody binds to a flagellar epitope. Infect. Immun. 52:549-554.
5. Baril, C., C. Richaud, G. Baranton, and I. Saint Girons. 1989. Linear chromosome of Borrelia burgdorferi. Res. Microbiol. 140:507-516.
6. Beaurepaire, C., and G. Chaconas. 2005. Mapping of essential replication functions of the linear plasmid lp17 of Borrelia burgdorferi by targeted deletion walking. Mol. Microbiol. 57:132-142.
7. Bestor, A., et al. 2010. Use of the Cre-lox recombination system to investigate lp54 gene requirement in the infectious cycle of Borrelia burgdorferi. Infect. Immun. 78:2397-2407.
8. Bono, J. L., et al. 2000. Efficient targeted mutagenesis in Borrelia burgdorferi. J. Bacteriol. 182:2445-2452.
9. Botkin, D. J., et al. 2006. Identification of potential virulence determinants by Himar1 transposition of infectious Borrelia burgdorferi B31. Infect. Immun. 74:6690-6699.
10. Brooks, C. S., P. S. Hefty, S. E. Jolliff, and D. R. Akins. 2003. Global analysis of Borrelia burgdorferi genes regulated by mammalian host-specific signals. Infect. Immun. 71:3371-3383.
11. Bunikis, J., et al. 2004. Borrelia burgdorferi infection in a natural population of Peromyscus leucopus mice: a longitudinal study in an area where Lyme borreliosis is highly endemic. J. Infect. Dis. 189:1515-1523.
12. Carle, G. F., M. Frank, and M. V. Olson. 1986. Electrophoretic separations of large DNA molecules by periodic inversion of the electric field. Science 232:65-68.
13. Carroll, J. A., R. M. Cordova, and C. F. Garon. 2000. Identification of 11 pH-regulated genes in Borrelia burgdorferi localizing to linear plasmids. Infect. Immun. 68:6677-6684.
14. Carroll, J. A., C. F. Garon, and T. G. Schwan. 1999. Effects of environmental pH on membrane proteins in Borrelia burgdorferi. Infect. Immun. 67:3181-3187.
15. Casjens, S., M. DeLange, H. L. Ley III, P. Rosa, and W. M. Huang. 1995. Linear chromosomes of Lyme disease agent spirochetes: genetic diversity and conservation of gene order. J. Bacteriol. 177:2769-2780.
16. Casjens, S., and W. M. Huang. 1998. The linear chromosomes of Borrelia burgdorferi and the other Lyme disease spirochetes, p. 621-624. In F. de Bruijn, G. Weinstock, and J. Lupski (ed.), Bacterial genomes: physical structure and analysis. Chapman and Hall, New York, NY.
17. Casjens, S., 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.
18. Eggers, C. H., et al. 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.
19. Elias, A. F., et al. 2002. Clonal polymorphism of Borrelia burgdorferi strain B31 MI: implications for mutagenesis in an infectious strain background. Infect. Immun. 70:2139-2150.
20. Ferdows, M. S., and A. G. Barbour. 1989. Megabase-sized linear DNA in the bacterium Borrelia burgdorferi, the Lyme disease agent. Proc. Natl. Acad. Sci. U. S. A. 86:5969-5973.
21. Fraser, C. M., et al. 1997. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390:580-586.
22. Fraser, C. M., et al. 1998. Complete genome sequence of Treponema pallidum, the syphilis spirochete. Science 281:375-388.
23. Grimm, D., et al. 2004. Experimental assessment of the roles of linear plasmids lp25 and lp28-1 of Borrelia burgdorferi throughout the infectious cycle. Infect. Immun. 72:5938-5946.
24. Grimm, D., A. F. Elias, K. Tilly, and P. A. Rosa. 2003. Plasmid stability during in vitro propagation of Borrelia burgdorferi assessed at a clonal level. Infect. Immun. 71:3138-3145.
25. Grimm, D., et al. 2005. Defining plasmids required by Borrelia burgdorferi for colonization of tick vector Ixodes scapularis (Acari: Ixodidae). J. Med. Entomol. 42:676-684.
26. Hinnebusch, J., and K. Tilly. 1993. Linear plasmids and chromosomes in bacteria. Mol. Microbiol. 10:917-922.
27. Iyer, R., et al. 2003. Linear and circular plasmid content in Borrelia burgdorferi clinical isolates. Infect. Immun. 71:3699-3706.
28. Jewett, M. W., et al. 2007. Genetic basis for retention of a critical virulence plasmid of Borrelia burgdorferi. Mol. Microbiol. 66:975-990.
29. Jewett, M. W., et al. 2007. The critical role of the linear plasmid lp36 in the infectious cycle of Borrelia burgdorferi. Mol. Microbiol. 64:1358-1374.
30. Jewett, M. W., et al. 2009. GuaA and GuaB are essential for Borrelia burgdorferi survival in the tick-mouse infectious cycle. J. Bacteriol. 191:6231-6241.
31. Kumar, M., X. Yang, A. S. Coleman, and U. Pal. 2010. BBA52 facilitates Borrelia burgdorferi transmission from feeding ticks to murine hosts. J. Infect. Dis. 201:1084-1095.
32. Labandeira-Rey, M., J. Seshu, and J. T. Skare. 2003. The absence of linear plasmid 25 or 28-1 of Borrelia burgdorferi dramatically alters the kinetics of experimental infection via distinct mechanisms. Infect. Immun. 71:4608-4613.
33. Lane, R. S., J. Piesman, and W. Burgdorfer. 1991. Lyme borreliosis: relation of its causative agent to its vectors and hosts in North America and Europe. Annu. Rev. Entomol. 36:587-609.
34. Levin, M., J. F. Levine, S. Yang, P. Howard, and C. S. Apperson. 1996. Reservoir competence of the southeastern five-lined skink (Eumeces inexpectatus) and the green anole (Anolis carolinensis) for Borrelia burgdorferi. Am. J. Trop. Med. Hyg. 54:92-97.
35. Li, X., et al. 2007. Role of outer surface protein D in the Borrelia burgdorferi life cycle. Infect. Immun. 75:4237-4244.
36. Maupin, G. O., et al. 1994. Discovery of an enzootic cycle of Borrelia burgdorferi in Neotoma mexicana and Ixodes spinipalpis from Northern Colorado, an area where Lyme disease is nonendemic. J. Infect. Dis. 170:36-43.
37. Norris, S. J., J. K. Howell, S. A. Garza, M. S. Ferdows, and A. G. Barbour. 1995. High- and low-infectivity phenotypes of clonal populations of in vitrocultured Borrelia burgdorferi. Infect. Immun. 63:2206-2212.
38. Norris, S. J., et al. 2011. High-throughput plasmid content analysis of Borrelia burgdorferi B31 by using Luminex multiplex technology. Appl. Environ. Microbiol. 77:1483-1492.
39. Ojaimi, C., et al. 2003. Profiling temperature-induced changes in Borrelia burgdorferi gene expression using whole genome arrays. Infect. Immun. 71: 1689-1705.
40. Ouyang, Z., et al. 2009. BosR (BB0647) governs virulence expression in Borrelia burgdorferi. Mol. Microbiol. 74:1331-1343.
41. Peavey, C. A., and R. S. Lane. 1995. Transmission of Borrelia burgdorferi by Ixodes pacificus nymphs and reservoir competence of deer mice (Peromyscus maniculatus) infected by tick-bite. J. Parasitol. 81:175-178.
42. Piesman, J., and L. Gern. 2004. Lyme borreliosis in Europe and North America. Parasitology 129(Suppl.):S191-S220.
43. Purser, J. E., and S. J. Norris. 2000. Correlation between plasmid content and infectivity in Borrelia burgdorferi. Proc. Natl. Acad. Sci. U. S. A. 97: 13865-13870.
44. Rego, R. O., A. Bestor, and P. A. Rosa. 2011. Defining the plasmid-encoded restriction-modification systems of the Lyme disease spirochete Borrelia burgdorferi. J. Bacteriol. 193:1161-1171.
45. Revel, A. T., A. M. Talaat, and M. V. Norgard. 2002. DNA microarray analysis of differential gene expression in Borrelia burgdorferi, the Lyme disease spirochete. Proc. Natl. Acad. Sci. U. S. A. 99:1562-1567.
46. Saint Girons, I., I. G. Old, and B. E. Davidson. 1994. Molecular biology of the Borrelia, bacteria with linear replicons. Microbiology 140:1803-1816.
47. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
48. Samuels, D. S. 1995. Electrotransformation of the spirochete Borrelia burgdorferi. Methods Mol. Biol. 47:253-259.
49. Schwan, T. G., W. Burgdorfer, and C. F. Garon. 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.
50. Schwan, T. G., J. Piesman, W. T. Golde, M. C. Dolan, and P. A. Rosa. 1995. Induction of an outer surface protein on Borrelia burgdorferi during tick feeding. Proc. Natl. Acad. Sci. U. S. A. 92:2909-2913.
51. Simpson, W. J., C. F. Garon, and T. G. Schwan. 1990. Analysis of supercoiled circular plasmids in infectious and non-infectious Borrelia burgdorferi. Microb. Pathog. 8:109-118.
52. Steere, A. C. 1989. Lyme disease. N. Engl. J. Med. 321:586-596.
53. Stevenson, B., et al. 1997. Characterization of cp18, a naturally truncated member of the cp32 family of Borrelia burgdorferi plasmids. J. Bacteriol. 179:4285-4291.
54. Stevenson, B., T. G. Schwan, and P. A. Rosa. 1995. Temperature-related differential expression of antigens in the Lyme disease spirochete, Borrelia burgdorferi. Infect. Immun. 63:4535-4539.
55. Stewart, P. E., A. Bestor, J. N. Cullen, and P. A. Rosa. 2008. A tightly regulated surface protein of Borrelia burgdorferi is not essential to the mousetick infectious cycle. Infect. Immun. 76:1970-1978.
56. Stewart, P. E., R. Byram, D. Grimm, K. Tilly, and P. A. Rosa. 2005. The plasmids of Borrelia burgdorferi: essential genetic elements of a pathogen. Plasmid 53:1-13.
57. Stewart, P. E., G. Chaconas, and P. Rosa. 2003. Conservation of plasmid maintenance functions between linear and circular plasmids in Borrelia burgdorferi. J. Bacteriol. 185:3202-3209.
58. Stewart, P. E., R. Thalken, J. L. Bono, and P. Rosa. 2001. Isolation of a circular plasmid region sufficient for autonomous replication and transformation of infectious Borrelia burgdorferi. Mol. Microbiol. 39:714-721.
59. Strother, K. O., A. Broadwater, and A. de Silva. 2005. Plasmid requirements for infection of ticks by Borrelia burgdorferi. Vector Borne Zoonotic Dis. 5:237-245.
60. Strother, K. O., and A. M. de Silva. 2005. Role of Borrelia burgdorferi linear plasmid 25 in infection of Ixodes scapularis ticks. J. Bacteriol. 187:5776-5781.
61. Terekhova, D., R. Iyer, G. P. Wormser, and I. Schwartz. 2006. Comparative genome hybridization reveals substantial variation among clinical isolates of Borrelia burgdorferi sensu stricto with different pathogenic properties. J. Bacteriol. 188:6124-6134.
62. Thomas, V., et al. 2001. Dissociation of infectivity and pathogenicity in Borrelia burgdorferi. Infect. Immun. 69:3507-3509.
63. Tilly, K., et al. 2006. Borrelia burgdorferi OspC protein required exclusively in a crucial early stage of mammalian infection. Infect. Immun. 74:3554-3564.
64. Tokarz, R., J. M. Anderton, L. I. Katona, and J. L. Benach. 2004. Combined effects of blood and temperature shift on Borrelia burgdorferi gene expression as determined by whole genome DNA array. Infect. Immun. 72:5419-5432.
65. Wang, G., et al. 2002. Disease severity in a murine model of Lyme borreliosis is associated with the genotype of the infecting Borrelia burgdorferi sensu stricto strain. J. Infect. Dis. 186:782-791.
66. Xu, Y., C. Kodner, L. Coleman, and R. C. Johnson. 1996. Correlation of plasmids with infectivity of Borrelia burgdorferi sensu stricto type strain B31. Infect. Immun. 64:3870-3876.