Distribution of cp32 prophages among lyme disease-causing spirochetes and natural diversity of their lipoprotein-encoding erp loci

Applied and Environmental Microbiology

Volumn 79, Issue 13, 2013, Pages 4115-4128

  Brisson, Dustin ^a   Zhou, Wei ^a   Jutras, Brandon L ^b   Casjens, Sherwood ^c   Stevenson, Brian ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EVOLUTIONARY HISTORY; EVOLUTIONARY ORIGIN; LYME DISEASE; MULTIPLE FUNCTION; NON-CODING REGION; PROTEIN CODING REGIONS; RECOMBINATION EVENTS; SURFACE PROTEINS;

ENCODING (SYMBOLS); GENES; PROTEINS;

BACTERIA;

BACTERIAL ANTIGEN; LIPOPROTEIN; OSPE PROTEIN, BORRELIA BURGDORFERI; OUTER MEMBRANE PROTEIN;

ALLELE; BACTERIOPHAGE; CHROMOSOME; DISEASE VECTOR; EVOLUTIONARY BIOLOGY; FUNCTIONAL ROLE; GENE EXPRESSION; GENOME; INFECTIVITY; LYME DISEASE; PROTEIN; TICK;

ARTICLE; BIOLOGY; BORRELIA BURGDORFERI; COMPARATIVE STUDY; DNA FLANKING REGION; DNA SEQUENCE; GENETIC VARIABILITY; GENETICS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PLASMID; PROPHAGE; SEQUENCE ALIGNMENT; SPECIES DIFFERENCE; VIROLOGY;

5' FLANKING REGION; ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BASE SEQUENCE; BORRELIA BURGDORFERI; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; GENETIC VARIATION; LIPOPROTEINS; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PLASMIDS; PROPHAGES; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

EUROPE; NORTH AMERICA; UNITED STATES;

BORRELIA; BORRELIA BURGDORFERI; IXODIDA; SPIROCHAETALES; VERTEBRATA;

EID: 84879826158     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00817-13     Document Type: Article

References (98)

1. Fraser CM, Casjens S, Huang WM, Sutton GG, Clayton R, Lathigra R, White O, Ketchum KA, Dodson R, Hickey EK, Gwinn M, Dougherty B, Tomb J-F, Fleischmann RD, Richardson D, Peterson J, Kerlavage AR, Quackenbush J, Salzberg S, Hanson M, van Vugt R, Palmer N, Adams MD, Gocayne J, Weidmann J, Utterback T, Watthey L, McDonald L, Artiach P, Bowman C, Garland S, Fujii C, Cotton MD, Horst K, Roberts K, Hatch B, Smith HO, Venter JC. 1997. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390:580-586.
2. Casjens S, van Vugt R, Tilly K, Rosa PA, Stevenson B. 1997. Homology throughout the multiple 32-kilobase circular plasmids present in Lyme disease spirochetes. J. Bacteriol. 179:217-227.
3. Casjens S, Palmer N, van Vugt R, Huang WM, Stevenson B, Rosa P, Lathigra R, Sutton G, Peterson J, Dodson RJ, Haft D, Hickey E, Gwinn M, White O, Fraser C. 2000. A bacterial genome in flux: the twelve linear and nine circular extrachromosomal DNAs of an infectious isolate of the Lyme disease spirochete Borrelia burgdorferi. Mol. Microbiol. 35:490-516.
4. Miller JC, Bono JL, Babb K, El-Hage N, Casjens S, Stevenson B. 2000. A second allele of eppA in Borrelia burgdorferi strain B31 is located on the previously undetected circular plasmid cp9-2. J. Bacteriol. 182:6254-6258.
5. Casjens SR, Eggers CH, Schwartz I. 2010. Borrelia genomics: chromosome, plasmids, bacteriophages and genetic variation, p 27-54. In Samuels DS, Radolf JD (ed), Borrelia: molecular biology, host interaction and pathogenesis. Caister Academic Press, Norfolk, United Kingdom.
6. Stevenson B, Tilly K, Rosa PA. 1996. A family of genes located on four separate 32-kilobase circular plasmids in Borrelia burgdorferi B31. J. Bacteriol. 178:3508-3516.
7. Stevenson B, Zückert WR, Akins DR. 2001. Repetition, conservation, and variation: the multiple cp32 plasmids of Borrelia species, p 87-100. In Saier MH, García-Lara J (ed), The spirochetes: molecular cellular biology. Horizon Press, Oxford, England.
8. Eggers CH, Samuels DS. 1999. Molecular evidence for a new bacteriophage of Borrelia burgdorferi. J. Bacteriol. 181:7308-7313.
9. Eggers CH, Kimmel BJ, Bono JL, Elias AF, Rosa P, Samuels DS. 2001. Transduction by BB-1, a bacteriophage of Borrelia burgdorferi. J. Bacteriol. 183:4771-4778.
10. Zhang H, Marconi RT. 2005. Demonstration of cotranscription and 1-methyl-3-nitroso-nitroguanidine induction of a 30-gene operon of Borrelia burgdorferi: evidence that the 32-kilobase circular plasmids are prophages. J. Bacteriol. 187:7985-7995.
11. Chenail AM, Jutras BL, Adams CA, Burns LH, Bowman A, Verma A, Stevenson B. 2012. Borrelia burgdorferi cp32 BpaB modulates expression of the prophage NucP nuclease and SsbP single-stranded DNA-binding protein. J. Bacteriol. 194:4570-4578.
12. Stevenson B, Casjens S, Rosa P. 1998. Evidence of past recombination events among the genes encoding the Erp antigens of Borrelia burgdorferi. Microbiology 144:1869-1879.
13. Akins DR, Caimano MJ, Yang X, Cerna F, Norgard MV, Radolf JD. 1999. Molecular and evolutionary analysis of Borrelia burgdorferi 297 circular plasmid-encoded lipoproteins with OspE-and OspF-like leader peptides. Infect. Immun. 67:1526-1532.
14. Eggers CH, Caimano MJ, Clawson ML, Miller WG, Samuels DS, Radolf JD. 2002. Identification of loci critical for replication and compatibility of a Borrelia burgdorferi cp32 plasmid and use of a cp32-based shuttle vector for the expression of fluorescent reporters in the Lyme disease spirochaete. Mol. Microbiol. 43:281-295.
15. Stevenson B, Bykowski T, Cooley AE, Babb K, Miller JC, Woodman ME, von Lackum K, Riley SP. 2006. The Lyme disease spirochete Erp lipoprotein family: structure, function and regulation of expression, p 354-372. In Cabello FC, Godfrey HP, HulinskaD(ed), Molecular biology of spirochetes. IOS Press, Amsterdam, Netherlands.
16. Casjens SR, Huang WM, Gilcrease EB, Qiu W, McCaig WD, Luft BJ, Schutzer SE, Fraser CM. 2006. Comparative genomics of Borrelia burgdorferi, p 79-95. In Cabello FC, Godfrey HP, Hulinska D (ed), Molecular biology of spirochetes. IOS Press, Amsterdam, Netherlands.
17. Porcella SF, Popova TG, Akins DR, Li M, Radolf JD, Norgard MV. 1996. Borrelia burgdorferi supercoiled plasmids encode multi-copy tandem open reading frames and a lipoprotein gene family. J. Bacteriol. 178:3293-3307
18. Lam TT, Nguyen T-PK, Montgomery RR, Kantor FS, Fikrig E, Flavell RA. 1994. Outer surface proteins E and F of Borrelia burgdorferi, the agent of Lyme disease. Infect. Immun. 62:290-298.
19. Akins DR, Porcella SF, Popova TG, Shevchenko D, Baker SI, Li M, Norgard MV, Radolf JD. 1995. Evidence for in vivo but not in vitro expression of a Borrelia burgdorferi outer surface protein F (OspF) homologue. Mol. Microbiol. 18:507-520.
20. Stevenson B, Schwan TG, Rosa PA. 1995. Temperature-related differential expression of antigens in the Lyme disease spirochete, Borrelia burgdorferi. Infect. Immun. 63:4535-4539.
21. Akins DR, Bourell KW, Caimano MJ, Norgard MV, Radolf JD. 1998. A new animal model for studying Lyme disease spirochetes in a mammalian host-adapted state. J. Clin. Invest. 101:2240-2250.
22. El-Hage N, Babb K, Carroll JA, Lindstrom N, Fischer ER, Miller JC, Gilmore RD, Mbow ML, Stevenson B. 2001. Surface exposure and protease insensitivity of Borrelia burgdorferi Erp (OspEF-related) lipoproteins. Microbiology 147:821-830.
23. Hefty PS, Jolliff SE, Caimano MJ, Wikel SK, Radolf JD, Akins DR. 2001. Regulation of OspE-related, OspF-related, and Elp lipoproteins of Borrelia burgdorferi strain 297 by mammalian host-specific signals. Infect. Immun. 69:3618-3627.
24. Hefty PS, Brooks CS, Jett AM, White GL, Wikel SK, Kennedy RC, Akins DR. 2002. OspE-related, OspF-related, and Elp lipoproteins are immunogenic in baboons experimentally infected with Borrelia burgdorferi and in human Lyme disease patients. J. Clin. Microbiol. 40:4256-4265.
25. Hefty PS, Jolliff SE, Caimano MJ, Wikel SK, Akins DR. 2002. Changes in the temporal and spatial patterns of outer surface lipoprotein expression generate population heterogeneity and antigenic diversity in the Lyme disease spirochete, Borrelia burgdorferi. Infect. Immun. 70:3468-3478.
26. Miller JC, von Lackum K, Babb K, McAlister JD, Stevenson B. 2003. Temporal analysis of Borrelia burgdorferi Erp protein expression throughout the mammal-tick infectious cycle. Infect. Immun. 71:6943-6952.
27. Miller JC, Narayan K, Stevenson B, Pachner AR. 2005. Expression of Borrelia burgdorferi erp genes during infection of non-human primates. Microb. Pathog. 39:27-33.
28. Miller JC, von Lackum K, Woodman ME, Stevenson B. 2006. Detection of Borrelia burgdorferi gene expression during mammalian infection using transcriptional fusions that produce green fluorescent protein. Microb. Pathog. 41:43-47.
29. Hellwage J, Meri T, Heikkilä T, Alitalo A, Panelius J, Lahdenne P, Seppälä IJT, Meri S. 2001. The complement regulatory factor H binds to the surface protein OspE of Borrelia burgdorferi. J. Biol. Chem. 276:8427-8435.
30. Kraiczy P, Skerka C, Brade V, Zipfel PF. 2001. Further characterization of complement regulator-acquiring surface proteins of Borrelia burgdorferi. Infect. Immun. 69:7800-7809.
31. Alitalo A, Meri T, Lankinen H, Seppälä I, Lahdenne P, Hefty PS, Akins D, Meri S. 2002. Complement inhibitor factor H binding to Lyme disease spirochetes is mediated by inducible expression of multiple plasmidencoded outer surface protein E paralogs. J. Immunol. 169:3847-3853.
32. Stevenson B, El-Hage N, Hines MA, Miller JC, Babb K. 2002. Differential binding of host complement inhibitor factor H by Borrelia burgdorferi Erp surface proteins: a possible mechanism underlying the expansive host range of Lyme disease spirochetes. Infect. Immun. 70:491-497.
33. Kraiczy P, Hellwage J, Skerka C, Kirschfink M, Brade V, Zipfel PF, Wallich R. 2003. Immune evasion of Borrelia burgdorferi: mapping of a complement inhibitor factor H-binding site of BbCRASP-3, a novel member of the Erp protein family. Eur. J. Immunol. 33:697-707.
34. Metts MS, McDowell JV, Theisen M, Hansen PR, Marconi RT. 2003. Analysis of the OspE determinants involved in binding of factor H and OspE-targeting antibodies elicited during Borrelia burgdorferi infection. Infect. Immun. 71:3587-3596.
35. Alitalo A, Meri T, Chen T, Lankinen H, Cheng Z-Z, Jokiranta TS, Seppälä IJT, Lahdenne P, Hefty PS, Akins DR, Meri S. 2004. Lysinedependent multipoint binding of the Borrelia burgdorferi virulence factor outer surface protein E to the C terminus of factor H. J. Immunol. 172: 6195-6201.
36. Kraiczy P, Hartmann K, Hellwage J, Skerka C, Brade V, Zipfel PF, Wallich R, Stevenson B. 2004. Immunological characterization of the complement regulator factor H-binding CRASP and Erp proteins of Borrelia burgdorferi. Int. J. Med. Microbiol. 293(Suppl 37):152-157.
37. Hovis KM, Tran E, Sundy CM, Buckles E, McDowell JV, Marconi RT. 2006. Selective binding of Borrelia burgdorferi OspE paralogs to factor H and serum proteins from diverse animals: possible expansion of the role of OspE in Lyme disease pathogenesis. Infect. Immun. 74:1967-1972.
38. Bykowski T, Woodman ME, Cooley AE, Brissette CA, Brade V, Wallich R, Kraiczy P, Stevenson B. 2007. Coordinated expression of Borrelia burgdorferi complement regulator-acquiring surface proteins during the Lyme disease spirochete's mammal-tick infection cycle. Infect. Immun. 75:4227-4236.
39. Haupt K, Kraiczy P, Wallich R, Brade V, Skerka C, Zipfel PF. 2007. Binding of human FHR-1 to serum resistant Borrelia burgdorferi is mediated by borrelial complement regulator-acquiring surface proteins. J. Infect. Dis. 196:124-133.
40. Brissette CA, Cooley AE, Burns LH, Riley SP, Verma A, Woodman ME, Bykowski T, Stevenson B. 2008. Lyme borreliosis spirochete Erp proteins, their known host ligands, and potential roles in mammalian infection. Int. J. Med. Microbiol. 298(Suppl 1):257-267.
41. Brissette CA, Haupt K, Barthel D, Cooley AE, Bowman A, Skerka C, Wallich R, Zipfel PF, Kraiczy P, Stevenson B. 2009. Borrelia burgdorferi infection-associated surface proteins ErpP, ErpA, and ErpC bind human plasminogen. Infect. Immun. 77:300-306.
42. Brissette CA, Verma A, Bowman A, Cooley AE, Stevenson B. 2009. The Borrelia burgdorferi outer-surface protein ErpX binds mammalian laminin. Microbiology 155:863-872.
43. Siegel C, Hallström T, Skerka C, Eberhardt H, Uzonyi B, Beckhaus T, Karas M, Wallich R, Stevenson B, Zipfel PF, Kraiczy P. 2010. Complement factor H-related proteins CFHR2 and CFHR5 represent novel ligands for the infection-associated CRASP proteins of Borrelia burgdorferi. PLoS One 5:e13519. doi:10.1371/journal.pone.0013519.
44. Kenedy MR, Akins DR. 2011. The OspE-related proteins inhibit complement deposition and enhance serum resistance of Borrelia burgdorferi, the Lyme disease agent. Infect. Immun. 79:1451-1457.
45. Stevenson B, Porcella SF, Oie KL, Fitzpatrick CA, Raffel SJ, Lubke L, Schrumpf ME, Schwan TG. 2000. The relapsing fever spirochete Borrelia hermsii contains multiple, antigen-encoding circular plasmids that are homologous to the cp32 plasmids of Lyme disease spirochetes. Infect. Immun. 68:3900-3908.
46. Stevenson B, Miller JC. 2003. Intra-and interbacterial genetic exchange of Lyme disease spirochete erp genes generates sequence identity amidst diversity. J. Mol. Evol. 57:309-324.
47. Qiu WG, Schutzer SE, Bruno JF, Attie O, Xu Y, Dunn JJ, Casjens SR, Luft BJ. 2004. Genetic exchange and plasmid transfers in Borrelia burgdorferi sensu stricto revealed by three-way genome comparisons and multilocus sequence typing. Proc. Natl. Acad. Sci. U. S. A. 101:14150-14155.
48. Wywial E, Haven J, Casjens SR, Hernandez YA, Singh S, Mongodin EF, Fraser-Liggett CM, Luft BJ, Schutzer SE, Qiu WG. 2009. Fast, adaptive evolution at a bacterial host-resistance locus: the PFam54 gene array in Borrelia burgdorferi. Gene 445:26-37.
49. Casjens SR, Fraser-Liggett CM, Mongodin EF, Qiu WG, Dunn JJ, Luft BJ, Schutzer SE. 2011. Whole genome sequence of an unusual Borrelia burgdorferi sensu lato isolate. J. Bacteriol. 193:1489-1490.
50. Casjens SR, Mongodin EF, Qiu WG, Dunn JJ, Luft BJ, Fraser-Liggett CM, Schutzer SE. 2011. Whole-genome sequences of two Borrelia afzelii and two Borrelia garinii Lyme disease agent isolates. J. Bacteriol. 193:6995-6996.
51. Schutzer SE, Fraser-Liggett CM, Casjens SR, Qiu WG, Dunn JJ, Mongodin EF, Luft BJ. 2011. Whole genome sequences of thirteen isolates of Borrelia burgdorferi. J. Bacteriol. 193:1018-1020.
52. Casjens SR, Mongodin EF, Qiu WG, Luft BJ, Schutzer SE, Gilcrease EB, Huang WM, Vujadinovic M, Aron JK, Vargas LC, Freeman S, Radune D, Weidman JF, Dimitrov GI, Khouri HM, Sosa JE, Halpin RA, Dunn JJ, Fraser CM. 2012. Genome stability of Lyme disease spirochetes: comparative genomics of Borrelia burgdorferi plasmids. PLoS One 7:e33280. doi:10.1371/journal.pone.0033280.
53. Schutzer SE, Fraser-Liggett CM, Qiu WG, Kraiczy P, Mongodin EF, Dunn JJ, Luft BJ, Casjens SR. 2012. Whole-genome sequences of Borrelia bissettii, Borrelia valaisiana, and Borrelia spielmanii. J. Bacteriol. 194:545-546.
54. Morlon H, Kemps BD, Plotkin JB, Brisson D. 2012. Explosive radiation of a bacterial species group. Evolution 66:2577-2586.
55. Wang G, Ojaimi C, Iyer R, Saksenberg V, McClain SA, Wormser GP, Schwartz IA. 2001. Impact of genotypic variation of Borrelia burgdorferi sensu stricto on kinetics of dissemination and severity of disease in C3H/ HeJ mice. Infect. Immun. 69:4303-4312.
56. Ojaimi C, Mulay V, Liveris D, Iyer R, Schwartz I. 2005. Comparative transcriptional profiling of Borrelia burgdorferi clinical isolates differing in capacities for hematogenous dissemination. Infect. Immun. 73:6791-6802.
57. Marconi RT, Sung SY, Hughes CAN, Carlyon JA. 1996. Molecular and evolutionary analyses of a variable series of genes in Borrelia burgdorferi that are related to ospE and ospF, constitute a gene family, and share a common upstream homology box. J. Bacteriol. 178:5615-5626.
58. Miller JC, Stevenson B. 2003. Immunological and genetic characterization of Borrelia burgdorferi BapA and EppA proteins. Microbiology 149: 1113-1125.
59. Wallich R, Brenner C, Kramer MD, Simon MM. 1995. Molecular cloning and immunological characterization of a novel linear-plasmidencoded gene, pG, of Borrelia burgdorferi expressed only in vivo. Infect. Immun. 63:3327-3335.
60. Katoh K, Kuma K, Toh H, Miyata T. 2005. MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33: 511-518.
61. Suyama M, Torrents D, Bork P. 2006. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34:W609-W612.
62. Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ. 1998. Multiple sequence alignment with Clustal X. Trends Biochem. Sci. 23: 403-405.
63. Needleman SB, Wunsch CD. 1970. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J. Mol. Biol. 48:443-453.
64. Gonnet GH, Cohen MA, Benner SA. 1992. Exhaustive matching of the entire protein sequence database. Science 256:1443-1445.
65. Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P. 2010. RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462-2463.
66. Martin D, Rybicki E. 2000. RDP: detection of recombination amongst aligned sequences. Bioinformatics 16:562-563.
67. Padidam M, Sawyer S, Fauquet CM. 1999. Possible emergence of new geminiviruses by frequent recombination. Virology 265:218-225.
68. Posada D, Crandall KA. 2001. Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc. Natl. Acad. Sci. U. S. A. 98:13757-13762.
69. Smith JM. 1992. Analyzing the mosaic structure of genes. J. Mol. Evol. 35:126-129.
70. Salminen M, Carr J, Burke D, McCutchan F. 1995. Identification of breakpoints in intergenotypic recombinants of HIV-1 by bootscanning. AIDS Res. Hum. Retroviruses 11:1423-1425.
71. Martin DP, Posada D, Crandall KA, Williamson C. 2005. A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res. Hum. Retroviruses 21:98-102.
72. Gibbs MJ, Armstrong JS, Gibbs AJ. 2000. Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16:573-582.
73. Boni MF, Posada D, Feldman MW. 2007. An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 176: 1035-1047.
74. Sadziene A, Wilske B, Ferdows MS, Barbour AG. 1993. The cryptic ospC gene of Borrelia burgdorferi B31 is located on a circular plasmid. Infect. Immun. 61:2192-2195.
75. Stevenson B, Casjens S, van Vugt R, Porcella SF, Tilly K, Bono JL, Rosa P. 1997. Characterization of cp18, a naturally truncated member of the cp32 family of Borrelia burgdorferi plasmids. J. Bacteriol. 179:4285-4291.
76. Caimano MJ, Yang X, Popova TG, Clawson ML, Akins DR, Norgard MV, Radolf JD. 2000. Molecular and evolutionary characterization of the cp32/18 family of supercoiled plasmids in Borrelia burgdorferi 297. Infect. Immun. 68:1574-1586.
77. Zückert WR, Meyer J. 1996. Circular and linear plasmids of Lyme disease spirochetes have extensive homology: characterization of a repeated DNA element. J. Bacteriol. 178:2287-2298.
78. Babb K, McAlister JD, Miller JC, Stevenson B. 2004. Molecular characterization of Borrelia burgdorferi erp promoter/operator elements. J. Bacteriol. 186:2745-2756.
79. Babb K, Bykowski T, Riley SP, Miller MC, DeMoll E, Stevenson B. 2006. Borrelia burgdorferi EbfC, a novel, chromosomal encoded protein, binds specific DNA sequences adjacent to erp loci on the spirochete's resident cp32 prophages. J. Bacteriol. 188:4331-4339.
80. Riley SP, Bykowski TT, Cooley AE, Burns LH, Babb K, Brissette CA, Bowman A, Rotondi M, Miller MC, DeMoll E, Lim K, Fried MG, Stevenson B. 2009. Borrelia burgdorferi EbfC defines a newly-identified, widespread family of bacterial DNA-binding proteins. Nucleic Acids Res. 37:1973-1983.
81. Burns LH, Adams CA, Riley SP, Jutras BL, Bowman A, Chenail AM, Cooley AE, Haselhorst LA, Moore AM, Babb K, Fried MG, Stevenson B. 2010. BpaB, a novel protein encoded by the Lyme disease spirochete's cp32 prophages, binds to erp operator 2 DNA. Nucleic Acids Res. 38:5443-5455.
82. Jutras BL, Verma A, Adams CA, Brissette CA, Burns LH, Whetstine CR, Bowman A, Chenail AM, Zückert WR, Stevenson B. 2012. BpaB and EbfC DNA-binding proteins regulate production of the Lyme disease spirochete's infection-associated Erp surface proteins. J. Bacteriol. 194:778-786.
83. Jutras BL, Bowman A, Brissette CA, Adams CA, Verma A, Chenail AM, Stevenson B. 2012. EbfC (YbaB) is a new type of bacterial nucleoidassociated protein and a global regulator of gene expression in the Lyme disease spirochete. J. Bacteriol. 194:3395-3406.
84. Das S, Barthold SW, Stocker Giles S, Montgomery RR, Telford SR, Fikrig E. 1997. Temporal pattern of Borrelia burgdorferi p21 expression in ticks and the mammalian host. J. Clin. Invest. 99:987-995.
85. Schulze RJ, Zückert WR. 2006. Borrelia burgdorferi lipoproteins are secreted to the outer surface by default. Mol. Microbiol. 59:1473-1484.
86. Setubal JC, Reis M, Matsunaga J, Haake DA. 2006. Lipoprotein computational prediction in spirochaetal genomes. Microbiology 152:113-121.
87. Kumru OS, Schulze RJ, Rodnin MV, Ladokhin AS, Zückert WR. 2011. Surface localization determinants of Borrelia OspC/Vsp family lipoproteins. J. Bacteriol. 193:2814-2825.
88. Stevenson B, Bono JL, Schwan TG, Rosa P. 1998. Borrelia burgdorferi Erp proteins are immunogenic in mammals infected by tick bite, and their synthesis is inducible in cultured bacteria. Infect. Immun. 66:2648-2654.
89. McDowell JV, Sung SY, Price G, Marconi RT. 2001. Demonstration of the genetic stability and temporal expression of select members of the Lyme disease spirochete OspF protein family during infection in mice. Infect. Immun. 69:4831-4838.
90. El-Hage N, Stevenson B. 2002. Simultaneous coexpression of Borrelia burgdorferi Erp proteins occurs through a specific, erp locus-directed regulatory mechanism. J. Bacteriol. 184:4536-4543.
91. Jutras BL, Chenail AM, Stevenson B. 2013. Changes in bacterial growth rate govern expression of the Borrelia burgdorferi OspC and Erp infectionassociated surface proteins. J. Bacteriol. 195:757-764.
92. Eggers CH, Caimano MJ, Radolf JD. 2006. Sigma factor selectivity in Borrelia burgdorferi: RpoS recognition of the ospE/ospF/elp promoters is dependent on the sequence of the -10 region. Mol. Microbiol. 59:1859-1875.
93. Eggers CH, Caimano MJ, Radolf JD. 2004. Analysis of promoter elements involved in the transcription initiation of RpoS-dependent Borrelia burgdorferi genes. J. Bacteriol. 186:7390-7402.
94. Caimano MJ, Iyer R, Eggers CH, Gonzalez C, Morton EA, Gilbert MA, Schwartz I, Radolf JD. 2007. Analysis of the RpoS regulon in Borrelia burgdorferi in response to mammalian host signals provides insight into RpoS function during the enzootic cycle. Mol. Microbiol. 65:1193-1217.
95. Seling A, Siegel C, Fingerle V, Jutras BL, Brissette CA, Skerka C, Wallich R, Zipfel PF, Stevenson B, Kraiczy P. 2010. Functional characterization of Borrelia spielmanii outer surface proteins that interact with distinct members of the human factorHprotein family and with plasminogen. Infect. Immun. 78:39-48.
96. El-Hage N, Lieto LD, Stevenson B. 1999. Stability of erp loci during Borrelia burgdorferi infection: recombination is not required for chronic infection of immunocompetent mice. Infect. Immun. 67:3146-3150.
97. Stevenson B. 2002. Borrelia burgdorferi erp (ospE-related) gene sequences remain stable during mammalian infection. Infect. Immun. 70:5307-5311.
98. Sung SY, McDowell JV, Carlyon JA, Marconi RT. 2000. Mutation and recombination in the upstream homology box-flanked ospE-related genes of the Lyme disease spirochetes result in the development of new antigenic variants during infection. Infect. Immun. 68:1319-1327.