Analysis of an Ordered, Comprehensive STM Mutant Library in Infectious Borrelia burgdorferi: Insights into the Genes Required for Mouse Infectivity

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Lin, Tao ^a   Gao, Lihui ^a   Zhang, Chuhua ^a   Odeh, Evelyn ^a   Jacobs, Mary B ^b   Coutte, Loïc ^a,d   Chaconas, George ^c   Philipp, Mario T ^b   Norris, Steven J ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b TULANE NATIONAL PRIMATE RESEARCH CENTER   (United States)

^c UNIVERSITY OF CALGARY   (Canada)

^d INSTITUT PASTEUR DE LILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNAB HELICASE; PERIPLASMIC PROTEIN; PHOSPHOENOLPYRUVATE SUGAR PHOSPHOTRANSFERASE; RNA 16S;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BORRELIA BURGDORFERI; CHEMOTAXIS; CONTROLLED STUDY; DNA EXTRACTION; GENE CONSTRUCT; GENE INSERTION; GENE LOCUS; GENE MAPPING; GENE MUTATION; GENE SEQUENCE; HIGH THROUGHPUT SCREENING; LYME DISEASE; MUTAGENESIS; NONHUMAN; PATHOGENESIS; PLASMID; REPLICON; TRANSPOSON;

ANIMALS; BORRELIA BURGDORFERI; CHEMOTAXIS; DNA TRANSPOSABLE ELEMENTS; GENE LIBRARY; LYME DISEASE; MICE; MICE, INBRED C3H; MODELS, BIOLOGICAL; MODELS, GENETIC; MUTAGENESIS; MUTATION; PLASMIDS; SEQUENCE ANALYSIS, DNA; TICKS;

BORRELIA; BORRELIA BURGDORFERI; MUS;

EID: 84868153034     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047532     Document Type: Article

References (91)

1. Steere AC, Coburn J, Glickstein L, (2004) The emergence of Lyme disease. J Clin Invest 113: 1093-1101.
2. Samuels DS, Radolf JD (2010) Borrelia: Molecular Biology, Host Interaction and Pathogenesis. Hethersett, Norwich, UK: Caister Academic Press.
3. Lane RS, Piesman J, Burgdorfer W, (1991) Lyme borreliosis: relation of its causative agent to its vectors and hosts in North America and Europe. Annu Rev Entomol 36: 587-609.
4. Fraser CM, Casjens S, Huang WM, Sutton GG, Clayton R, et al. (1997) Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390: 580-586.
5. Casjens S, Palmer N, van Vugt R, Huang WM, Stevenson B, 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.
6. Rosa PA, Tilly K, Stewart PE, (2005) The burgeoning molecular genetics of the Lyme disease spirochaete. Nat Rev Microbiol 3: 129-143.
7. Norris SJ, Coburn J, Leong JM, Hu LT, Höök M (2010) Pathobiology of Lyme disease Borrelia. In: Samuels DS, Radolf JD, editors. Borrelia: Molecular and Cellular Biology. Hethersett, Norwich, UK: Caister Academic Press. 299-331.
8. Purser JE, Norris SJ, (2000) Correlation between plasmid content and infectivity in Borrelia burgdorferi. Proc Natl Acad Sci USA 97: 13865-13870.
9. Purser JE, Lawrenz MB, Caimano MJ, Howell JK, Radolf JD, et al. (2003) A plasmid-encoded nicotinamidase (PncA) is essential for infectivity of Borrelia burgdorferi in a mammalian host. Mol Microbiol 48: 753-764.
10. Grimm D, Eggers CH, Caimano MJ, Tilly K, Stewart PE, 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.
11. Labandeira-Rey M, Baker E, Skare J, (2001) Decreased infectivity in Borrelia burgdorferi strain B31 is associated with loss of linear plasmid 25 or 28-1. Infect Immun 69: 446-455.
12. Labandeira-Rey M, Seshu J, Skare JT, (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.
13. Revel AT, Blevins JS, Almazan C, Neil L, Kocan KM, 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.
14. Jewett MW, Lawrence K, Bestor AC, Tilly K, Grimm D, et al. (2007) The critical role of the linear plasmid lp36 in the infectious cycle of Borrelia burgdorferi. Mol Microbiol 64: 1358-1374.
15. Jewett MW, Byram R, Bestor A, Tilly K, Lawrence K, et al. (2007) Genetic basis for retention of a critical virulence plasmid of Borrelia burgdorferi. Mol Microbiol 66: 975-990.
16. Byram R, Stewart PE, Rosa P, (2004) The essential nature of the ubiquitous 26-kilobase circular replicon of Borrelia burgdorferi. J Bacteriol 186: 3561-3569.
17. Grimm D, Tilly K, Byram R, Stewart PE, Krum JG, et al. (2004) Outer-surface protein C of the Lyme disease spirochete: a protein induced in ticks for infection of mammals. Proc Natl Acad Sci U S A 101: 3142-3147.
18. Pal U, Yang X, Chen M, Bockenstedt LK, Anderson JF, et al. (2004) OspC facilitates Borrelia burgdorferi invasion of Ixodes scapularis salivary glands. J Clin Invest 113: 220-230.
19. Stewart PE, Wang X, Bueschel DM, Clifton DR, Grimm D, et al. (2006) Delineating the requirement for the Borrelia burgdorferi virulence factor OspC in the mammalian host. Infect Immun 74: 3547-3553.
20. Tilly K, Krum JG, Bestor A, Jewett MW, Grimm D, et al. (2006) Borrelia burgdorferi OspC protein required exclusively in a crucial early stage of mammalian infection. Infect Immun 74: 3554-3564.
21. Tilly K, Bestor A, Dulebohn DP, Rosa PA, (2009) OspC-independent infection and dissemination by host-adapted Borrelia burgdorferi. Infect Immun 77: 2672-2682.
22. Zhang JR, Hardham JM, Barbour AG, Norris SJ, (1997) Antigenic variation in Lyme disease borreliae by promiscuous recombination of VMP-like sequence cassettes. Cell 89: 275-285.
23. Bankhead T, Chaconas G, (2007) The role of VlsE antigenic variation in the Lyme disease spirochete: persistence through a mechanism that differs from other pathogens. Mol Microbiol 65: 1547-1558.
24. Pal U, Li X, Wang T, Montgomery RR, Ramamoorthi N, et al. (2004) TROSPA, an Ixodes scapularis receptor for Borrelia burgdorferi. Cell 119: 457-468.
25. Schwan TG, Piesman J, (2000) Temporal changes in outer surface proteins A and C of the Lyme disease- associated spirochete, Borrelia burgdorferi, during the chain of infection in ticks and mice. J Clin Microbiol 38: 382-388.
26. Schwan TG, (2003) Temporal regulation of outer surface proteins of the Lyme-disease spirochaete Borrelia burgdorferi. Biochem Soc Trans 31: 108-112.
27. Schwan TG, Piesman J, Golde WT, Dolan MC, Rosa PA, (1995) Induction of an outer surface protein on Borrelia burgdorferi during tick feeding. Proc Natl Acad Sci USA 92: 2909-2913.
28. Yang XF, Pal U, Alani SM, Fikrig E, Norgard MV, (2004) Essential role for OspA/B in the life cycle of the Lyme disease spirochete. J Exp Med 199: 641-648.
29. Lawrenz MB, Kawabata H, Purser JE, Norris SJ, (2002) Decreased electroporation efficiency in Borrelia burgdorferi containing linear plasmids lp25 and lp56: impact on transformation of infectious B. burgdorferi. Infect Immun 70: 4798-4804.
30. Kawabata H, Norris SJ, Watanabe H, (2004) BBE02 disruption mutants of Borrelia burgdorferi B31 have a highly transformable, infectious phenotype. Infect Immun 72: 7147-7154.
31. Muñoz-López M, García-Pérez JL, (2010) DNA transposons: nature and applications in genomics. Curr Genomics 11: 115-128.
32. Hayes F, (2003) Transposon-based strategies for microbial functional genomics and proteomics. Ann Rev Genetics 37: 3-29.
33. Judson N, Mekalanos JJ, (2000) Transposon-based approaches to identify essential bacterial genes. Trends Microbiol 8: 521-526.
34. Lampe DJ, Akerley BJ, Rubin EJ, Mekalanos JJ, Robertson HM, (1999) Hyperactive transposase mutants of the Himar1 mariner transposon. Proc Natl Acad Sci U S A 96: 11428-11433.
35. Hensel M, Shea JE, Gleeson C, Jones MD, Dalton E, et al. (1995) Simultaneous identification of bacterial virulence genes by negative selection. Science 269: 400-403.
36. Autret N, Charbit A, (2005) Lessons from signature-tagged mutagenesis on the infectious mechanisms of pathogenic bacteria. FEMS Microbiology Reviews 29: 703-717.
37. Saenz HL, Dehio C, (2005) Signature-tagged mutagenesis: technical advances in a negative selection method for virulence gene identification. Current Opinion in Microbiology 8: 612-619.
38. Stewart PE, Hoff J, Fischer E, Krum JG, Rosa PA, (2004) Genome-wide transposon mutagenesis of Borrelia burgdorferi for identification of phenotypic mutants. Appl Environ Microbiol 70: 5973-5979.
39. Botkin DJ, Abbott AN, Stewart PE, Rosa PA, Kawabata H, et al. (2006) Identification of potential virulence determinants by Himar1 transposition of infectious Borrelia burgdorferi B31. Infect Immun 74: 6690-6699.
40. Stewart PE, Rosa PA, (2008) Transposon mutagenesis of the Lyme disease agent Borrelia burgdorferi. Methods Mol Biol 431: 85-95.
41. Gallagher LA, Ramage E, Jacobs MA, Kaul R, Brittnacher M, et al. (2007) A comprehensive transposon mutant library of Francisella novicida, a bioweapon surrogate. Proc Natl Acad Sci USA 104: 1009-1014.
42. Tilly K, Checroun C, Rosa PA, (2012) Requirements for Borrelia burgdorferi plasmid maintenance. Plasmid 68: 1-12.
43. Tourand Y, Lee L, Chaconas G, (2007) Telomere resolution by Borrelia burgdorferi ResT through the collaborative efforts of tethered DNA binding domains. Mol Microbiol 64: 580-590.
44. Kobryn K, Chaconas G, (2002) ResT, a telomere resolvase encoded by the Lyme disease spirochete. Mol Cell 9: 195-201.
45. Norris SJ, Howell JK, Odeh EA, Lin T, Gao L, et al. (2011) High-throughput plasmid content analysis of Borrelia burgdorferi B31 by using Luminex multiplex technology. Appl Environ Microbiol 77: 1483-1492.
46. Grimm D, Elias AF, Tilly K, Rosa PA, (2003) Plasmid stability during in vitro propagation of Borrelia burgdorferi assessed at a clonal level. Infect Immun 71: 3138-3145.
47. Beaurepaire C, Chaconas G, (2005) Mapping of essential replication functions of the linear plasmid lp17 of B. burgdorferi by targeted deletion walking. Mol Microbiol 57: 132-142.
48. Deneke J, Chaconas G, (2008) Purification and properties of the plasmid maintenance proteins from the Borrelia burgdorferi linear plasmid lp17. J Bacteriol 190: 3992-4000.
49. Eggers CH, Caimano MJ, Clawson ML, Miller WG, Samuels DS, 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 the expression of fluorescent reporters in the Lyme disease spirochaete. Mol Microbiol 43: 281-295.
50. Lin T, Gao L, Edmondson DG, Jacobs MB, Philipp MT, et al. (2009) Central role of the Holliday junction helicase RuvAB in vlsE recombination and infectivity of Borrelia burgdorferi. PLoS Pathog 5: e1000679.
51. Botkin DJ, Abbott A, Howell JK, Mosher M, Stewart PE, et al. (2006) Transposon mutagenesis of infectious Borrelia burgdorferi B31: a pilot study. In: Cabello FC, Hulinska D, Godfrey HP, editors. Molecular Biology of Spirochetes. Amsterdam: IOS Press. 13-23.
52. Jewett MW, Jain S, Linowski AK, Sarkar A, Rosa PA, (2011) Molecular characterization of the Borrelia burgdorferi in vivo-essential protein PncA. Microbiology 157: 2831-2840.
53. Strother KO, Broadwater A, De Silva A, (2005) Plasmid requirements for infection of ticks by Borrelia burgdorferi. Vector Borne Zoonotic Dis 5: 237-245.
54. Zhang L, Zhang Y, Adusumilli S, Liu L, Narasimhan S, et al. (2012) Molecular interactions that enable movement of the Lyme disease agent from the tick gut into the hemolymph. PLoS Pathog 7: e1002079.
55. Rhodes RG, Atoyan JA, Nelson DR, (2010) The chitobiose transporter, chbC, is required for chitin utilization in Borrelia burgdorferi. BMC Microbiol 10: 21.
56. Tilly K, Elias AF, Errett J, Fischer E, Iyer R, et al. (2001) Genetics and regulation of chitobiose utilization in Borrelia burgdorferi. J Bacteriol 183: 5544-5553.
57. Feng S, Hodzic E, Barthold SW, (2000) Lyme arthritis resolution with antiserum to a 37-kilodalton Borrelia burgdorferi protein. Infect Immun 68: 4169-4173.
58. Barthold SW, Hodzic E, Tunev S, Feng S, (2006) Antibody-mediated disease remission in the mouse model of Lyme borreliosis. Infect Immun 74: 4817-4825.
59. Feng S, Hodzic E, Freet K, Barthold SW, (2003) Immunogenicity of Borrelia burgdorferi arthritis-related protein. Infect Immun 71: 7211-7214.
60. Li X, Liu X, Beck DS, Kantor FS, Fikrig E, (2006) Borrelia burgdorferi lacking BBK32, a fibronectin-binding protein, retains full pathogenicity. Infect Immun 74: 3305-3313.
61. Seshu J, Esteve-Gassent MD, Labandeira-Rey M, Kim JH, Trzeciakowski JP, et al. (2006) Inactivation of the fibronectin-binding adhesin gene bbk32 significantly attenuates the infectivity potential of Borrelia burgdorferi. Mol Microbiol 59: 1591-1601.
62. Norman MU, Moriarty TJ, Dresser AR, Millen B, Kubes P, et al. (2008) Molecular mechanisms involved in vascular interactions of the Lyme disease pathogen in a living host. PLoS Pathog 4: e1000169.
63. Hagman KE, Yang X, Wikel SK, Schoeler GB, Caimano MJ, et al. (2000) Decorin-binding protein A (DbpA) of Borrelia burgdorferi is not protective when immunized mice are challenged via tick infestation and correlates with the lack of DbpA expression by B. burgdorferi in ticks. Infect Immun 68: 4759-4764.
64. Mulay V, Caimano MJ, Liveris D, Desrosiers DC, Radolf JD, et al. (2007) Borrelia burgdorferi BBA74, a periplasmic protein associated with the outer membrane, lacks porin-like properties. J Bacteriol 189: 2063-2068.
65. Mulay VB, Caimano MJ, Iyer R, Dunham-Ems S, Liveris D, et al. (2009) Borrelia burgdorferi bba74 is expressed exclusively during tick feeding and is regulated by both arthropod- and mammalian host-specific signals. J Bacteriol 191: 2783-2794.
66. Skare JT, Champion CI, Mirzabekov TA, Shang ES, Blanco DR, et al. (1996) Porin activity of the native and recombinant outer membrane protein Oms28 of Borrelia burgdorferi. J Bacteriol 178: 4909-4918.
67. Sze CW, Zhang K, Kariu T, Pal U, Li C, (2012) Borrelia burgdorferi needs chemotaxis to establish infection in mammals and to accomplish its enzootic cycle. Infect Immun 80: 2485-2492.
68. Szurmant H, Ordal GW, (2004) Diversity in chemotaxis mechanisms among the bacteria and archaea. Microbiol Mol Biol Rev 68: 301-319.
69. Liu J, Hu B, Morado DR, Jani S, Manson MD, et al. (2012) Molecular architecture of chemoreceptor arrays revealed by cryoelectron tomography of Escherichia coli minicells. Proc Natl Acad Sci (USA): In press.
70. Motaleb MA, Sultan SZ, Miller MR, Li C, Charon NW, (2011) CheY3 of Borrelia burgdorferi is the key response regulator essential for chemotaxis and forms a long-lived phosphorylated intermediate. J Bacteriol 193: 3332-3341.
71. Escalante A, Salinas Cervantes A, Gosset G, Bolivar F, (2012) Current knowledge of the Escherichia coli phosphoenolpyruvate-carbohydrate phosphotransferase system: peculiarities of regulation and impact on growth and product formation. Appl Microbiol Biotechnol 94: 1483-1494.
72. Stewart PE, Thalken R, Bono JL, Rosa P, (2001) Isolation of a circular plasmid region sufficient for autonomous replication and transformation of infectious Borrelia burgdorferi. Mol Microbiol 39: 714-721.
73. Stewart PE, Chaconas G, Rosa P, (2003) Conservation of plasmid maintenance functions between linear and circular plasmids in Borrelia burgdorferi. J Bacteriol 185: 3202-3209.
74. Chaconas G, Kobryn K, (2010) Structure, function, and evolution of linear replicons in Borrelia. Ann Rev Microbiol 64: 185-202.
75. Kobryn K, Chaconas G, (2005) Fusion of hairpin telomeres by the B. burgdorferi telomere resolvase ResT implications for shaping a genome in flux. Mol Cell 17: 783-791.
76. Chaconas G (2010) Replication of the B. burgdorferi genome and scrambling of the linear replicons through reverse telomere resolution. In: Samuels DS, Radolf JD, editors. Borrelia: Molecular Biology, Host Interaction and Pathogenesis. Hethersett, Norwich, UK: Caister Academic Press. 55-66.
77. Indest KJ, Howell JK, Jacobs MB, Scholl-Meeker D, Norris SJ, et al. (2001) Analysis of Borrelia burgdorferi vlsE gene expression and recombination in the tick vector. Infect Immun 69: 7083-7090.
78. Sze CW, Zhang K, Kariu T, Pal U, Li C (2012) Borrelia burgdorferi needs chemotaxis to establish infection in mammals and to accomplish its enzootic cycle. Infect Immun: Epub ahead of print.
79. Li C, Xu H, Zhang K, Liang FT, (2010) Inactivation of a putative flagellar motor switch protein FliG1 prevents Borrelia burgdorferi from swimming in highly viscous media and blocks its infectivity. Molec Microbiol 75: 1563-1576.
80. Stevenson B, Babb K, (2002) LuxS-mediated quorum sensing in Borrelia burgdorferi, the Lyme disease spirochete. Infect Immun 70: 4099-4105.
81. Miller JC, Stevenson B, (2004) Increased expression of Borrelia burgdorferi factor H-binding surface proteins during transmission from ticks to mice. Int J Med Microbiol 293Suppl 37: 120-125.
82. Stevenson B, von Lackum K, Wattier RL, McAlister JD, Miller JC, et al. (2003) Quorum sensing by the Lyme disease spirochete. Microbes Infect 5: 991-997.
83. Blevins JS, Revel AT, Caimano MJ, Yang XF, Richardson JA, et al. (2004) The luxS gene is not required for Borrelia burgdorferi tick colonization, transmission to a mammalian host, or induction of disease. Infect Immun 72: 4864-4867.
84. von Lackum K, Babb K, Riley SP, Wattier RL, Bykowski T, et al. (2006) Functionality of Borrelia burgdorferi LuxS: the Lyme disease spirochete produces and responds to the pheromone autoinducer-2 and lacks a complete activated-methyl cycle. Int J Med Microbiol 296Suppl 40: 92-102.
85. Babb K, von Lackum K, Wattier RL, Riley SP, Stevenson B, (2005) Synthesis of autoinducer 2 by the Lyme disease spirochete, Borrelia burgdorferi. J Bacteriol 187: 3079-3087.
86. Hübner A, Revel AT, Nolen DM, Hagman KE, Norgard MV, (2003) Expression of a luxS gene is not required for Borrelia burgdorferi infection of mice via needle inoculation. Infect Immun 71: 2892-2896.
87. Barbour AG, (1984) Isolation and cultivation of Lyme disease spirochetes. Yale J Biol Med 57: 521-525.
88. Lehoux DE, Sanschagrin F, Levesque RC (1999) Defined oligonucleotide tag pools and PCR screening in signature-tagged mutagenesis of essential genes from bacteria. Biotechniques 26: 473-478, 480.
89. Hunt TA, Kooi C, Sokol PA, Valvano MA, (2004) Identification of Burkholderia cenocepacia genes required for bacterial survival in vivo. Infect Immun 72: 4010-4022.
90. Samuels DS, (1995) Electrotransformation of the spirochete Borrelia burgdorferi. Methods Mol Biol 47: 253-259.
91. Norris SJ, Howell JK, Garza SA, Ferdows MS, Barbour AG, (1995) High- and low-infectivity phenotypes of clonal populations of in vitro-cultured Borrelia burgdorferi. Infect Immun 63: 2206-2212.