A novel gene inactivation system reveals altered periplasmic flagellar orientation in a Borrelia burgdorferi flil mutant

Journal of Bacteriology

Volumn 193, Issue 13, 2011, Pages 3324-3331

  Motaleb, M A ^a   Pitzer, Joshua E ^a   Sultan, Syed Z ^a   Liu, Jun ^b  

^a EAST CAROLINA UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FLIL PROTEIN; RNA POLYMERASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIAL GENE; BORRELIA BURGDORFERI; CONTROLLED STUDY; ELECTRON TOMOGRAPHY; FLAGELLUM; GENE INACTIVATION; GENE MUTATION; METHODOLOGY; MORPHOLOGY; NONHUMAN; OPERON; PRIORITY JOURNAL; WILD TYPE;

BACTERIAL PROTEINS; BORRELIA BURGDORFERI; CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPE TOMOGRAPHY; FLAGELLA; GENE KNOCKOUT TECHNIQUES; GENE SILENCING; GENETIC COMPLEMENTATION TEST; GENETICS, MICROBIAL; LOCOMOTION; MEMBRANE PROTEINS; PERIPLASMIC PROTEINS;

BORRELIA BURGDORFERI;

EID: 79959326635     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00202-11     Document Type: Article

References (58)

1. Aldridge, P., and K. T. Hughes. 2002. Regulation of flagellar assembly. Curr. Opin. Microbiol. 5:160-165.
2. Aldridge, P., and U. Jenal. 1999. Cell cycle-dependent degradation of a flagellar motor component requires a novel-type response regulator. Mol. Microbiol. 32:379-391.
3. Attmannspacher, U., B. E. Scharf, and R. M. Harshey. 2008. FliL is essential for swarming: motor rotation in absence of FliL fractures the flagellar rod in swarmer cells of Salmonella enterica. Mol. Microbiol. 68:328-341.
4. Bakker, R. G., C. Li, M. R. Miller, C. Cunningham, and N. W. Charon. 2007. Identification of specific chemoattractants and genetic complementation of a Borrelia burgdorferi chemotaxis mutant: flow cytometry-based capillary tube chemotaxis assay. Appl. Environ. Microbiol. 73:1180-1188.
5. Belas, R., and R. Suvanasuthi. 2005. The ability of Proteus mirabilis to sense surfaces and regulate virulence gene expression involves FliL, a flagellar basal body protein. J. Bacteriol. 187:6789-6803.
6. Bono, J. L., et al. 2000. Efficient targeted mutagenesis in Borrelia burgdorferi. J. Bacteriol. 182:2445-2452.
7. Canale-Parola, E. 1978. Motility and chemotaxis of spirochetes. Annu. Rev. Microbiol. 32:69-99.
8. Carroll, J. A., N. El Hage, J. C. Miller, K. Babb, and B. Stevenson. 2001. Borrelia burgdorferi RevA antigen is a surface-exposed outer membrane protein whose expression is regulated in response to environmental temperature and pH. Infect. Immun. 69:5286-5293.
9. Charon, N. W., and S. F. Goldstein. 2002. Genetics of motility and chemotaxis of a fascinating group of bacteria: the spirochetes. Annu. Rev. Genet. 36:47-73.
10. Charon, N. W., et al. 2009. The flat ribbon configuration of the periplasmic flagella of Borrelia burgdorferi and its relationship to motility and morphology. J. Bacteriol. 191:600-607.
11. Cummings, M. C., et al. 1996. Comparison of methods for the detection of Treponema pallidum in lesions of early syphilis. Sex. Transm. Dis. 23:366-369.
12. Dombrowski, C., et al. 2009. The elastic basis for the shape of Borrelia burgdorferi. Biophys. J. 96:4409-4417.
13. Frank, K. L., S. F. Bundle, M. E. Kresge, C. H. Eggers, and D. S. Samuels. 2003. aadA confers streptomycin resistance in Borrelia burgdorferi. J. Bacteriol. 185:6723-6727.
14. Fraser, C. M., et al. 1997. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390:580-586.
15. Fukuoka, H., T. Wada, S. Kojima, A. Ishijima, and M. Homma. 2009. Sodium-dependent dynamic assembly of membrane complexes in sodiumdriven flagellar motors. Mol. Microbiol. 71:825-835.
16. Ge, Y., and N. W. Charon. 1997. Identification of a large motility operon in Borrelia burgdorferi by semi-random PCR chromosome walking. Gene 189: 195-201.
17. Ge, Y., C. Li, L. Corum, C. A. Slaughter, and N. W. Charon. 1998. Structure and expression of the FlaA periplasmic flagellar protein of Borrelia burgdorferi. J. Bacteriol. 180:2418-2425.
18. 70 promoter. J. Bacteriol. 179:2289-2299.
19. Goldstein, S. F., N. W. Charon, and J. A. Kreiling. 1994. Borrelia burgdorferi swims with a planar waveform similar to that of eukaryotic flagella. Proc. Natl. Acad. Sci. U. S. A. 91:3433-3437.
20. Goldstein, S. F., et al. 2010. The chic motility and chemotaxis of Borrelia burgdorferi, p. 161-181. In D. S. Samuels and J. D. Radolf (ed.), Borrelia: molecular biology, host interaction and pathogenesis. Caister Academic Press, Norfolk, United Kingdom.
21. Harshey, R. M. 2003. Bacterial motility on a surface: many ways to a common goal. Annu. Rev. Microbiol. 57:249-273.
22. Hofmann, K., and W. Stoffel. 1993. TMbase-database of membrane spanning proteins segments. Biol. Chem. Hoppe Seyler 374:166.
23. Hyde, J. A., D. K. Shaw, I. R. Smith, J. P. Trzeciakowski, and J. T. Skare. 2009. The BosR regulatory protein of Borrelia burgdorferi interfaces with the RpoS regulatory pathway and modulates both the oxidative stress response and pathogenic properties of the Lyme disease spirochete. Mol. Microbiol. 74:1344-1355.
24. Izard, J., C. E. Hsieh, R. J. Limberger, C. A. Mannella, and M. Marko. 2008. Native cellular architecture of Treponema denticola revealed by cryo-electron tomography. J. Struct. Biol. 163:10-17.
25. Izard, J., et al. 2009. Cryo-electron tomography elucidates the molecular architecture of Treponema pallidum, the syphilis spirochete. J. Bacteriol. 191:7566-7580.
26. Jenal, U., J. White, and L. Shapiro. 1994. Caulobacter flagellar function, but not assembly, requires FliL, a non-polarly localized membrane protein present in all cell types. J. Mol. Biol. 243:227-244.
27. Jones, C. J., R. M. Macnab, H. Okino, and S. Aizawa. 1990. Stoichiometric analysis of the flagellar hook-(basal-body) complex of Salmonella typhimurium. J. Mol. Biol. 212:377-387.
28. Kanbe, M., S. Shibata, Y. Umino, U. Jenal, and S. I. Aizawa. 2005. Protease susceptibility of the Caulobacter crescentus flagellar hook-basal body: a possible mechanism of flagellar ejection during cell differentiation. Microbiology 151:433-438.
29. Kihara, M., M. Homma, K. Kutsukake, and R. M. Macnab. 1989. Flagellar switch of Salmonella typhimurium: gene sequences and deduced protein sequences. J. Bacteriol. 171:3247-3257.
30. Kimsey, R. B., and A. Spielman. 1990. Motility of Lyme disease spirochetes in fluids as viscous as the extracellular matrix. J. Infect. Dis. 162:1205-1208.
31. Kojima, S., and D. F. Blair. 2004. The bacterial flagellar motor: structure and function of a complex molecular machine. Int. Rev. Cytol. 233:93-134.
32. Kremer, J. R., D. N. Mastronarde, and J. R. McIntosh. 1996. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116:71-76.
33. Kudryashev, M., et al. 2009. Comparative cryo-electron tomography of pathogenic Lyme disease spirochetes. Mol. Microbiol. 71:1415-1434.
34. Kudryashev, M., M. Cyrklaff, R. Wallich, W. Baumeister, and F. Frischknecht. 2010. Distinct in situ structures of the Borrelia flagellar motor. J. Struct. Biol. 169:54-61.
35. Li, C., et al. 2002. Asymmetrical flagellar rotation in Borrelia burgdorferi nonchemotactic mutants. Proc. Natl. Acad. Sci. U. S. A. 99:6169-6174.
36. Li, C., M. Sal, M. Marko, and N. W. Charon. 2010. Differential regulation of the multiple flagellins in spirochetes. J. Bacteriol. 192:2596-2603.
37. Li, C., C. W. Wolgemuth, M. Marko, D. G. Morgan, and N. W. Charon. 2008. Genetic analysis of spirochete flagellin proteins and their involvement in motility, filament assembly, and flagellar morphology. J. Bacteriol. 190:5607-5615.
38. Li, C., H. Xu, K. Zhang, and F. T. Liang. 2010. Inactivation of a putative flagellar motor switch protein FliG1 prevents Borrelia burgdorferi from swimming in highly viscous media and blocks its infectivity. Mol. Microbiol. 75:1563-1576.
39. Li, X., et al. 2007. The Lyme disease agent Borrelia burgdorferi requires BB0690, a Dps homologue, to persist within ticks. Mol. Microbiol. 63:694-710.
40. Liu, J., et al. 2010. Cellular architecture of Treponema pallidum: novel flagellum, periplasmic cone, and cell envelope as revealed by cryo electron tomography. J. Mol. Biol. 403:546-561.
41. Liu, J., et al. 2009. Intact flagellar motor of Borrelia burgdorferi revealed by cryo-electron tomography: evidence for stator ring curvature and rotor/Cring assembly flexion. J. Bacteriol. 191:5026-5036.
42. Macnab, R. M. 2003. How bacteria assemble flagella. Annu. Rev. Microbiol. 57:77-100.
43. Motaleb, M. A., et al. 2000. Borrelia burgdorferi periplasmic flagella have both skeletal and motility functions. Proc. Natl. Acad. Sci. U. S. A. 97:10899-10904.
44. Motaleb, M. A., M. R. Miller, R. G. Bakker, C. Li, and N. W. Charon. 2007. Isolation and characterization of chemotaxis mutants of the Lyme disease spirochete Borrelia burgdorferi using allelic exchange mutagenesis, flow cytometry, and cell tracking. Methods Enzymol. 422:421-437.
45. Motaleb, M. A., et al. 2005. CheX is a phosphorylated CheY phosphatase essential for Borrelia burgdorferi chemotaxis. J. Bacteriol. 187:7963-7969.
46. Motaleb, M. A., M. S. Sal, and N. W. Charon. 2004. The decrease in FlaA observed in a flaB mutant of Borrelia burgdorferi occurs posttranscriptionally. J. Bacteriol. 186:3703-3711.
47. Murphy, G. E., J. R. Leadbetter, and G. J. Jensen. 2006. In situ structure of the complete Treponema primitia flagellar motor. Nature 442:1062-1064.
48. Paul, R., et al. 2004. Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev. 18:715-727.
49. Rajasekhar Karna, S. L., et al. 2011. CsrABb modulates levels of lipoproteins and key regulators of gene expression (RpoS and BosR) critical for pathogenic mechanisms of Borrelia burgdorferi. Infect. Immun. 79:732-744.
50. Rosa, P. A., K. Tilly, and P. E. Stewart. 2005. The burgeoning molecular genetics of the Lyme disease spirochaete. Nat. Rev. Microbiol. 3:129-143.
51. Sal, M. S., et al. 2008. Borrelia burgdorferi uniquely regulates its motility genes and has an intricate flagellar hook-basal body structure. J. Bacteriol. 190:1912-1921.
52. Samuels, D. S., K. E. Mach, and C. F. Garon. 1994. Genetic transformation of the Lyme disease agent Borrelia burgdorferi with coumarin-resistant gyrB. J. Bacteriol. 176:6045-6049.
53. Sanjuan, E., M. D. Esteve-Gassent, M. Maruskova, and J. Seshu. 2009. Overexpression of CsrA (BB0184) alters the morphology and antigen profiles of Borrelia burgdorferi. Infect. Immun. 77:5149-5162.
54. Steere, A. C., J. Coburn, and L. Glickstein. 2004. The emergence of Lyme disease. J. Clin. Invest. 113:1093-1101.
55. Suaste-Olmos, F., et al. 2010. The flagellar protein FliL is essential for swimming in Rhodobacter sphaeroides. J. Bacteriol. 192:6230-6239.
56. Sultan, S. Z., J. E. Pitzer, M. R. Miller, and M. A. Motaleb. 2010. Analysis of a Borrelia burgdorferi phosphodiesterase demonstrates a role for cyclic-diguanosine monophosphate in motility and virulence. Mol. Microbiol. 77: 128-142.
57. Wang, Q., and R. M. Harshey. 2009. Rcs signalling-activated transcription of rcsA induces strong anti-sense transcription of upstream fliPQR flagellar genes from a weak intergenic promoter: regulatory roles for the anti-sense transcript in virulence and motility. Mol. Microbiol. 74:71-84.
58. Zhang, X., X. Yang, M. Kumar, and U. Pal. 2009. BB0323 function is essential for Borrelia burgdorferi virulence and persistence through tick-rodent transmission cycle. J. Infect. Dis. 200:1318-1330.