Differential regulation of the multiple flagellins in spirochetes

Journal of Bacteriology

Volumn 192, Issue 10, 2010, Pages 2596-2603

  Li, Chunhao ^a,b   Sal, Melanie ^b   Marko, Michael ^c   Charon, Nyles W ^b  

^a UNIVERSITY AT BUFFALO   (United States)

^b WEST VIRGINIA UNIVERSITY   (United States)

^c WADSWORTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLA A PROTEIN; FLA B1 PROTEIN; FLA B2 PROTEIN; FLA B3 PROTEIN; FLAGELLIN; SIGMA FACTOR; SIGMA FACTOR 28; SIGMA FACTOR 70; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BRACHYSPIRA HYODYSENTERIAE; CELL MOTILITY; CONTROLLED STUDY; CORRELATION FUNCTION; FLAGELLUM; GENE MUTATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; SPIROCHETE; TRANSCRIPTION REGULATION;

BACTERIAL PROTEINS; BLOTTING, WESTERN; BRACHYSPIRA HYODYSENTERIAE; ELECTROPHORESIS; FLAGELLA; FLAGELLIN; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPIROCHAETALES;

BACTERIA (MICROORGANISMS); BRACHYSPIRA HYODYSENTERIAE; SPIROCHAETALES;

EID: 77952061602     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01502-09     Document Type: Article

References (65)

1. Aldridge, P., and K. T. Hughes. 2002. Regulation of flagellar assembly. Curr. Opin. Microbiol. 5:160-165.
2. Bellgard, M. I., P. Wanchanthuek, T. La, K. Ryan, P. Moolhuijzen, Z. Albertyn, B. Shaban, Y. Motro, D. S. Dunn, D. Schibeci, A. Hunter, R. Barrero, N. D. Phillips, and D. J. Hampson. 2009. Genome sequence of the pathogenic intestinal spirochete Brachyspira hyodysenteriae reveals adaptations to its lifestyle in the porcine large intestine. PLoS One 4:e4641.
3. Blanco, D. R., J. D. Radolf, M. A. Lovett, and J. N. Miller. 1986. The antigenic interrelationship between the endoflagella of Treponema phagedenis biotype Reiter and Treponema pallidum, Nichols strain. I. Treponemicidal activity of cross-reactive endoflagellar antibodies against T. pallidum. J. Immunol. 137:2973-2979. (Pubitemid 17177809)
4. Brahamsha, B., and E. P. Greenberg. 1989. Cloning and sequence analysis of flaA, a gene encoding a Spirochaeta aurantia flagellar filament surface antigen. J. Bacteriol. 171:1692-1697.
5. Byrne, S. J., S. G. Dashper, I. B. Darby, G. G. Adams, B. Hoffmann, and E. C. Reynolds. 2009. Progression of chronic periodontitis can be predicted by the levels of Porphyromonas gingivalis and Treponema denticola in subgingival plaque. Oral Microbiol. Immunol. 24:469-477.
6. 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.
7. Charon, N. W., S. F. Goldstein, S. M. Block, K. Curci, J. D. Ruby, J. A. Kreiling, and R. J. Limberger. 1992. Morphology and dynamics of protruding spirochete periplasmic flagella. J. Bacteriol. 174:832-840.
8. Charon, N. W., S. F. Goldstein, M. Marko, C. Hsieh, L. L. Gebhardt, M. A. Motaleb, C. W. Wolgemuth, R. J. Limberger, and N. Rowe. 2009. The flat-ribbon configuration of the periplasmic flagella of Borrelia burgdorferi and its relationship to motility and morphology. J. Bacteriol. 191:600-607.
9. Chesnokova, O., J. B. Coutinho, I. H. Khan, M. S. Mikhail, and C. I. Kado. 1997. Characterization of flagella genes of Agrobacterium tumefaciens, and the effect of a bald strain on virulence. Mol. Microbiol. 23:579-590.
10. Chevance, F. F., and K. T. Hughes. 2008. Coordinating assembly of a bacterial macromolecular machine. Nat. Rev. Microbiol. 6:455-465.
11. Colland, F., J. C. Rain, P. Gounon, A. Labigne, P. Legrain, and R. H. De. 2001. Identification of the Helicobacter pylori anti-sigma28 factor. Mol. Microbiol. 41:477-487.
12. Daskalakis, D. 2008. Syphilis: continuing public health and diagnostic challenges. Curr. HIV/AIDS Rep. 5:72-77.
13. Deakin, W. J., V. E. Parker, E. L. Wright, K. J. Ashcroft, G. J. Loake, and C. H. Shaw. 1999. Agrobacterium tumefaciens possesses a fourth flagellin gene located in a large gene cluster concerned with flagellar structure, assembly and motility. Microbiol. 145:1397-1407.
14. Driks, A., R. Bryan, L. Shapiro, and D. J. DeRosier. 1989. The organization of the Caulobacter crescentus flagellar filament. J. Mol. Biol. 206:627-636.
15. Fraser, C. M., S. Casjens, W. M. Huang, G. G. Sutton, R. Clayton, R. Lathigra, O. White, K. A. Ketchum, R. Dodson, E. K. Hickey, M. Gwinn, B. Dougherty, J. F. Tomb, R. D. Fleischmann, D. Richardson, J. Peterson, A. R. Kerlavage, J. Quackenbush, S. Salzberg, M. Hanson, R. van Vugt, N. Palmer, M. D. Adams, and J. Gocayne. 1997. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390:580-586.
16. Fraser, C. M., S. J. Norris, C. M. Weinstock, O. White, G. G. Sutton, R. Dodson, M. Gwinn, E. K. Hickey, R. Clayton, K. A. Ketchum, E. Sodergren, J. M. Hardham, M. P. McLeod, S. Salzberg, J. Peterson, H. Khalak, D. Richardson, J. K. Howell, M. Chidambaram, T. Utterback, L. McDonald, P. Artiach, C. Bowman, and M. D. Cotton. 1998. Complete genome sequence of Treponema pallidum, the syphilis spirochete. Science 281:375-388.
17. Gabe, J. D., R.-J. Chang, R. Slomiany, W. H. Andrews, and M. T. McCaman. 1995. Isolation of extracytoplasmic proteins from Serpulina hyodysenteriae B204 and molecular cloning of the flaB1 gene encoding a 38-kilodalton flagellar protein. Infect. Immun. 63:142-148.
18. Ge, Y., and N. W. Charon. 1997. An unexpected flaA homolog is present and expressed in Borrelia burgdorferi. J. Bacteriol. 179:552-556.
19. 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.
20. 70 promoter. J. Bacteriol. 179:2289-2299.
21. 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.
22. Hendrixson, D. R., and V. J. DiRita. 2003. Transcription of sigma54-dependent but not sigma28-dependent flagellar genes in Campylobacter jejuni is associated with formation of the flagellar secretory apparatus. Mol. Microbiol. 50:687-702.
23. Humphrey, S. B., T. B. Stanton, N. S. Jensen, and R. L. Zuerner. 1997. Purification and characterization of VSH-1, a generalized transducing bacteriophage of Serpulina hyodysenteriae. J. Bacteriol. 179:323-329.
24. Iida, Y., L. Hobley, C. Lambert, A. K. Fenton, R. E. Sockett, and S. Aizawa. 2009. Roles of multiple flagellins in flagellar formation and flagellar growth post bdelloplast lysis in Bdellovibrio bacteriovorus. J. Mol. Biol. 394:1011-1021.
25. Irikura, V. M., M. Kihara, S. Yamaguchi, H. Sockett, and R. M. Macnab. 1993. Salmonella typhimurium fliG and fliN mutations causing defects in assembly, rotation, and switching of the flagellar motor. J. Bacteriol. 175: 802-810.
26. Isaacs, R. D., J. H. Hanke, L. M. Guzman-Verduzco, G. Newport, N. Agabian, M. V. Norgard, S. A. Lukehart, and J. D. Radolf. 1989. Molecular cloning and DNA sequence analysis of the 37-kilodalton endoflagellar sheath protein gene of Treponema pallidum. Infect. Immun. 57:3403-3411. (Pubitemid 19259869)
27. 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.
28. Izard, J., C. Renken, C. E. Hsieh, D. C. Desrosiers, S. Dunham-Ems, V. C. La, L. L. Gebhardt, R. J. Limberger, D. L. Cox, M. Marko, and J. D. Radolf. 2009. Cryo-electron tomography elucidates the molecular architecture of Treponema pallidum, the syphilis spirochete. J. Bacteriol. 191:7566-7580.
29. Kihara, M., G. U. Miller, and R. M. Macnab. 2000. Deletion analysis of the flagellar switch protein FliG of Salmonella. J. Bacteriol. 182:3022-3028. (Pubitemid 30326914)
30. Koopman, M. B., E. Baats, O. S. de Leeuw, B. A. Van der Zeijst, and J. G. Kusters. 1993. Molecular analysis of a flagellar core protein gene of Serpulina (Treponema) hyodysenteriae. J. Gen. Microbiol. 139:1701-1706.
31. Koopman, M. B., E. Baats, C. J. van Vorstenbosch, B. A. Van der Zeijst, and J. G. Kusters. 1992. The periplasmic flagella of Serpulina (Treponema) hyodysenteriae are composed of two sheath proteins and three core proteins. J. Gen. Microbiol. 138:2697-2706.
32. Koopman, M. B., O. S. de Leeuw, B. M. Van der Zeijst, and J. G. Kusters. 1992. Cloning and DNA sequence analysis of a Serpulina (Treponema) hyodysenteriae gene encoding a periplasmic flagellar sheath protein. Infect. Immun. 60:2920-2925.
33. Levett, P. N. 2001. Leptospirosis. Clin. Microbiol. Rev. 14:296-326.
34. Li, C., R. G. Bakker, M. A. Motaleb, M. L. Sartakova, F. C. Cabello, and N. W. Charon. 2002. Asymmetrical flagellar rotation in Borrelia burgdorferi nonchemotactic mutants. Proc. Natl. Acad. Sci. U. S. A. 99:6169-6174.
35. Li, C., L. Corum, D. Morgan, E. L. Rosey, T. B. Stanton, and N. W. Charon. 2000. The spirochete FlaA periplasmic flagellar sheath protein impacts flagellar helicity. J. Bacteriol. 182:6698-6706. (Pubitemid 32249253)
36. Li, C., A. Motaleb, M. Sal, S. F. Goldstein, and N. W. Charon. 2000. Spirochete periplasmic flagella and motility. J. Mol. Microbiol. Biotechnol. 2:345-354.
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. Limberger, R. J. 2004. The periplasmic flagellum of spirochetes. J. Mol. Microbiol. Biotechnol. 7:30-40.
39. Liu, J., T. Lin, D. J. Botkin, E. McCrum, H. Winkler, and S. J. Norris. 2009. Intact flagellar motor of Borrelia burgdorferi revealed by cryo-electron tomography: evidence for stator ring curvature and rotor/C-ring assembly flexion. J. Bacteriol. 191:5026-5036.
40. Lloyd, S. A., H. Tang, X. Wang, S. Billings, and D. F. Blair. 1996. Torque generation in the flagellar motor of Escherichia coli: Evidence of a direct role for FliG but not for FliM or FliN. J. Bacteriol. 178:223-231.
41. Lloyd, S. A., F. G. Whitby, D. F. Blair, and C. P. Hill. 1999. Structure of the C-terminal domain of FliG, a component of the rotor in the bacterial flagellar motor. Nature 400:472-475.
42. Loh, J. T., M. H. Forsyth, and T. L. Cover. 2004. Growth phase regulation of flaA expression in Helicobacter pylori is luxS dependent. Infect. Immun. 72:5506-5510.
43. McCarter, L. L. 2001. Polar flagellar motility of the Vibrionaceae. Microbiol. Mol. Biol. Rev. 65:445-462.
44. Merrell, D. S., M. L. Goodrich, G. Otto, L. S. Tompkins, and S. Falkow. 2003. pH-regulated gene expression of the gastric pathogen Helicobacter pylori. Infect. Immun. 71:3529-3539.
45. Mikosza, A. S., and D. J. Hampson. 2001. Human intestinal spirochetosis: Brachyspira aalborgi and/or Brachyspira pilosicoli? Anim. Health Res. Rev. 2:101-110.
46. Motaleb, M. A., L. Corum, J. L. Bono, A. F. Elias, P. Rosa, D. S. Samuels, and N. W. Charon. 2000. Borrelia burgdorferi periplasmic flagella have both skeletal and motility functions. Proc. Natl. Acad. Sci. U. S. A. 97:10899-10904.
47. 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.
48. 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.
49. Norris, S. J., N. W. Charon, R. G. Cook, M. D. Fuentes, and R. J. Limberger. 1988. Antigenic relatedness and N-terminal sequence homology define two classes of major periplasmic flagellar proteins of Treponema pallidum subsp. pallidum and Treponema phagedenis. J. Bacteriol. 170:4072-4082.
50. Norris, S. J., and Treponema pallidum polypeptide research group. 1993. Polypeptides of Treponema pallidum: progress toward understanding their structural, functional, and immunologic roles. Microbiol. Rev. 57:750-779.
51. Pleier, E., and R. Schmitt. 1991. Expression of two Rhizobium meliloti flagellin genes and their contribution to the complex filament structure. J. Bacteriol. 173:2077-2085.
52. Ren, S. X., G. Fu, X. G. Jiang, R. Zeng, Y. G. Miao, H. Xu, Y. X. Zhang, H. Xiong, G. Lu, L. F. Lu, H. Q. Jiang, J. Jia, Y. F. Tu, J. X. Jiang, W. Y. Gu, Y. Q. Zhang, Z. Cai, H. H. Sheng, H. F. Yin, Y. Zhang, G. F. Zhu, M. Wan, H. L. Huang, Z. Qian, S. Y. Wang, W. Ma, Z. J. Yao, Y. Shen, B. Q. Qiang, Q. C. Xia, X. K. Guo, A. Danchin, I. Saint Girons, R. L. Somerville, Y. M. Wen, M. H. Shi, Z. Chen, J. G. Xu, and G. P. Zhao. 2003. Unique physiological and pathogenic features of Leptospira interrogans revealed by wholegenome sequencing. Nature 422:888-893.
53. Rosey, E. L., M. J. Kennedy, D. K. Petrella, R. G. Ulrich, and R. J. Yancey, Jr. 1995. Inactivation of Serpulina hyodysenteriae flaA1 and flaB1 periplasmic flagellar genes by electroporation-mediated allelic exchange. J. Bacteriol. 177:5959-5970.
54. Rust, M., S. Borchert, E. Niehus, S. A. Kuehne, E. Gripp, A. Bajceta, J. L. McMurry, S. Suerbaum, K. T. Hughes, and C. Josenhans. 2009. The Helicobacter pylori anti-sigma factor FlgM is predominantly cytoplasmic and cooperates with the flagellar basal body protein FlhA. J. Bacteriol. 191:4824-4834.
55. Sal, M. S., C. Li, M. A. Motalab, S. Shibata, S. Aizawa, and N. W. Charon. 2008. Borrelia burgdorferi uniquely regulates its motility genes and has an intricate flagellar hook-basal body structure. J. Bacteriol. 190:1912-1921.
56. Seshadri, R., G. S. Myers, H. Tettelin, J. A. Eisen, J. F. Heidelberg, R. J. Dodson, T. M. Davidsen, R. T. DeBoy, D. E. Fouts, D. H. Haft, J. Selengut, Q. Ren, L. M. Brinkac, R. Madupu, J. Kolonay, S. A. Durkin, S. C. Daugherty, J. Shetty, A. Shvartsbeyn, E. Gebregeorgis, K. Geer, G. Tsegaye, J. Malek, B. Ayodeji, S. Shatsman, M. P. McLeod, D. Smajs, J. K. Howell, S. Pal, A. Amin, P. Vashisth, T. Z. McNeill, Q. Xiang, E. Sodergren, E. Baca, G. M. Weinstock, S. J. Norris, C. M. Fraser, and I. T. Paulsen. 2004. Comparison of the genome of the oral pathogen Treponema denticola with other spirochete genomes. Proc. Natl. Acad. Sci. U. S. A. 101:5646-5651.
57. Slivienski-Gebhardt, L. L., J. Izard, W. A. Samsonoff, and R. J. Limberger. 2004. Development of a novel chloramphenicol resistance expression plasmid used for genetic complementation of a fliG deletion mutant in Treponema denticola. Infect. Immun. 72:5493-5497.
58. Stanton, T. B., E. L. Rosey, M. J. Kennedy, N. S. Jensen, and B. T. Bosworth. 1999. Isolation, oxygen sensitivity, and virulence of NADH oxidase mutants of the anaerobic spirochete Brachyspira (Serpulina) hyodysenteriae, etiologic agent of swine dysentery. Appl. Environ. Microbiol. 65:5028-5034.
59. Steere, A. C., J. Coburn, and L. Glickstein. 2004. The emergence of Lyme disease. J. Clin. Invest. 113:1093-1101.
60. Suerbaum, S. 1995. The complex flagella of gastric Helicobacter species. Trends Microbiol. 3:168-170.
61. Thompson, L. J., D. S. Merrell, B. A. Neilan, H. Mitchell, A. Lee, and S. Falkow. 2003. Gene expression profiling of Helicobacter pylori reveals a growth-phase-dependent switch in virulence gene expression. Infect. Immun. 71:2643-2655.
62. Wang, L. Y., L. Brown, M. Elliott, and T. Elliott. 1997. Regulation of heme biosynthesis in Salmonella typhimurium: activity of glutamyl-tRNA reductase (HemA) is greatly elevated during heme limitation by a mechanism which increases abundance of the protein. J. Bacteriol. 179:2907-2914.
63. Wassenaar, T. M., N. M. Bleumink-Pluym, and B. A. Van der Zeijst. 1991. Inactivation of Campylobacter jejuni flagellin genes by homologous recombination demonstrates that flaA but not flaB is required for invasion. EMBO J. 10:2055-2061.
64. Wilson, D. R., and T. J. Beveridge. 1993. Bacterial flagellar filaments and their component flagellins. Can. J. Microbiol. 39:451-472.
65. Yang, Y., and C. Li. 2009. Transcription and genetic analyses of a putative N-acetylmuramyl-L-alanine amidase in Borrelia burgdorferi. FEMS Microbiol. Lett. 290:164-173.