Molecular characterization of the flagellar hook in Bacillus subtilis

Journal of Bacteriology

Volumn 194, Issue 17, 2012, Pages 4619-4629

  Courtney, Colleen R ^a,b   Cozy, Loralyn M ^a,c   Kearns, Daniel B ^a  

^a INDIANA UNIVERSITY   (United States)

^b NEW YORK UNIVERSITY   (United States)

^c UNIVERSITY OF HAWAII   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CYSTEINE; FLGD PROTEIN; FLGE PROTEIN; FLHO PROTEIN; FLHP PROTEIN; FLIK PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; FLUORESCENCE; GENE EXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; FLAGELLA; GENE EXPRESSION REGULATION, BACTERIAL; PROMOTER REGIONS, GENETIC; SIGMA FACTOR;

BACILLUS SUBTILIS; POSIBACTERIA; SALMONELLA ENTERICA;

EID: 84866315642     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00444-12     Document Type: Article

References (74)

1. Aizawa S-I, Dean GE, Jones CJ, Macnab RM, Yamaguchi S. 1985. Purification and characterization of the flagellar hook-basal body complex of Salmonella typhimurium. J. Bacteriol. 161:836-849.
2. Aizawa S-I Zhulin IB, Márquez-Magaña L, Ordal GW. 2002. Chemotaxis and motility in Bacillus subtilis, p 437-452. In Sonenshein AL, Hoch JA, Losick R (ed), Bacillus subtilis and its closest relatives: from genes to cells. ASM Press, Washington, DC.
3. Albertini AM, Caramori T, Crabb WD, Scoffone F, Galizzi A. 1991. The flaA locus of Bacillus subtilis is part of a large operon coding for flagellar structures, motility functions, and an ATPase-like polypeptide. J. Bacteriol. 173:3573-3579.
4. Antoniewski C, Savelli B, Stragier P. 1990. The spoIIJ gene, which regulates early developmental steps in Bacillus subtilis, belongs to a class of environmentally responsive genes. J. Bacteriol. 172:86-93.
5. Barill D, Caramori T, Galizzi A. 1994. Coupling of flagellin gene transcription to flagellar assembly in Bacillus subtilis. J. Bacteriol. 176:4558-4564.
6. Berg HC, Anderson RA. 1973. Bacteria swim by rotating their flagellar filaments. Nature 245:380-382.
7. Bertero MG, Gonzales B, Tarricone C, Ceciliani F, Galizzi A. 1999. Overproduction and characterization of the Bacillus subtilis anti-sigma factor FlgM. J. Biol. Chem. 274:12103-12107.
8. Blair KM, Turner L, Winkelman JT, Berg HC, Kearns DB. 2008. A molecular clutch disables flagella in the Bacillus subtilis biofilm. Science 320:1636-1638.
9. Bonifield HR, Yamaguchi S, Hughes KT. 2000. The flagellar hook protein, FlgE, of Salmonella enterica serovar Typhimurium is posttranscriptionally regulated in response to the state of flagellar assembly. J. Bacteriol. 182:4044-4050.
10. D-dependent gene expression in Bacillus subtilis. J. Bacteriol. 178: 3113-3118.
11. Carpenter PB, Zuberi AR, Ordal GW. 1993. Bacillus subtilis flagellar proteins FliP, FliQ, FliR and FlhB are related to Shigella flexneri virulence factors. Gene 137:243-245.
12. D-dependent autolysins in Bacillus subtilis population heterogeneity. J. Bacteriol. 191:5775-5784.
13. Chevance FFV, et al. 2007. The mechanism of outer membrane penetration by the eubacterial flagellum and implications for spirochete evolution. Genes Dev. 21:2326-2335.
14. Cozy LM, Kearns DB. 2010. Gene position in a long operon governs motility development in Bacillus subtilis. Mol. Microbiol.76:273-285.
15. DePamphilis ML, Adler J. 1971. Fine structure and isolation of the hookbasal body complex of flagella from Escherichia coli and Bacillus subtilis. J. Bacteriol. 105:384-395.
16. Erhardt M, Namba K, Hughes KT. 2010. Bacterial nanomachines: the flagellum and type III injectisome. Cold Spring Harbor Perspect. Biol. 2:a000299. doi:10.1101/cshperspect.a000299.
17. Erhardt M, Singer HM, Wee DH, Keener JP, Hughes KT. 2011. An infrequent molecular ruler controls flagellar hook length in Salmonella enterica. EMBO J. 30:2948-2961.
18. Estacio W, Santa Anna-Arriola S, Adedipe M, Márquez-Magaña LM. 1998. Dual promoters are responsible for transcription initiation of the fla/che operon in Bacillus subtilis. J. Bacteriol. 180:3548-3555.
19. Ferris HU, et al. 2005. FlhB regulates ordered export of flagellar components via autocleavage mechanism. J. Biol. Chem. 280:41236-41242.
20. Fraser GM, et al. 2003. Substrate specificity of the type III flagellar protein export in Salmonella is controlled by subdomain interactions in FlhB. Mol. Microbiol. 48:1043-1057.
21. D activity, and its absence restores motility to a sinR mutant. J. Bacteriol. 178:7010-7013.
22. Fujii T, Kato T, Namba K. 2009. Specific arrangement of the α-helical
23. Gillen KL, Hughes KT. 1991. Molecular characterization of flgM, a gene encoding a negative regulator of flagellin synthesis of Salmonella typhimurium. J. Bacteriol. 173:6453-6459.
24. Guérout-Fleury AM, Shazand K, Frandsen N, Stragier P. 1995. Antibiotic-resistance cassettes for Bacillus subtilis. Gene 167:335-336.
25. Guérout-Fleury AM, Frandsen N, Stragier P. 1996. Plasmids for ectopic integration in. Bacillus subtilis. Gene 180:57-61.
26. Helmann JD, Moran Jr, CP. 2002. RNA polymerase and sigma factors, p 289-312. In Sonenshein AL, Hoch JA, Losick R (ed), Bacillus subtilis and its closest relatives: from genes to cells. ASM Press, Washington, DC.
27. Hirano T, Yamaguchi S, Oosawa K, Aizawa S-I. 1994. Roles of FliK and FlhB in determination of flagellar hook length in Salmonella typhimurium. J. Bacteriol. 176:5439-5449.
28. Homma M, Kutsukake K, Hasebe M, Iino T, Macnab RM. 1990. FlgB, FlgC, FlgF, and FlgG, a family of structurally related proteins in the flagellar basal body of Salmonella typhimurium. J. Mol. Biol. 211:465-477.
29. Hsueh Y-H, et al. 2011. DegU-phosphate activates expression of the anti-sigma factor FlgM in Bacillus subtilis. Mol. Microbiol. 81:1092-1108. 30.
30. Hughes KT, Gillen KL, Semon MJ, Karlinsey JE. 1993. Sensing structural intermediates in bacterial flagellar assembly by export of a negative regulator. Science 262:1277-1280.
31. Iino T. 1969. Polarity of flagellar growth in Salmonella. J. Gen. Microbiol. 56:227-239.
32. Iino T, et al. 1988. New unified nomenclature for the flagellar genes of Escherichia coli and Salmonella typhimurium. Microbiol. Rev. 52:533-535.
33. Iyoda S, Kutsukake K. 1995. Molecular dissection of the flagellum specific anti-sigma factor, FlgM, of Salmonella typhimurium. Mol. Gen. Genet. 249:417-424.
34. Journet L, Agrain C, Broz P, Cornelis GR. 2003. The needle length of bacterial injectisomes is determined by a molecular ruler. Science 302: 1757-1760.
35. Kagawa H, Owaribe K, Asakura S, Takahashi N. 1976. Flagellar hook protein from Salmonella SJ25. J. Bacteriol. 125:68-73.
36. Karlinsey JE, et al. 2000. Completion of the hook-basal body complex of the Salmonella typhimurium flagellum is coupled to FlgM secretion and fliC transcription. Mol. Microbiol. 37:1220-1231.
37. Kearns DB, Losick R. 2003. Swarming motility in undomesticated Bacillus subtilis. Mol. Microbiol. 49:581-590.
38. Komeda Y, Silverman M, Simon MI. 1978. Identification of the structural gene for the hook subunit protein of Escherichia coli flagella. J. Bacteriol. 133:364-371.
39. Kubori T, et al. 1997. Purification and characterization of the flagellar hook-basal body complex of Bacillus subtilis. Mol. Microbiol. 24:399-410.
40. Kutsukake K, Iino T, Komeda Y, Yamaguchi S. 1980. Functional homology of flagenes between Salmonella typhimurium and Escherichia coli. Mol. Gen. Genet. 178:59-67.
41. Kutsukake K. 1994. Excretion of the anti-sigma factor through a flagellar substructure couples flagellar gene expression with flagellar assembly in Salmonella typhimurium. Mol. Gen. Genet. 243:605-612.
42. Lee HJ, Hughes KT. 2006. Posttranscriptional control of the Salmonella enterica flagellar hook protein FlgE. J. Bacteriol. 188:3308-3316.
43. Liu R, Ochman H. 2007. Stepwise formation of the bacterial flagellar system. Proc. Natl. Acad. Sci. U. S. A. 104:7116-7121.
44. Macnab RM. 1992. Genetics and biogenesis of bacterial flagella. Annu. Rev. Genet. 26:131-158.
45. Macnab RM. 2003. How bacteria assemble flagella. Annu. Rev. Microbiol. 57:77-100.
46. D-. Microbiology 145: 57-65.
47. Michiels T, Wattiau P, Brasseur R, Ruysschaert Cornelis J-MG. 1990. Secretion of Yop proteins by yersiniae. Infect. Immun. 58:2840-2849.
48. Minamino T, Macnab R. 1999. Components of the Salmonella flagellar export apparatus and classification of export substrates. J. Bacteriol. 181: 1388-1394.
49. Minamino T, González-Pedrajo B, Yamaguchi K, Aizawa SI, Macnab RM. 1999. FliK, the protein responsible for flagellar hook length control in Salmonella, is exported during hook assembly. Mol. Microbiol. 34:295-304.
50. Minamino T, Yamaguchi S, Macnab RM. 2000. Interaction between FliE and FlgB, a proximal rod component of the flagellar basal body of Salmonella. J. Bacteriol. 182:3029-3036.
51. Minamino T, Ferris HU, Moriya N, Kihara M, Namba K. 2006. Two parts of the T3S4 domain of the hook-length control protein FliK are essential for the substrate specificity switching of the flagellar type III export apparatus. J. Mol. Biol. 362:1148-1158.
52. Minamino T, Moriya N, Hirano T, Hughes KT, Namba K. 2009. Interaction of FliK with the bacterial flagellar hook is required for efficient export specificity switching. Mol. Microbiol. 74:239-251.
53. 28 form of RNA polymerase. J. Bacteriol. 171:3095-3101.
54. D-dependent operon of Bacillus subtilis. J. Bacteriol. 176:4492-4500.
55. Moriya N, Minamino T, Hughes KT, Macnab RM, Namba K. 2006. The type III flagellar export specificity switch is dependent on FliK ruler and a molecular clock. J. Mol. Biol. 359:466-477.
56. Moriya N, Minamino T, Imada K, Namba K. 2011. Genetic analysis of the bacterial hook-capping protein FlgD responsible for hook assembly. Microbiology 157:1354-1362.
57. Mukherjee S, et al. 2011. CsrA-FliW interaction governs flagellin homeostasis and a checkpoint on flagellar morphogenesis in Bacillus subtilis. Mol. Microbiol. 82:447-461.
58. F Mol. Microbiol. 6:3149-3157.
59. Ohnishi K, Ohto Y, Aizawa Macnab S-IRM, Iino T. 1994. FlgD is a scaffolding protein needed for flagellar hook assembly in Salmonella typhimurium. J. Bacteriol. 176:2272-2281.
60. Ordal GW, Márquez-Magaña L, Chamberlin MJ. 1993. Motility and chemotaxis, p 765-784. In Sonenshein AL, Hoch JA, Losick R (ed), Bacillus subtilis and other Gram-positive bacteria: biochemistry, physiology, and molecular genetics. American Society for Microbiology, Washington, DC.
61. Pallen MJ, Penn CW, Chaudhuri RR. 2005. Bacterial flagellar diversity in the post-genomic era. Trends Microbiol. 13:143-149.
62. Patrick JE, Kearns DB. 2008. MinJ (YvjD) is a topological determinant of cell division in Bacillus subtilis. Mol. Microbiol. 70:1166-1179.
63. Patterson-Delafield J, Martinez JR, Stocker BAD, Yamaguchi S. 1973. A new fla gene in Salmonella typhimurium-flaR--and its mutant phenotype-superhooks. Arch. Microbiol. 90:107-120.
64. Samatey FA, et al. 2004. Structure of the bacterial flagellar hook and implication for the molecular universal joint mechanism. Nature 431: 1062-1068.
65. Shibata S, et al. 2007. FliK regulates flagellar hook length as an internal ruler. Mol. Microbiol. 64:1404-1415.
66. Silverman MR, Simon MI. 1972. Flagellar assembly mutants in Escherichia coli. J. Bacteriol. 112:986-993.
67. Suzuki T, Iino T. 1981. Role of the flaR gene in flagellar hook formation in Salmonella spp. J. Bacteriol. 148:973-979.
68. Turner L, Zhang R, Darnton NC, Berg HC. 2010. Visualization of flagella during bacterial swarming. J. Bacteriol. 192:3259-3267.
69. Wach A. 1996. PCR-synthesis of marker cassettes with long flanking homology regions for gene disruptions in S. cereviseae. Yeast 12:259-295.
70. West JT, Estacio W, Márquez-Magaña L. 2000. Relative roles of the fla/che PA,PD-3, and PsigD promoters in regulating motility and sigD expression in Bacillus subtilis. J. Bacteriol. 182:4841-4848.
71. Williams AW, Yamaguchi S, Togashi F, Aizawa SI, Kawagishi I, Macnab RM. 1996. Mutations in fliK and flhB affecting flagellar hook and filament assembly in Salmonella typhimurium. J. Bacteriol. 178: 2960-2970.
72. Yasbin RE, Young FE. 1974. Transduction in Bacillus subtilis by bacteriophage SPP1. J. Virol. 14:1343-1348.
73. Yonekura K, Maki-Yonekura S, Namba K. 2003. Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424:643-650.
74. Zuberi AR, Ying C, Bischoff DS, Ordal GW. 1991. Gene-protein relationships in the flagellar hook-basal body complex of Bacillus subtilis: sequences of the flgB, flgC, flgG, fliE, and fliF genes. Gene 101:23-31.