Building a flagellum outside the bacterial cell

Trends in Microbiology

Volumn 22, Issue 10, 2014, Pages 566-572

  Evans, Lewis D B ^a   Hughes, Colin ^a   Fraser, Gillian M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Bacterial flagellum; Cell motility; Chain mechanism; Protein export; Rotary nanomotor; Type III secretion system

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN;

AMINO TERMINAL SEQUENCE; BACTERIAL CELL; BACTERIAL FLAGELLUM; BACTERIAL GROWTH; BIOGENESIS; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CELL MEMBRANE; CELL SURFACE; CELL TRANSPORT; CELLULAR DISTRIBUTION; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; REVIEW; TYPE III SECRETION SYSTEM; BACTERIUM; FLAGELLUM; METABOLISM; PROTEIN TRANSPORT;

BACTERIA; BACTERIAL PROTEINS; CELL MEMBRANE; FLAGELLA; PROTEIN TRANSPORT;

EID: 84908545891     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2014.05.009     Document Type: Review

References (72)

1. Snyder L.A.S., et al. Bacterial flagellar diversity and evolution: seek simplicity and distrust it?. Trends Microbiol. 2009, 17:1-5.
2. Abby S.S., Rocha E.P.C. The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems. PLoS Genet. 2012, 8:e1002983.
3. Berg H.C. The rotary motor of bacterial flagella. Annu. Rev. Biochem. 2003, 72:19-54.
4. Roberts M.A.J., et al. Adaptation and control circuits in bacterial chemotaxis. Biochem. Soc. Trans. 2010, 38:1265-1269.
5. Sowa Y., Berry R.M. The bacterial flagellar motor. Single Mol. Biol. 2009, 105-142.
6. Tipping M.J., et al. Load-dependent assembly of the bacterial flagellar motor. Mbio 2013, 4:e00551-e613.
7. Tipping M.J., et al. Quantification of flagellar motor stator dynamics through in vivo proton-motive force control. Mol. Microbiol. 2013, 87:338-347.
8. Che Y.S., et al. Load-sensitive coupling of proton translocation and torque generation in the bacterial flagellar motor. Mol. Microbiol. 2014, 91:175-184.
9. Lele P.P., et al. Dynamics of mechanosensing in the bacterial flagellar motor. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:11839-11844.
10. Suzuki H., et al. Structure of the rotor of the bacterial flagellar motor revealed by electron cryomicroscopy and single-particle image analysis. J. Mol. Biol. 2004, 337:105-113.
11. Chevance F.F.V., et al. The mechanism of outer membrane penetration by the eubacterial flagellum and implications for spirochete evolution. Gene Dev. 2007, 21:2326-2335.
12. Samatey F.A., et al. Structure of the bacterial flagellar hook and implication for the molecular universal joint mechanism. Nature 2004, 431:1062-1068.
13. Samatey F.A., et al. Structure of the bacterial flagellar protofilament and implications for a switch for supercoiling. Nature 2001, 410:331-337.
14. Trachtenberg S., et al. Bacterial flagellar microhydrodynamics: laminar flow over complex flagellar filaments, analog Archimedean screws and cylinders, and its perturbations. Biophys. J. 2003, 85:1345-1357.
15. Chevance F.F.V., Hughes K.T. Coordinating assembly of a bacterial macromolecular machine. Nat. Rev. Microbiol. 2008, 6:455-465.
16. Paul K., et al. Energy source of flagellar type III secretion. Nature 2008, 451:489-492.
17. Minamino T., Namba K. Distinct roles of the FliI ATPase and proton motive force in bacterial flagellar protein export. Nature 2008, 451:485-488.
18. Yonekura K., et al. The bacterial flagellar cap as the rotary promoter of flagellin self-assembly. Science 2000, 290:2148-2152.
19. Moriya N., et al. Genetic analysis of the bacterial hook-capping protein FlgD responsible for hook assembly. Microbiology 2011, 157:1354-1362.
20. Nambu T., et al. Plasticity of the domain structure in FlgJ, a bacterial protein involved in flagellar rod formation. Genes Genet. Syst. 2006, 81:381-389.
21. Hirano T., et al. The role in flagellar rod assembly of the N-terminal domain of Salmonella FlgJ, a flagellum-specific muramidase. J. Mol. Biol. 2001, 312:359-369.
22. Turner L., et al. Growth of flagellar filaments of Escherichia coli is independent of filament length. J. Bacteriol. 2012, 194:2437-2442.
23. Chen S.Y., et al. Structural diversity of bacterial flagellar motors. EMBO J. 2011, 30:2972-2981.
24. Liu J., et al. Cellular architecture of Treponema pallidum: novel flagellum, periplasmic cone, and cell envelope as revealed by cryo electron tomography. J. Mol. Biol. 2010, 403:546-561.
25. Zhao X.W., et al. Cryoelectron tomography reveals the sequential assembly of bacterial flagella in Borrelia burgdorferi. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:14390-14395.
26. Abrusci P., et al. Architecture of the major component of the type III secretion system export apparatus. Nat. Struct. Mol. Biol. 2013, 20:99-104.
27. Kawamoto A., et al. Common and distinct structural features of Salmonella injectisome and flagellar basal body. Sci. Rep. 2013, 3:3369.
28. Ibuki T., et al. Common architecture of the flagellar type III protein export apparatus and F- and V-type ATPases. Nat. Struct. Mol. Biol. 2011, 18:277-282.
29. Pallen M.J., et al. Evolutionary links between FliH/YscL-like proteins from bacterial type III secretion systems and second-stalk components of the FoF1 and vacuolar ATPases. Protein Sci. 2006, 15:935-940.
30. Kishikawa J., et al. Common evolutionary origin for the rotor domain of rotary ATPases and flagellar protein export apparatus. PLoS ONE 2013, 8:e64695.
31. Fraser G.M., et al. Interactions of FliJ with the Salmonella type III flagellar export apparatus. J. Bacteriol. 2003, 185:5546-5554.
32. Bange G., et al. FlhA provides the adaptor for coordinated delivery of late flagella building blocks to the type III secretion system. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:11295-11300.
33. Gonzalez-Pedrajo B., et al. Interactions between C ring proteins and export apparatus components: a possible mechanism for facilitating type III protein export. Mol. Microbiol. 2006, 60:984-998.
34. Vegh B.M., et al. Localization of the flagellum-specific secretion signal in Salmonella flagellin. Biochem. Biophys. Res. Comumn. 2006, 345:93-98.
35. Stafford G.P., et al. Sorting of early and late flagellar subunits after docking at the membrane ATPase of the type III export pathway. J. Mol. Biol. 2007, 374:877-882.
36. Evans L.D.B., et al. A chain mechanism for flagellum growth. Nature 2013, 504:287-290.
37. Thomas J., et al. Docking of cytosolic chaperone-substrate complexes at the membrane ATPase during flagellar type III protein export. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:3945-3950.
38. Fraser G.M., et al. Substrate-specific binding of hook-associated proteins by FlgN and FliT, putative chaperones for flagellum assembly. Mol. Microbiol. 1999, 32:569-580.
39. Auvray F., et al. Flagellin polymerisation control by a cytosolic export chaperone. J. Mol. Biol. 2001, 308:221-229.
40. Imada K., et al. Structural insight into the regulatory mechanisms of interactions of the flagellar type III chaperone FliT with its binding partners. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:8812-8817.
41. Minamino T., et al. Interaction of a bacterial flagellar chaperone FlgN with FlhA is required for efficient export of its cognate substrates. Mol. Microbiol. 2012, 83:775-788.
42. Kinoshita M., et al. Interactions of bacterial flagellar chaperone-substrate complexes with FlhA contribute to co-ordinating assembly of the flagellar filament. Mol. Microbiol. 2013, 90:1249-1261.
43. Evans L.D.B., et al. An escort mechanism for cycling of export chaperones during flagellum assembly. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:17474-17479.
44. Ferris H.U., et al. FlhB regulates ordered export of flagellar components via autocleavage mechanism. J. Biol. Chem. 2005, 280:41236-41242.
45. Meshcheryakov V.A., et al. Inhibition of a type III secretion system by the deletion of a short loop in one of its membrane proteins. Acta Crystallogr. D: Biol. Crystallogr. 2013, 69:812-820.
46. Minamino T., Macnab R.M. Domain structure of Salmonella FlhB, a flagellar export component responsible for substrate specificity switching. J. Bacteriol. 2000, 182:4906-4914.
47. Fraser G., et al. Substrate specificity of type III flagellar protein export in Salmonella is controlled by subdomain interactions in FlhB. Mol. Microbiol. 2003, 48:1043-1057.
48. Meshcheryakov V.A., et al. Structural flexibility of the cytoplasmic domain of flagellar type III secretion protein FlhB is important for the function of the protein. Biophys. J. 2012, 102:626A.
49. Meshcheryakov V.A., et al. Function of FlhB, a membrane protein implicated in the bacterial flagellar type III secretion system. PLoS ONE 2013, 8:e68384.
50. Erhardt M., et al. The role of the FliK molecular ruler in hook-length control in Salmonella enterica. Mol. Microbiol. 2010, 75:1272-1284.
51. Mizuno S., et al. The NMR structure of FliK, the trigger for the switch of substrate specificity in the flagellar type III secretion apparatus. J. Mol. Biol. 2011, 409:558-573.
52. Hughes K.T. Flagellar hook length is controlled by a secreted molecular ruler. J. Bacteriol. 2012, 194:4793-4796.
53. Aizawa S. Mystery of FliK in length control of the flagellar hook. J. Bacteriol. 2012, 194:4798-4800.
54. Erhardt M., et al. An infrequent molecular ruler controls flagellar hook length in Salmonella enterica. EMBO J. 2011, 30:2948-2961.
55. Minamino T., et al. Interaction of FliK with the bacterial flagellar hook is required for efficient export specificity switching. Mol. Microbiol. 2009, 74:239-251.
56. Moriya N., et al. The type III flagellar export specificity switch is dependent on FliK ruler and a molecular clock. J. Mol. Biol. 2006, 359:466-477.
57. Minamino T., et al. An energy transduction mechanism used in bacterial flagellar type III protein export. Nat. Commun. 2011, 2:475.
58. Hara N., et al. Genetic characterization of conserved charged residues in the bacterial flagellar type III export protein FlhA. PLoS ONE 2011, 6:e22417.
59. Aizawa S., Kubori T. Bacterial flagellation and cell division. Genes Cells 1998, 3:625-634.
60. Iino T. Assembly of Salmonella flagellin in vitro and in vivo. J. Supramol. Struct. 1974, 2:372-384.
61. Koroyasu S., et al. Kinetic analysis of the growth rate of the flagellar hook in Salmonella typhimurium by the population balance method. Biophys. J. 1998, 74:436-443.
62. Lappala A., et al. Ratcheted diffusion transport through crowded nanochannels. Sci. Rep. 2013, 3:3103.
63. Stern A.S., Berg H.C. Single-file diffusion of flagellin in flagellar filaments. Biophys. J. 2013, 105:182-184.
64. Radics J., et al. Structure of a pathogenic type 3 secretion system in action. Nat. Struct. Mol. Biol. 2014, 21:82-87.
65. Yonekura K., et al. Structure analysis of the flagellar cap-filament complex by electron cryomicroscopy and single-particle image analysis. J. Struct. Biol. 2001, 133:246-253.
66. Ellis R.J. Protein folding: importance of the Anfinsen cage. Curr. Biol. 2003, 13:R881-R883.
67. Imada K., et al. Structural similarity between the flagellar type III ATPase Flil and F-1-ATPase subunits. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:485-490.
68. Brown P.N., et al. Crystal structure of the middle and C-terminal domains of the flagellar rotor protein FliG. EMBO J. 2002, 21:3225-3234.
69. Park S.Y., et al. Structure of FliM provides insight into assembly of the switch complex in the bacterial flagella motor. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:11886-11891.
70. Brown P.N., et al. Crystal structure of the flagellar rotor protein FIN from Thermotoga maritima. J. Bacteriol. 2005, 187:2890-2902.
71. Evdokimov A.G., et al. Similar modes of polypeptide recognition by export chaperones in flagellar biosynthesis and type III secretion. Nat. Struct. Biol. 2003, 10:789-793.
72. Saijo-Hamano Y., et al. Structure of the cytoplasmic domain of FlhA and implication for flagellar type III protein export. Mol. Microbiol. 2010, 76:260-268.