Biophysical Reviews

, Volume 10, Issue 2, pp 617–629 | Cite as

Molecular dynamics simulation of bacterial flagella

Review

Abstract

The bacterial flagellum is a biological nanomachine for the locomotion of bacteria, and is seen in organisms like Salmonella and Escherichia coli. The flagellum consists of tens of thousands of protein molecules and more than 30 different kinds of proteins. The basal body of the flagellum contains a protein export apparatus and a rotary motor that is powered by ion motive force across the cytoplasmic membrane. The filament functions as a propeller whose helicity is controlled by the direction of the torque. The hook that connects the motor and filament acts as a universal joint, transmitting torque generated by the motor to different directions. This report describes the use of molecular dynamics to study the bacterial flagellum. Molecular dynamics simulation is a powerful method that permits the investigation, at atomic resolution, of the molecular mechanisms of biomolecular systems containing many proteins and solvent. When applied to the flagellum, these studies successfully unveiled the polymorphic supercoiling and transportation mechanism of the filament, the universal joint mechanism of the hook, the ion transfer mechanism of the motor stator, the flexible nature of the transport apparatus proteins, and activation of proteins involved in chemotaxis.

Keywords

Molecular dynamics Polymorphic supercoiling Universal joint Protein export Ion transport Chemotaxis 

Notes

Acknowledgements

This research was supported by MEXT/JSPS KAKENHI (nos. 25104002 and 15H04357) to A.K. and by MEXT as “Priority Issue on Post-K Computer” (Building Innovative Drug Discovery Infrastructure Through Functional Control of Biomolecular Systems) to A.K. The computations were partly performed using the supercomputers at the RCCS, The National Institute of Natural Science, and ISSP, The University of Tokyo. This research also used computational resources of the K computer provided by the RIKEN Advanced Institute for Computational Science through the HPCI System Research project (project IDs: hp120223, hp140030, hp140031, hp150049, hp150270, hp160207, and hp170254).

Compliance with ethical standards

Conflict of interest

Akio Kitao declares that he has no conflict of interest. Hiroaki Hata declares that he has no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Aizawa S (2001) Bacterial flagella and type III secretion systems. FEMS Microbiol Lett 202(2):157–164Google Scholar
  2. Arkhipov A, Freddolino PL, Imada K, Namba K, Schulten K (2006) Coarse-grained molecular dynamics simulations of a rotating bacterial flagellum. Biophys J 91(12):4589–4597PubMedPubMedCentralCrossRefGoogle Scholar
  3. Asai Y, Yakushi T, Kawagishi I, Homma M (2003) Ion-coupling determinants of Na+-driven and H+-driven flagellar motors. J Mol Biol 327(2):453–463PubMedCrossRefGoogle Scholar
  4. Asakura S (1970) Polymerization of flagellin and polymorphism of flagella. Adv Biophys 1:99–155PubMedGoogle Scholar
  5. Berg HC (2003) The rotary motor of bacterial flagella. Annu Rev Biochem 72(1):19–54PubMedCrossRefGoogle Scholar
  6. Berg HC, Anderson RA (1973) Bacteria swim by rotating their flagellar filaments. Nature 245(5425):380–382PubMedCrossRefGoogle Scholar
  7. Berry RM (1993) Torque and switching in the bacterial flagellar motor. An electrostatic model. Biophys J 64(4):961–973PubMedPubMedCentralCrossRefGoogle Scholar
  8. Block SM, Berg HC (1984) Successive incorporation of force-generating units in the bacterial rotary motor. Nature 309(5967):470–472PubMedCrossRefGoogle Scholar
  9. Braun TF, Blair DF (2001) Targeted disulfide cross-linking of the MotB protein of Escherichia coli: evidence for two H(+) channels in the stator complex. Biochemistry 40(43):13051–13059PubMedCrossRefGoogle Scholar
  10. Braun TF, Al-Mawsawi LQ, Kojima S, Blair DF (2004) Arrangement of core membrane segments in the MotA/MotB proton-channel complex of Escherichia coli. Biochemistry 43(1):35–45PubMedCrossRefGoogle Scholar
  11. Calladine CR (1975) Construction of bacterial flagella. Nature 255(5504):121–124PubMedCrossRefGoogle Scholar
  12. Calladine CR (1976) Design requirements for the construction of bacterial flagella. J Theor Biol 57(2):469–489PubMedCrossRefGoogle Scholar
  13. Calladine CR (1978) Change of waveform in bacterial flagella: the role of mechanics at the molecular level. J Mol Biol 118(4):457–479CrossRefGoogle Scholar
  14. Chng C-P, Kitao A (2008) Thermal unfolding simulations of bacterial flagellin: insight into its refolding before assembly. Biophys J 94(10):3858–3871PubMedPubMedCentralCrossRefGoogle Scholar
  15. Chng C-P, Kitao A (2010) Mechanical unfolding of bacterial flagellar filament protein by molecular dynamics simulation. J Mol Graph Model 28(6):548–554PubMedCrossRefGoogle Scholar
  16. Chun SY, Parkinson JS (1988) Bacterial motility: membrane topology of the Escherichia coli MotB protein. Science 239(4837):276–278PubMedCrossRefGoogle Scholar
  17. Cornelis GR (2006) The type III secretion injectisome. Nat Rev Microbiol 4(11):811–825PubMedCrossRefGoogle Scholar
  18. Dasgupta J, Dattagupta JK (2008) Structural determinants of V. cholerae CheYs that discriminate them in FliM binding: comparative modeling and MD simulation studies. J Biomol Struct Dyn 25(5):495–503PubMedCrossRefGoogle Scholar
  19. De Mot R, Vanderleyden J (1994) The C-terminal sequence conservation between Ompa-related outer membrane proteins and Motb suggests a common function in both Gram-positive and Gram-negative bacteria, possibly in the interaction of these domains with peptidoglycan. Mol Microbiol 12(2):333–336PubMedCrossRefGoogle Scholar
  20. Dean GE, Macnab RM, Stader J, Matsumura P, Burks C (1984) Gene sequence and predicted amino acid sequence of the motA protein, a membrane-associated protein required for flagellar rotation in Escherichia coli. J Bacteriol 159(3):991–999PubMedPubMedCentralGoogle Scholar
  21. Elston TC, Oster G (1997) Protein turbines. I: the bacterial flagellar motor. Biophys J 73(2):703–721PubMedPubMedCentralCrossRefGoogle Scholar
  22. Enomoto M (1966) Genetic studies of paralyzed mutants in Salmonella. II. Mapping of three mot loci by linkage analysis. Genetics 54(5):1069–1076PubMedPubMedCentralGoogle Scholar
  23. Fraiberg M, Afanzar O, Cassidy CK, Gabashvili A, Schulten K, Levin Y, Eisenbach M (2015) CheY’s acetylation sites responsible for generating clockwise flagellar rotation in Escherichia coli. Mol Microbiol 95(2):231–244PubMedCrossRefGoogle Scholar
  24. Fraser GM, Hirano T, Ferris HU, Devgan LL, Kihara M, Macnab RM (2003) Substrate specificity of type III flagellar protein export in Salmonella is controlled by subdomain interactions in FlhB. Mol Microbiol 48(4):1043–1057PubMedCrossRefGoogle Scholar
  25. Fujii T, Kato T, Namba K (2009) Specific arrangement of alpha-helical coiled coils in the core domain of the bacterial flagellar hook for the universal joint function. Structure 17(11):1485–1493PubMedCrossRefGoogle Scholar
  26. Furuta T, Samatey FA, Matsunami H, Imada K, Namba K, Kitao A (2007) Gap compression/extension mechanism of bacterial flagellar hook as the molecular universal joint. J Struct Biol 157(3):481–490PubMedCrossRefGoogle Scholar
  27. Ghosh A, Albers SV (2011) Assembly and function of the archaeal flagellum. Biochem Soc Trans 39(1):64–69PubMedCrossRefGoogle Scholar
  28. Hasegawa K, Yamashita I, Namba K (1998) Quasi- and nonequivalence in the structure of bacterial flagellar filament. Biophys J 74(1):569–575PubMedPubMedCentralCrossRefGoogle Scholar
  29. Hayward S (1999) Structural principles governing domain motions in proteins. Proteins 36(4):425–435PubMedCrossRefGoogle Scholar
  30. Hayward S, Berendsen HJ (1998) Systematic analysis of domain motions in proteins from conformational change: new results on citrate synthase and T4 lysozyme. Proteins 30(2):144–154PubMedCrossRefGoogle Scholar
  31. Hirano T, Yamaguchi S, Oosawa K, Aizawa S (1994) Roles of FliK and FlhB in determination of flagellar hook length in Salmonella typhimurium. J Bacteriol 176(17):5439–5449Google Scholar
  32. Hirota N, Kitada M, Imae Y (1981) Flagellar motors of alkalophilic Bacillus are powered by an electrochemical potential gradient of Na+. FEBS Lett 132(2):278–280CrossRefGoogle Scholar
  33. Honda S, Uedaira H, Vonderviszt F, Kidokoro S, Namba K (1999) Folding energetics of a multidomain protein, flagellin. J Mol Biol 293(3):719–732PubMedCrossRefGoogle Scholar
  34. Hotani H (1980) Micro-video study of moving bacterial flagellar filaments II. Polymorphic transition in alcohol. Biosystems 12(3–4):325–330PubMedCrossRefGoogle Scholar
  35. Hotani H (1982) Micro-video study of moving bacterial flagellar filaments: III. Cyclic transformation induced by mechanical force. J Mol Biol 156(4):791–806PubMedCrossRefGoogle Scholar
  36. Hyakutake A, Homma M, Austin MJ, Boin MA, Häse CC, Kawagishi I (2005) Only one of the five CheY homologs in Vibrio cholerae directly switches flagellar rotation. J Bacteriol 187(24):8403–8410PubMedPubMedCentralCrossRefGoogle Scholar
  37. Ikeda T, Yamaguchi S, Hotani H (1993) Flagellar growth in a filament-less Salmonella fliD mutant supplemented with purified hook-associated protein 2. J Biochem 114(1):39–44PubMedCrossRefGoogle Scholar
  38. Isralewitz B, Baudry J, Gullingsrud J, Kosztin D, Schulten K (2001a) Steered molecular dynamics investigations of protein function. J Mol Graph Model 19(1):13–25PubMedCrossRefGoogle Scholar
  39. Isralewitz B, Gao M, Schulten K (2001b) Steered molecular dynamics and mechanical functions of proteins. Curr Opin Struct Biol 11(2):224–230PubMedCrossRefGoogle Scholar
  40. Jensen MØ, Park S, Tajkhorshid E, Schulten K (2002) Energetics of glycerol conduction through aquaglyceroporin GlpF. Proc Natl Acad Sci U S A 99(10):6731–6736PubMedPubMedCentralCrossRefGoogle Scholar
  41. Kamiya R, Asakura S (1976a) Flagellar transformations at alkaline pH. J Mol Biol 108(2):513–518PubMedCrossRefGoogle Scholar
  42. Kamiya R, Asakura S (1976b) Helical transformations of Salmonella flagella in vitro. J Mol Biol 106(1):167–186PubMedCrossRefGoogle Scholar
  43. Kamiya R, Hotani H, Asakura S (1982) Polymorphic transition in bacterial flagella. Symp Soc Exp Biol 35:53–76PubMedGoogle Scholar
  44. Kanto S, Okino H, Aizawa S, Yamaguchi S (1991) Amino acids responsible for flagellar shape are distributed in terminal regions of flagellin. J Mol Biol 219(3):471–480PubMedCrossRefGoogle Scholar
  45. Kato S, Okamoto M, Asakura S (1984) Polymorphic transition of the flagellar polyhook from Escherichia coli and Salmonella typhimurium. J Mol Biol 173(4):463–476PubMedCrossRefGoogle Scholar
  46. Kawamoto A, Morimoto YV, Miyata T, Minamino T, Hughes KT, Kato T, Namba K (2013) Common and distinct structural features of Salmonella injectisome and flagellar basal body. Sci Rep 3:3369PubMedPubMedCentralCrossRefGoogle Scholar
  47. Khan S, Dapice M, Reese TS (1988) Effects of mot gene expression on the structure of the flagellar motor. J Mol Biol 202(3):575–584PubMedCrossRefGoogle Scholar
  48. Kim EA, Price-Carter M, Carlquist WC, Blair DF (2008) Membrane segment organization in the stator complex of the flagellar motor: implications for proton flow and proton-induced conformational change. Biochemistry 47(43):11332–11339PubMedPubMedCentralCrossRefGoogle Scholar
  49. Kitao A, Takemura K (2017) High anisotropy and frustration: the keys to regulating protein function efficiently in crowded environments. Curr Opin Struct Biol 42:50–58PubMedCrossRefGoogle Scholar
  50. Kitao A, Yonekura K, Maki-Yonekura S, Samatey FA, Imada K, Namba K, Go N (2006) Switch interactions control energy frustration and multiple flagellar filament structures. Proc Natl Acad Sci U S A 103(13):4894–4899PubMedPubMedCentralCrossRefGoogle Scholar
  51. Kojima S, Blair DF (2001) Conformational change in the stator of the bacterial flagellar motor. Biochemistry 40(43):13041–13050PubMedCrossRefGoogle Scholar
  52. Kojima S, Imada K, Sakuma M, Sudo Y, Kojima C, Minamino T, Homma M, Namba K (2009) Stator assembly and activation mechanism of the flagellar motor by the periplasmic region of MotB. Mol Microbiol 73(4):710–718PubMedCrossRefGoogle Scholar
  53. Kutsukake K, Minamino T, Yokoseki T (1994) Isolation and characterization of FliK-independent flagellation mutants from Salmonella typhimurium. J Bacteriol 176(24):7625–7629PubMedPubMedCentralCrossRefGoogle Scholar
  54. Larsen SH, Adler J, Gargus JJ, Hogg RW (1974a) Chemomechanical coupling without ATP: the source of energy for motility and chemotaxis in bacteria. Proc Natl Acad Sci U S A 71(4):1239–1243PubMedPubMedCentralCrossRefGoogle Scholar
  55. Larsen SH, Reader RW, Kort EN, Tso WW, Adler J (1974b) Change in direction of flagellar rotation is the basis of the chemotactic response in Escherichia coli. Nature 249(5452):74–77PubMedCrossRefGoogle Scholar
  56. Lountos GT, Austin BP, Nallamsetty S, Waugh DS (2009) Atomic resolution structure of the cytoplasmic domain of Yersinia pestis YscU, a regulatory switch involved in type III secretion. Protein Sci 18(2):467–474PubMedPubMedCentralCrossRefGoogle Scholar
  57. Macnab RM (2003) How bacteria assemble flagella. Annu Rev Microbiol 57:77–100PubMedCrossRefGoogle Scholar
  58. Macnab RM, Ornston MK (1977) Normal-to-curly flagellar transitions and their role in bacterial tumbling. Stabilization of an alternative quaternary structure by mechanical force. J Mol Biol 112(1):1–30PubMedCrossRefGoogle Scholar
  59. Maki-Yonekura S, Yonekura K, Namba K (2010) Conformational change of flagellin for polymorphic supercoiling of the flagellar filament. Nat Struct Mol Biol 17(4):417–422PubMedCrossRefGoogle Scholar
  60. Matsunami H, Barker CS, Yoon YH, Wolf M, Samatey FA (2016) Complete structure of the bacterial flagellar hook reveals extensive set of stabilizing interactions. Nat Commun 7:13425PubMedPubMedCentralCrossRefGoogle Scholar
  61. Meister M, Lowe G, Berg HC (1987) The proton flux through the bacterial flagellar motor. Cell 49(5):643–650PubMedCrossRefGoogle Scholar
  62. Meshcheryakov VA, Kitao A, Matsunami H, Samatey FA (2013) 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 69(Pt 5):812–820PubMedPubMedCentralCrossRefGoogle Scholar
  63. Minamino T, Macnab RM (1999) Components of the Salmonella flagellar export apparatus and classification of export substrates. J Bacteriol 181(5):1388–1394PubMedPubMedCentralGoogle Scholar
  64. Morgan DG, Macnab RM, Francis NR, DeRosier DJ (1993) Domain organization of the subunit of the Salmonella typhimurium flagellar hook. J Mol Biol 229(1):79–84PubMedCrossRefGoogle Scholar
  65. Muskotál A, Király R, Sebestyén A, Gugolya Z, Végh BM, Vonderviszt F (2006) Interaction of FliS flagellar chaperone with flagellin. FEBS Lett 580(16):3916–3920PubMedCrossRefGoogle Scholar
  66. Namba K, Vonderviszt F (1997) Molecular architecture of bacterial flagellum. Q Rev Biophys 30(1):1–65PubMedCrossRefGoogle Scholar
  67. Nishihara Y, Kitao A (2015) Gate-controlled proton diffusion and protonation-induced ratchet motion in the stator of the bacterial flagellar motor. Proc Natl Acad Sci U S A 112(25):7737–7742PubMedPubMedCentralCrossRefGoogle Scholar
  68. Nishima W, Qi G, Hayward S, Kitao A (2009) DTA: dihedral transition analysis for characterization of the effects of large main-chain dihedral changes in proteins. Bioinformatics 25(5):628–635PubMedCrossRefGoogle Scholar
  69. O’Brien EJ, Bennett PM (1972) Structure of straight flagella from a mutant Salmonella. J Mol Biol 70(1):133–152PubMedCrossRefGoogle Scholar
  70. O’Neill J, Xie M, Hijnen M, Roujeinikova A (2011) Role of the MotB linker in the assembly and activation of the bacterial flagellar motor. Acta Crystallogr D Biol Crystallogr 67(Pt 12):1009–1016PubMedCrossRefGoogle Scholar
  71. Ozin AJ, Claret L, Auvray F, Hughes C (2003) The FliS chaperone selectively binds the disordered flagellin C-terminal D0 domain central to polymerisation. FEMS Microbiol Lett 219(2):219–224PubMedCrossRefGoogle Scholar
  72. Patterson-Delafield J, Martinez RJ, Stocker BA, Yamaguchi S (1973) A new fla gene in Salmonella typhimurium—flaR—and its mutant phenotype-superhooks. Arch Microbiol 90(2):107–120Google Scholar
  73. Qi G, Lee R, Hayward S (2005) A comprehensive and non-redundant database of protein domain movements. Bioinformatics 21(12):2832–2838PubMedCrossRefGoogle Scholar
  74. Reboul CF, Andrews DA, Nahar MF, Buckle AM, Roujeinikova A (2011) Crystallographic and molecular dynamics analysis of loop motions unmasking the peptidoglycan-binding site in stator protein MotB of flagellar motor. PLoS One 6(4):e18981PubMedPubMedCentralCrossRefGoogle Scholar
  75. Roujeinikova A (2008) Crystal structure of the cell wall anchor domain of MotB, a stator component of the bacterial flagellar motor: implications for peptidoglycan recognition. Proc Natl Acad Sci U S A 105(30):10348–10353PubMedPubMedCentralCrossRefGoogle Scholar
  76. Saijo-Hamano Y, Imada K, Minamino T, Kihara M, Shimada M, Kitao A, Namba K (2010) Structure of the cytoplasmic domain of FlhA and implication for flagellar type III protein export. Mol Microbiol 76(1):260–268PubMedCrossRefGoogle Scholar
  77. Samatey FA, Imada K, Nagashima S, Vonderviszt F, Kumasaka T, Yamamoto M, Namba K (2001) Structure of the bacterial flagellar protofilament and implications for a switch for supercoiling. Nature 410(6826):331–337PubMedCrossRefGoogle Scholar
  78. Samatey FA, Matsunami H, Imada K, Nagashima S, Shaikh TR, Thomas DR, Chen JZ, Derosier DJ, Kitao A, Namba K (2004) Structure of the bacterial flagellar hook and implication for the molecular universal joint mechanism. Nature 431(7012):1062–1068PubMedCrossRefGoogle Scholar
  79. Samuel AD, Berg HC (1996) Torque-generating units of the bacterial flagellar motor step independently. Biophys J 71(2):918–923PubMedPubMedCentralCrossRefGoogle Scholar
  80. Shaikh TR, Thomas DR, Chen JZ, Samatey FA, Matsunami H, Imada K, Namba K, Derosier DJ (2005) A partial atomic structure for the flagellar hook of Salmonella typhimurium. Proc Natl Acad Sci U S A 102(4):1023–1028PubMedPubMedCentralCrossRefGoogle Scholar
  81. Sharp LL, Zhou J, Blair DF (1995a) Tryptophan-scanning mutagenesis of MotB, an integral membrane protein essential for flagellar rotation in Escherichia coli. Biochemistry 34(28):9166–9171PubMedCrossRefGoogle Scholar
  82. Sharp LL, Zhou J, Blair DF (1995b) Features of MotA proton channel structure revealed by tryptophan-scanning mutagenesis. Proc Natl Acad Sci U S A 92(17):7946–7950PubMedPubMedCentralCrossRefGoogle Scholar
  83. Silverman M, Simon M (1974) Characterization of Escherichia coli flagellar mutants that are insensitive to catabolite repression. J Bacteriol 120(3):1196–1203PubMedPubMedCentralGoogle Scholar
  84. Stader J, Matsumura P, Vacante D, Dean GE, Macnab RM (1986) Nucleotide sequence of the Escherichia coli motB gene and site-limited incorporation of its product into the cytoplasmic membrane. J Bacteriol 166(1):244–252PubMedPubMedCentralCrossRefGoogle Scholar
  85. Tanner DE, Ma W, Chen Z, Schulten K (2011) Theoretical and computational investigation of flagellin translocation and bacterial flagellum growth. Biophys J 100(11):2548–2556PubMedPubMedCentralCrossRefGoogle Scholar
  86. Terahara N, Sano M, Ito M (2012) A Bacillus flagellar motor that can use both Na+ and K+ as a coupling ion is converted by a single mutation to use only Na+. PLoS One 7(9):e46248PubMedPubMedCentralCrossRefGoogle Scholar
  87. Thomas NA, Bardy SL, Jarrell KF (2001) The archaeal flagellum: a different kind of prokaryotic motility structure. FEMS Microbiol Rev 25(2):147–174PubMedCrossRefGoogle Scholar
  88. Turner L, Ryu WS, Berg HC (2000) Real-time imaging of fluorescent flagellar filaments. J Bacteriol 182(10):2793–2801PubMedPubMedCentralCrossRefGoogle Scholar
  89. Vonderviszt F, Aizawa SI, Namba K (1991) Role of the disordered terminal regions of flagellin in filament formation and stability. J Mol Biol 221(4):1461–1474PubMedCrossRefGoogle Scholar
  90. Wagenknecht T, DeRosier DJ, Aizawa S, Macnab RM (1982) Flagellar hook structures of Caulobacter and Salmonella and their relationship to filament structure. J Mol Biol 162(1):69–87PubMedCrossRefGoogle Scholar
  91. Walz D, Caplan SR (2000) An electrostatic mechanism closely reproducing observed behavior in the bacterial flagellar motor. Biophys J 78(2):626–651PubMedPubMedCentralCrossRefGoogle Scholar
  92. Welch M, Oosawa K, Aizawa S, Eisenbach M (1993) Phosphorylation-dependent binding of a signal molecule to the flagellar switch of bacteria. Proc Natl Acad Sci U S A 90(19):8787–8791PubMedPubMedCentralCrossRefGoogle Scholar
  93. Welch M, Oosawa K, Aizawa S, Eisenbach M (1994) Effects of phosphorylation, Mg2+, and conformation of the chemotaxis protein CheY on its binding to the flagellar switch protein FliM. Biochemistry 33(34):10470–10476Google Scholar
  94. Williams AW, Yamaguchi S, Togashi F, Aizawa S, Kawagishi I, Macnab RM (1996) Mutations in fliK and flhB affecting flagellar hook and filament assembly in Salmonella typhimurium. J Bacteriol 178(10):2960–2970Google Scholar
  95. Yamaguchi S, Fujita H, Ishihara A, Aizawa S, Macnab RM (1986) Subdivision of flagellar genes of Salmonella typhimurium into regions responsible for assembly, rotation, and switching. J Bacteriol 166(1):187–193PubMedPubMedCentralCrossRefGoogle Scholar
  96. Yamashita I, Hasegawa K, Suzuki H, Vonderviszt F, Mimori-Kiyosue Y, Namba K (1998) Structure and switching of bacterial flagellar filaments studied by X-ray fiber diffraction. Nat Struct Mol Biol 5(2):125–132CrossRefGoogle Scholar
  97. Yonekura K, Maki S, Morgan DG, DeRosier DJ, Vonderviszt F, Imada K, Namba K (2000) The bacterial flagellar cap as the rotary promoter of flagellin self-assembly. Science 290(5499):2148–2152PubMedCrossRefGoogle Scholar
  98. Yonekura K, Maki-Yonekura S, Namba K (2003) Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424(6949):643–650PubMedCrossRefGoogle Scholar
  99. Zarivach R, Deng W, Vuckovic M, Felise HB, Nguyen HV, Miller SI, Finlay BB, Strynadka NC (2008) Structural analysis of the essential self-cleaving type III secretion proteins EscU and SpaS. Nature 453(7191):124–127PubMedCrossRefGoogle Scholar
  100. Zhou J, Fazzio RT, Blair DF (1995) Membrane topology of the MotA protein of Escherichia coli. J Mol Biol 251(2):237–242PubMedCrossRefGoogle Scholar
  101. Zhu S, Takao M, Li N, Sakuma M, Nishino Y, Homma M, Kojima S, Imada K (2014) Conformational change in the periplamic region of the flagellar stator coupled with the assembly around the rotor. Proc Natl Acad Sci U S A 111(37):13523–13528PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© International Union for Pure and Applied Biophysics (IUPAB) and Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.School of Life Science and TechnologyTokyo Institute of TechnologyTokyoJapan
  2. 2.Institute of Molecular and Cellular BiosciencesThe University of TokyoTokyoJapan

Personalised recommendations