Abstract
One of the central systems responsible for bacterial motility is the flagellum. The bacterial flagellum is a macromolecular protein complex that is more than five times the cell length. Flagella-driven motility is coordinated via a chemosensory signal transduction pathway, and so bacterial cells sense changes in the environment and migrate towards more desirable locations. The flagellum of Salmonella enterica serovar Typhimurium is composed of a bi-directional rotary motor, a universal joint and a helical propeller. The flagellar motor, which structurally resembles an artificial motor, is embedded within the cell envelop and spins at several hundred revolutions per second. In contrast to an artificial motor, the energy utilized for high-speed flagellar motor rotation is the inward-directed proton flow through a transmembrane proton channel of the stator unit of the flagellar motor. The flagellar motor realizes efficient chemotaxis while performing high-speed movement by an ingenious directional switching mechanism of the motor rotation. To build the universal joint and helical propeller structures outside the cell body, the flagellar motor contains its own protein transporter called a type III protein export apparatus. In this chapter we summarize the structure and assembly of the Salmonella flagellar motor complex.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Similar content being viewed by others
References
Abrusci P, Vergara-Irigaray M, Johnson S, Beeby MD, Hendrixson DR, Roversi P, Friede ME, Deane JE, Jensen GJ, Tang CM, Lea SM (2013) Architecture of the major component of the type III secretion system export apparatus. Nat Struct Mol Biol 20(1):99–104. https://doi.org/10.1038/nsmb.2452
Aldridge P, Karlinsey J, Hughes KT (2003) The type III secretion chaperone FlgN regulates flagellar assembly via a negative feedback loop containing its chaperone substrates FlgK and FlgL. Mol Microbiol 49(5):1333–1345. https://doi.org/10.1046/j.1365-2958.2003.03637.x
Asakura S (1970) Polymerization of flagellin and polymorphism of flagella. Adv Biophys 1:99–155
Auvray F, Thomas J, Fraser GM, Hughes C (2001) Flagellin polymerisation control by a cytosolic export chaperone. J Mol Biol 308(2):221–229. https://doi.org/10.1006/jmbi.2001.4597
Bai F, Morimoto YV, Yoshimura SDJ, Hara N, Kami-Ike N, Namba K, Minamino T (2014) Assembly dynamics and the roles of FliI ATPase of the bacterial flagellar export apparatus. Sci Rep 4:6528. https://doi.org/10.1038/srep06528
Baker MA, Hynson RM, Ganuelas LA, Mohammadi NS, Liew CW, Rey AA, Duff AP, Whitten AE, Jeffries CM, Delalez NJ, Morimoto YV, Stock D, Armitage JP, Turberfield AJ, Namba K, Berry RM, Lee LK (2016) Domain-swap polymerization drives the self-assembly of the bacterial flagellar motor. Nat Struct Mol Biol 23(3):197–203. https://doi.org/10.1038/nsmb.3172
Bange G, Kummerer N, Engel C, Bozkurt G, Wild K, Sinning I (2010) FlhA provides the adaptor for coordinated delivery of late flagella building blocks to the type III secretion system. Proc Natl Acad Sci USA 107(25):11295–11300. https://doi.org/10.1073/pnas.1001383107
Bennett JC, Thomas J, Fraser GM, Hughes C (2001) Substrate complexes and domain organization of the Salmonella flagellar export chaperones FlgN and FliT. Mol Microbiol 39(3):781–791. https://doi.org/10.1046/j.1365-2958.2001.02268.x
Berg HC (2003) The rotary motor of bacterial flagella. Annu Rev Biochem 72:19–54. https://doi.org/10.1146/annurev.biochem.72.121801.161737
Bi S, Sourjik V (2018) Stimulus sensing and signal processing in bacterial chemotaxis. Curr Opin Microbiol 45:22–29. https://doi.org/10.1016/j.mib.2018.02.002
Boehm A, Kaiser M, Li H, Spangler C, Kasper CA, Ackermann M, Kaever V, Sourjik V, Roth V, Jenal U (2010) Second messenger-mediated adjustment of bacterial swimming velocity. Cell 141(1):107–116. https://doi.org/10.1016/j.cell.2010.01.018
Branch RW, Sayegh MN, Shen C, Nathan VSJ, Berg HC (2014) Adaptive remodelling by FliN in the bacterial rotary motor. J Mol Biol 426(19):3314–3324. https://doi.org/10.1016/j.jmb.2014.07.009
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):13051–13059. https://doi.org/10.1021/bi011264g
Braun TF, Poulson S, Gully JB, Empey JC, Van Way S, Putnam A, Blair DF (1999) Function of proline residues of MotA in torque generation by the flagellar motor of Escherichia coli. J Bacteriol 181(11):3542–3551
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):35–45. https://doi.org/10.1021/bi035406d
Butan C, Lara-Tejero M, Li W, Liu J, Galan JE (2019) High-resolution view of the type III secretion export apparatus in situ reveals membrane remodeling and a secretion pathway. Proc Natl Acad Sci USA 116(49):24786–24795. https://doi.org/10.1073/pnas.1916331116
Calladine CR (1975) Construction of bacterial flagella. Nature 255(5504):121–124. https://doi.org/10.1038/255121a0
Calladine CR (1976) Design requirements for the construction of bacterial flagella. J Theor Biol 57(2):469–489. https://doi.org/10.1016/0022-5193(76)90016-3
Castillo DJ, Nakamura S, Morimoto YV, Che YS, Kami-Ike N, Kudo S, Minamino T, Namba K (2013) The C-terminal periplasmic domain of MotB is responsible for load-dependent control of the number of stators of the bacterial flagellar motor. Biophysics 9:173–181. https://doi.org/10.2142/biophysics.9.173
Che YS, Nakamura S, Kojima S, Kami-ike N, Namba K, Minamino T (2008) Suppressor analysis of the MotB(D33E) mutation to probe bacterial flagellar motor dynamics coupled with proton translocation. J Bacteriol 190(20):6660–6667. https://doi.org/10.1128/JB.00503-08
Che YS, Nakamura S, Morimoto YV, Kami-Ike N, Namba K, Minamino T (2014) Load-sensitive coupling of proton translocation and torque generation in the bacterial flagellar motor. Mol Microbiol 91(1):175–184. https://doi.org/10.1111/mmi.12453
Chevance FF, Takahashi N, Karlinsey JE, Gnerer J, Hirano T, Samudrala R, Aizawa S, Hughes KT (2007) The mechanism of outer membrane penetration by the eubacterial flagellum and implications for spirochete evolution. Genes Dev 21(18):2326–2335. https://doi.org/10.1101/gad.1571607
Cho SY, Song WS, Yoon SI (2019) Crystal structure of the flagellar cap protein FliD from Bdellovibrio bacteriovorus. Biochem Biophys Res Commun 519(3):652–658. https://doi.org/10.1016/j.bbrc.2019.09.024
Claret L, Calder SR, Higgins M, Hughes C (2003) Oligomerization and activation of the FliI ATPase central to bacterial flagellum assembly. Mol Microbiol 48(5):1349–1355. https://doi.org/10.1046/j.1365-2958.2003.03506.x
Delalez NJ, Wadhams GH, Rosser G, Xue Q, Brown MT, Dobbie IM, Berry RM, Leake MC, Armitage JP (2010) Signal-dependent turnover of the bacterial flagellar switch protein FliM. Proc Natl Acad Sci USA 107(25):11347–11351. https://doi.org/10.1073/pnas.1000284107
Delalez NJ, Berry RM, Armitage JP (2014) Stoichiometry and turnover of the bacterial flagellar switch protein FliN. mBio 5(4):e01216–01214. https://doi.org/10.1128/mBio.01216-14
Dyer CM, Vartanian AS, Zhou H, Dahlquist FW (2009) A molecular mechanism of bacterial flagellar motor switching. J Mol Biol 388(1):71–84. https://doi.org/10.1016/j.jmb.2009.02.004
Erhardt M, Wheatley P, Kim EA, Hirano T, Zhang Y, Sarkar MK, Hughes KT, Blair DF (2017) Mechanism of type-III protein secretion: regulation of FlhA conformation by a functionally critical charged-residue cluster. Mol Microbiol 104(2):234–249. https://doi.org/10.1111/mmi.13623
Evans LD, Stafford GP, Ahmed S, Fraser GM, Hughes C (2006) An escort mechanism for cycling of export chaperones during flagellum assembly. Proc Natl Acad Sci USA 103(46):17474–17479. https://doi.org/10.1073/pnas.0605197103
Evdokimov AG, Phan J, Tropea JE, Routzahn KM, Peters HK, Pokross M, Waugh DS (2003) Similar modes of polypeptide recognition by export chaperones in flagellar biosynthesis and type III secretion. Nat Struct Biol 10(10):789–793. https://doi.org/10.1038/nsb982
Fabiani FD, Renault TT, Peters B, Dietsche T, Galvez EJC, Guse A, Freier K, Charpentier E, Strowig T, Franz-Wachtel M, Macek B, Wagner S, Hensel M, Erhardt M (2017) A flagellum-specific chaperone facilitates assembly of the core type III export apparatus of the bacterial flagellum. PLoS Biol 15(8):e2002267. https://doi.org/10.1371/journal.pbio.2002267
Fan F, Macnab RM (1996) Enzymatic characterization of FliI—an ATPase involved in flagellar assembly in Salmonella typhimurium. J Biol Chem 271(50):31981–31988
Fang X, Gomelsky M (2010) A post-translational, c-di-GMP-dependent mechanism regulating flagellar motility. Mol Microbiol 76(5):1295–1305. https://doi.org/10.1111/j.1365-2958.2010.07179.x
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):1043–1057. https://doi.org/10.1046/j.1365-2958.2003.03487.x
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):1485–1493. https://doi.org/10.1016/j.str.2009.08.017
Fujii T, Kato T, Hiraoka KD, Miyata T, Minamino T, Chevance FF, Hughes KT, Namba K (2017) Identical folds used for distinct mechanical functions of the bacterial flagellar rod and hook. Nat Commun 8:14276. https://doi.org/10.1038/ncomms14276
Fukumura T, Makino F, Dietsche T, Kinoshita M, Kato T, Wagner S, Namba K, Imada K, Minamino T (2017) Assembly and stoichiometry of the core structure of the bacterial flagellar type III export gate complex. PLoS Biol 15(8):e2002281. https://doi.org/10.1371/journal.pbio.2002281
Fukuoka H, Wada T, Kojima S, Ishijima A, Homma M (2009) Sodium-dependent dynamic assembly of membrane complexes in sodium-driven flagellar motors. Mol Microbiol 71(4):825–835. https://doi.org/10.1111/j.1365-2958.2008.06569.x
Fukuoka H, Inoue Y, Terasawa S, Takahashi H, Ishijima A (2010) Exchange of rotor components in functioning bacterial flagellar motor. Biochem Biophys Res Commun 394(1):130–135. https://doi.org/10.1016/j.bbrc.2010.02.129
Furukawa Y, Imada K, Vonderviszt F, Matsunami H, Sano K, Kutsukake K, Namba K (2002) Interactions between bacterial flagellar axial proteins in their monomeric state in solution. J Mol Biol 318(3):889–900. https://doi.org/10.1016/S0022-2836(02)00139-0
Furukawa Y, Inoue Y, Sakaguchi A, Mori Y, Fukumura T, Miyata T, Namba K, Minamino T (2016) Structural stability of flagellin subunit affects the rate of flagellin export in the absence of FliS chaperone. Mol Microbiol 102(3):405–416. https://doi.org/10.1111/mmi.13469
Galán JE, Lara-Tejero M, Marlovits TC, Wagner S (2014) Bacterial type III secretion systems: specialized nanomachines for protein delivery into target cells. Annu Rev Microbiol 68:415–438. https://doi.org/10.1146/annurev-micro-092412-155725
Gillen KL, Hughes KT (1991) Negative regulatory loci coupling flagellin synthesis to flagellar assembly in Salmonella typhimurium. J Bacteriol 173(7):2301–2310. https://doi.org/10.1128/jb.173.7.2301-2310.1991
Gonzalez-Pedrajo B, Minamino T, Kihara M, Namba K (2006) Interactions between C ring proteins and export apparatus components: a possible mechanism for facilitating type III protein export. Mol Microbiol 60(4):984–998. https://doi.org/10.1016/j.1365-2958.2006.05149.x
Hara N, Morimoto YV, Kawamoto A, Namba K, Minamino T (2012) Interaction of the extreme N-terminal region of FliH with FlhA is required for efficient bacterial flagellar protein export. J Bacteriol 194(19):5353–5360. https://doi.org/10.1128/JB.01028-12
Hirano T, Mizuno S, Aizawa S, Hughes KT (2009) Mutations in flk, flgG, flhA, and flhE that affect the flagellar type III secretion specificity switch in Salmonella enterica. J Bacteriol 191(12):3938–3949. https://doi.org/10.1128/JB.01811-08
Hiraoka KD, Morimoto YV, Inoue Y, Fujii T, Miyata T, Makino F, Minamino T, Namba K (2017) Straight and rigid flagellar hook made by insertion of the FlgG specific sequence into FlgE. Sci Rep 7:46723. https://doi.org/10.1038/srep46723
Hizukuri Y, Kojima S, Homma M (2010) Disulphide cross-linking between the stator and the bearing components in the bacterial flagellar motor. J Biochem 148(3):309–318. https://doi.org/10.1093/jb/mvq067
Homma M, Iino T (1985) Locations of hook-associated proteins in flagellar structures of Salmonella typhimurium. J Bacteriol 162(1):183–189
Homma M, Fujita H, Yamaguchi S, Iino T (1984) Excretion of unassembled flagellin by Salmonella typhimurium mutants deficient in hook-associated proteins. J Bacteriol 159(3):1056–1059
Horvath P, Kato T, Miyata T, Namba K (2019) Structure of Salmonella flagellar hook reveals intermolecular domain interactions for the universal joint function. Biomolecules 9(9):462. https://doi.org/10.3390/biom9090462
Hosking ER, Vogt C, Bakker EP, Manson MD (2006) The Escherichia coli MotAB proton channel unplugged. J Mol Biol 364(5):921–937. https://doi.org/10.1016/j.jmb.2006.09.035
Ibuki T, Imada K, Minamino T, Kato T, Miyata T, Namba K (2011) Common architecture of the flagellar type III protein export apparatus and F- and V-type ATPases. Nat Struct Mol Biol 18(3):277–282. https://doi.org/10.1038/nsmb.1977
Ibuki T, Uchida Y, Hironaka Y, Namba K, Imada K, Minamino T (2013) Interaction between FliJ and FlhA, components of the bacterial flagellar type III export apparatus. J Bacteriol 195(3):466–473. https://doi.org/10.1128/JB.01711-12
Ikeda T, Asakura S, Kamiya R (1985) “Cap” on the tip of Salmonella flagella. J Mol Biol 184(4):735–737. https://doi.org/10.1016/0022-2836(85)90317-1
Ikeda T, Oosawa K, Hotani H (1996) Self-assembly of the filament capping protein, FliD, of bacterial flagella into an annular structure. J Mol Biol 259(4):679–686. https://doi.org/10.1006/jmbi.1996.0349
Imada K, Minamino T, Tahara A, Namba K (2007) Structural similarity between the flagellar type III ATPase FliI and F1-ATPase subunits. Proc Natl Acad Sci USA 104(2):485–490. https://doi.org/10.1073/pnas.0608090104
Imada K, Minamino T, Kinoshita M, Furukawa Y, Namba K (2010) Structural insight into the regulatory mechanisms of interactions of the flagellar type III chaperone FliT with its binding partners. Proc Natl Acad Sci USA 107(19):8812–8817. https://doi.org/10.1073/pnas.1001866107
Imada K, Minamino T, Uchida Y, Kinoshita M, Namba K (2016) Insight into the flagella type III export revealed by the complex structure of the type III ATPase and its regulator. Proc Natl Acad Sci USA 113(13):3633–3638. https://doi.org/10.1073/pnas.1524025113
Inoue Y, Morimoto YV, Namba K, Minamino T (2018) Novel insights into the mechanism of well-ordered assembly of bacterial flagellar proteins in Salmonella. Sci Rep 8(1):1787. https://doi.org/10.1038/s41598-018-20209-3
Inoue Y, Ogawa Y, Kinoshita M, Terahara N, Shimada M, Kodera N, Ando T, Namba K, Kitao A, Imada K, Minamino T (2019) Structural insights into the substrate specificity switch mechanism of the type III protein export apparatus. Structure 27(6):965-976.e6. https://doi.org/10.1016/j.str.2019.03.017
Johnson S, Fong YH, Deme J, Furlong E, Kuhlen L, Lea SM (2020) Symmetry mismatch in the MS-ring of the bacterial flagellar rotor explains the structural coordination of secretion and rotation. Nat Microbiol 5(7): 966–975. https://doi.org/10.1038/s41564-020-0703-3.
Kato T, Makino F, Miyata T, Horvath P, Namba K (2019) Structure of the native supercoiled flagellar hook as a universal joint. Nat Commun 10(1):5295. https://doi.org/10.1038/s41467-019-13252-9
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 3:3369. https://doi.org/10.1038/srep03369
Kihara M, Miller GU, Macnab RM (2000) Deletion analysis of the flagellar switch protein FliG of Salmonella. J Bacteriol 182(11):3022–3028. https://doi.org/10.1128/jb.182.11.3022-3028.2000
Kihara M, Minamino T, Yamaguchi S, Macnab RM (2001) Intergenic suppression between the flagellar MS ring protein FliF of Salmonella and FlhA, a membrane component of its export apparatus. J Bacteriol 183(5):1655–1662. https://doi.org/10.1128/jb.183.5.1655-1662.2001
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):11332–11339. https://doi.org/10.1021/bi801347a
Kim EA, Panushka J, Meyer T, Carlisle R, Baker S, Ide N, Lynch M, Crane BR, Blair DF (2017) Architecture of the flagellar switch complex of Escherichia coli: conformational plasticity of FliG and implications for adaptive remodeling. J Mol Biol 429(9):1305–1320. https://doi.org/10.1016/j.jmb.2017.02.014
Kinoshita M, Hara N, Imada K, Namba K, Minamino T (2013) Interactions of bacterial flagellar chaperone-substrate complexes with FlhA contribute to co-ordinating assembly of the flagellar filament. Mol Microbiol 90(6):1249–1261. https://doi.org/10.1111/mmi.12430
Kinoshita M, Nakanishi Y, Furukawa Y, Namba K, Imada K, Minamino T (2016) Rearrangements of alpha-helical structures of FlgN chaperone control the binding affinity for its cognate substrates during flagellar type III export. Mol Microbiol 101(4):656–670. https://doi.org/10.1111/mmi.13415
Kinoshita M, Furukawa Y, Uchiyama S, Imada K, Namba K, Minamino T (2018a) Insight into adaptive remodeling of the rotor ring complex of the bacterial flagellar motor. Biochem Biophys Res Commun 496(1):12–17. https://doi.org/10.1016/j.bbrc.2017.12.118
Kinoshita M, Namba K, Minamino T (2018b) Effect of a clockwise-locked deletion in FliG on the FliG ring structure of the bacterial flagellar motor. Genes Cells 23(3):241–247. https://doi.org/10.1111/gtc.12565
Kojima S, Blair DF (2001) Conformational change in the stator of the bacterial flagellar motor. Biochemistry 40(43):13041–13050. https://doi.org/10.1021/bi011263o
Kojima S, Blair DF (2004) Solubilization and purification of the MotA/MotB complex of Escherichia coli. Biochemistry 43(1):26–34. https://doi.org/10.1021/bi035405l
Kojima S, Furukawa Y, Matsunami H, Minamino T, Namba K (2008) Characterization of the periplasmic domain of MotB and implications for its role in the stator assembly of the bacterial flagellar motor. J Bacteriol 190(9):3314–3322. https://doi.org/10.1128/JB.01710-07
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):710–718. https://doi.org/10.1111/j.1365-2958.2009.06802.x
Kojima S, Takao M, Almira G, Kawahara I, Sakuma M, Homma M, Kojima C, Imada K (2018) The helix rearrangement in the periplasmic domain of the flagellar stator B subunit activates peptidoglycan binding and ion influx. Structure 26(4):590–598, e595. https://doi.org/10.1016/j.str.2018.02.016
Ko W, Lim S, Lee W, Kim Y, Berg HC, Peskin CS (2017) Modeling polymorphic transformation of rotating bacterial flagella in a viscous fluid. Phys Rev E 95(6–1):063106. https://doi.org/10.1103/PhysRevE.95.063106
Kuhlen L, Abrusci P, Johnson S, Gault J, Deme J, Caesar J, Dietsche T, Mebrhatu MT, Ganief T, Macek B, Wagner S, Robinson CV, Lea SM (2018) Structure of the core of the type III secretion system export apparatus. Nat Struct Mol Biol 25(7):583–590. https://doi.org/10.1038/s41594-018-0086-9
Kuhlen L, Johnson S, Zeitler A, Bäurle S, Deme JC, Debo R, Fisher J, Wagner S, Lea SM (2019) The flagellar substrate specificity switch protein FlhB assembles onto the extra-membrane export gate to regulate type three secretion. bioRxiv:686782. https://doi.org/10.1101/686782
Lam KH, Ip WS, Lam YW, Chan SO, Ling TKW, Au SWN (2012) Multiple conformations of the FliG C-terminal domain provide insight into flagellar motor switching. Structure 20(2):315–325. https://doi.org/10.1016/j.str.2011.11.020
Lam KH, Lam WW, Wong JY, Chan LC, Kotaka M, Ling TK, Jin DY, Ottemann KM, Au SW (2013) Structural basis of FliG-FliM interaction in Helicobacter pylori. Mol Microbiol 88(4):798–812. https://doi.org/10.1111/mmi.12222
Larsen SH, Adler J, Gargus JJ, Hogg RW (1974) Chemomechanical coupling without ATP: the source of energy for motility and chemotaxis in bacteria. Proc Natl Acad Sci USA 71(4):1239–1243. https://doi.org/10.1073/pnas.71.4.1239
Leake MC, Chandler JH, Wadhams GH, Bai F, Berry RM, Armitage JP (2006) Stoichiometry and turnover in single, functioning membrane protein complexes. Nature 443(7109):355–358. https://doi.org/10.1038/nature05135
Lee J, Monzingo AF, Keatinge-Clay AT, Harshey RM (2015) Structure of Salmonella FlhE, conserved member of a flagellar type III secretion operon. J Mol Biol 427(6):1254–1262. https://doi.org/10.1016/j.jmb.2014.11.022
Lele PP, Branch RW, Nathan VS, Berg HC (2012) Mechanism for adaptive remodeling of the bacterial flagellar switch. Proc Natl Acad Sci USA 109(49):20018–20022. https://doi.org/10.1073/pnas.1212327109
Lele PP, Hosu BG, Berg HC (2013) Dynamics of mechanosensing in the bacterial flagellar motor. Proc Natl Acad Sci USA 110(29):11839–11844. https://doi.org/10.1073/pnas.1305885110
Levenson R, Zhou H, Dahlquist FW (2012) Structural insights into the interaction between the bacterial flagellar motor proteins FliF and FliG. Biochemistry 51(25):5052–5060. https://doi.org/10.1021/bi3004582
Macnab RM (2003) How bacteria assemble flagella. Annu Rev Microbiol 57:77–100. https://doi.org/10.1146/annurev.micro.57.030502.090832
Maki-Yonekura S, Yonekura K, Namba K (2003) Domain movements of HAP2 in the cap-filament complex formation and growth process of the bacterial flagellum. Proc Natl Acad Sci USA 100(26):15528–15533. https://doi.org/10.1073/pnas.2534343100
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):417–422. https://doi.org/10.1038/nsmb.1774
Manson MD, Tedesco P, Berg HC, Harold FM, Van der Drift C (1977) A protonmotive force drives bacterial flagella. Proc Natl Acad Sci USA 74(7):3060–3064. https://doi.org/10.1073/pnas.74.7.3060
Minamino T (2014) Protein export through the bacterial flagellar type III export pathway. Biochim Biophys Acta 1843(8):1642–1648. https://doi.org/10.1016/j.bbamcr.2013.09.005
Minamino T (2018) Hierarchical protein export mechanism of the bacterial flagellar type III protein export apparatus. FEMS Microbiol Lett 365(12):fny117. https://doi.org/10.1093/femsle/fny117
Minamino T, Namba K (2008) Distinct roles of the FliI ATPase and proton motive force in bacterial flagellar protein export. Nature 451(7177):485–488. https://doi.org/10.1038/nature06449
Minamino T, Macnab RM (2000a) Domain structure of Salmonella FlhB, a flagellar export component responsible for substrate specificity switching. J Bacteriol 182(17):4906–4914. https://doi.org/10.1128/jb.182.17.4906-4914.2000
Minamino T, Macnab RM (2000b) Interactions among components of the Salmonella flagellar export apparatus and its substrates. Mol Microbiol 35(5):1052–1064. https://doi.org/10.1046/j.1365-2958.2000.01771.x
Minamino T, Imada K (2015) The bacterial flagellar motor and its structural diversity. Trends Microbiol 23(5):267–274. https://doi.org/10.1016/j.tim.2014.12.011
Minamino T, Iino T, Kutuskake K (1994) Molecular characterization of the Salmonella typhimurium flhB operon and its protein products. J Bacteriol 176(24):7630–7637. https://doi.org/10.1128/jb.176.24.7630-7637.1994
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(11):3029–3036. https://doi.org/10.1128/jb.182.11.3029-3036.2000
Minamino T, Kazetani KI, Tahara A, Suzuki H, Furukawa Y, Kihara M, Namba K (2006) Oligomerization of the bacterial flagellar ATPase FliI is controlled by its extreme N-terminal region. J Mol Biol 360(2):510–519. https://doi.org/10.1016/j.jmb.2006.05.010
Minamino T, Yoshimura SD, Morimoto YV, Gonzalez-Pedrajo B, Kami-Ike N, Namba K (2009) Roles of the extreme N-terminal region of FliH for efficient localization of the FliH-FliI complex to the bacterial flagellar type III export apparatus. Mol Microbiol 74(6):1471–1483. https://doi.org/10.1111/j.1365-2958.2009.06946.x
Minamino T, Imada K, Namba K (2008) Molecular motors of the bacterial flagella. Curr Opin Struct Biol 18(6):693–701. https://doi.org/10.1016/j.sbi.2008.09.006
Minamino T, Shimada M, Okabe M, Saijo-Hamano Y, Imada K, Kihara M, Namba K (2010) Role of the C-terminal cytoplasmic domain of FlhA in bacterial flagellar type III protein export. J Bacteriol 192(7):1929–1936. https://doi.org/10.1128/JB.01328-09
Minamino T, Imada K, Kinoshita M, Nakamura S, Morimoto YV, Namba K (2011a) Structural insight into the rotational switching mechanism of the bacterial flagellar motor. PLoS Biol 9(5):12. https://doi.org/10.1371/journal.pbio.1000616
Minamino T, Morimoto YV, Hara N, Namba K (2011b) An energy transduction mechanism used in bacterial flagellar type III protein export. Nat Commun 2:475. https://doi.org/10.1038/ncomms1488
Minamino T, Kinoshita M, Hara N, Takeuchi S, Hida A, Koya S, Glenwright H, Imada K, Aldridge PD, Namba K (2012) Interaction of a bacterial flagellar chaperone FlgN with FlhA is required for efficient export of its cognate substrates. Mol Microbiol 83(4):775–788. https://doi.org/10.1111/j.1365-2958.2011.07964.x
Minamino T, Kinoshita M, Inoue Y, Morimoto YV, Ihara K, Koya S, Hara N, Nishioka N, Kojima S, Homma M, Namba K (2016a) FliH and FliI ensure efficient energy coupling of flagellar type III protein export in Salmonella. Microbiologyopen 5(3):424–435. https://doi.org/10.1002/mbo3.340
Minamino T, Morimoto YV, Hara N, Aldridge PD, Namba K (2016b) The bacterial flagellar type III export gate complex is a dual fuel engine that can use both H+ and Na+ for flagellar protein export. PLoS Pathog 12(3):e1005495. https://doi.org/10.1371/journal.ppat.1005495
Minamino T, Terahara N, Kojima S, Namba K (2018) Autonomous control mechanism of stator assembly in the bacterial flagellar motor in response to changes in the environment. Mol Microbiol 109(6):723–734. https://doi.org/10.1111/mmi.14092
Minamino T, Kawamoto A, Kinoshita M, Namba K (2020a) Molecular organization and assembly of the export apparatus of flagellar type III secretion systems. Curr Top Microbiol Immunol. 427: 91–107. https://doi.org/10.1007/82_2019_170
Minamino T, Inoue Y, Kinoshita M, Namba K (2020b) FliK-driven conformational rearrangements of FlhA and FlhB are required for export switching of the flagellar protein export apparatus. J Bacteriol 202(3): e00637-19. https://doi.org/10.1128/JB.00637-19
Miyanoiri Y, Hijikata A, Nishino Y, Gohara M, Onoue Y, Kojima S, Kojima C, Shirai T, Kainosho M, Homma M (2017) Structural and functional analysis of the C-terminal region of FliG, an essential motor component of Vibrio Na+-driven flagella. Structure 25(10):1540–1548, e1543. https://doi.org/10.1016/j.str.2017.08.010
Morimoto YV, Minamino T (2014) Structure and function of the bi-directional bacterial flagellar motor. Biomolecules 4(1):217–234. https://doi.org/10.3390/biom4010217
Morimoto YV, Che YS, Minamino T, Namba K (2010a) Proton-conductivity assay of plugged and unplugged MotA/B proton channel by cytoplasmic pHluorin expressed in Salmonella. FEBS Lett 584(6):1268–1272. https://doi.org/10.1016/j.febslet.2010.02.051
Morimoto YV, Nakamura S, Kami-ike N, Namba K, Minamino T (2010b) Charged residues in the cytoplasmic loop of MotA are required for stator assembly into the bacterial flagellar motor. Mol Microbiol 78(5):1117–1129. https://doi.org/10.1111/j.1365-2958.2010.07391.x
Morimoto YV, Nakamura S, Hiraoka KD, Namba K, Minamino T (2013) Distinct roles of highly conserved charged residues at the MotA-FliG interface in bacterial flagellar motor rotation. J Bacteriol 195(3):474–481. https://doi.org/10.1128/JB.01971-12
Morimoto YV, Ito M, Hiraoka KD, Che YS, Bai F, Kami-Ike N, Namba K, Minamino T (2014) Assembly and stoichiometry of FliF and FlhA in Salmonella flagellar basal body. Mol Microbiol 91(6):1214–1226. https://doi.org/10.1111/mmi.12529
Morimoto YV, Kami-Ike N, Miyata T, Kawamoto A, Kato T, Namba K, Minamino T (2016) High-resolution pH imaging of living bacterial cells to detect local pH differences. mBio 7(6). https://doi.org/10.1128/mBio.01911-16
Muramoto K, Macnab RM (1998) Deletion analysis of MotA and MotB, components of the force-generating unit in the flagellar motor of Salmonella. Mol Microbiol 29(5):1191–1202. https://doi.org/10.1046/j.1365-2958.1998.00998.x
Muskotal A, Seregelyes C, Sebestyen A, Vonderviszt F (2010) Structural basis for stabilization of the hypervariable D3 domain of Salmonella flagellin upon filament formation. J Mol Biol 403(4):607–615. https://doi.org/10.1016/j.jmb.2010.09.024
Nakamura S, Minamino T (2019) Flagella-driven motility of bacteria. Biomolecules 9(7):279. https://doi.org/10.3390/biom9070279
Nakamura S, Hanaizumi Y, Morimoto YV, Inoue Y, Erhardt M, Minamino T, Namba K (2019) Direct observation of speed fluctuations of flagellar motor rotation at extremely low load close to zero. Mol Microbiol 113 vhttps://doi.org/10.1111/mmi.14440
Namba K, Vonderviszt F (1997) Molecular architecture of bacterial flagellum. Q Rev Biophys 30(1):1–65. https://doi.org/10.1017/s0033583596003319
Okabe M, Minamino T, Imada K, Namba K, Kihara M (2009) Role of the N-terminal domain of FliI ATPase in bacterial flagellar protein export. FEBS Lett 583(4):743–748. https://doi.org/10.1016/j.febslet.2009.01.026
Paul K, Gonzalez-Bonet G, Bilwes AM, Crane BR, Blair D (2011) Architecture of the flagellar rotor. EMBO J 30(14):2962–2971. https://doi.org/10.1038/emboj.2011.188
Paul K, Erhardt M, Hirano T, Blair DF, Hughes KT (2008) Energy source of flagellar type III secretion. Nature 451(7177):489–492. https://doi.org/10.1038/nature06497
Paul K, Nieto V, Carlquist WC, Blair DF, Harshey RM (2010) The c-di-GMP binding protein YcgR controls flagellar motor direction and speed to affect chemotaxis by a “backstop brake” mechanism. Mol Cell 38(1):128–139. https://doi.org/10.1016/j.molcel.2010.03.001
Postel S, Deredge D, Bonsor DA, Yu X, Diederichs K, Helmsing S, Vromen A, Friedler A, Hust M, Egelman EH, Beckett D, Wintrode PL, Sundberg EJ (2016) Bacterial flagellar capping proteins adopt diverse oligomeric states. eLife 5:e18857. https://doi.org/10.7554/eLife.18857
Pourjaberi SNS, Terahara N, Namba K, Minamino T (2017) The role of a cytoplasmic loop of MotA in load-dependent assembly and disassembly dynamics of the MotA/B stator complex in the bacterial flagellar motor. Mol Microbiol 106(4):646–658. https://doi.org/10.1111/mmi.13843
Ravid S, Eisenbach M (1984) Minimal requirements for rotation of bacterial flagella. J Bacteriol 158(3):1208–1210
Reid SW, Leake MC, Chandler JH, Lo CJ, Armitage JP, Berry RM (2006) The maximum number of torque-generating units in the flagellar motor of Escherichia coli is at least 11. Proc Natl Acad Sci USA 103(21):8066–8071. https://doi.org/10.1073/pnas.0509932103
Saijo-Hamano Y, Uchida N, Namba K, Oosawa K (2004) In vitro characterization of FlgB, FlgC, FlgF, FlgG, and FliE, flagellar basal body proteins of Salmonella. J Mol Biol 339(2):423–435. https://doi.org/10.1016/j.jmb.2004.03.070
Saijo-Hamano Y, Matsunami H, Namba K, Imada K (2019) Architecture of the Bacterial Flagellar Distal Rod and Hook of Salmonella. Biomolecules 9(7):260. https://doi.org/10.3390/biom9070260
Sakai T, Inoue Y, Terahara N, Namba K, Minamino T (2018) A triangular loop of domain D1 of FlgE is essential for hook assembly but not for the mechanical function. Biochem Biophys Res Commun 495(2):1789–1794. https://doi.org/10.1016/j.bbrc.2017.12.037
Sakai T, Miyata T, Terahara N, Mori K, Inoue Y, Morimoto YV, Kato T, Namba K, Minamino T (2019) Novel insights into conformational rearrangements of the bacterial flagellar switch complex. mBio 10(2):e00079–19. https://doi.org/10.1128/mBio.00079-19
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):331–337. https://doi.org/10.1038/35066504
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):1062–1068. https://doi.org/10.1038/nature02997
Sarkar MK, Paul K, Blair D (2010) Chemotaxis signaling protein CheY binds to the rotor protein FliN to control the direction of flagellar rotation in Escherichia coli. Proc Natl Acad Sci USA 107(20):9370–9375. https://doi.org/10.1073/pnas.1000935107
Shibata S, Matsunami H, Aizawa SI, Wolf M (2019) Torque transmission mechanism of the curved bacterial flagellar hook revealed by cryo-EM. Nat Struct Mol Biol 26(10):941–945. https://doi.org/10.1038/s41594-019-0301-3
Song WS, Cho SY, Hong HJ, Park SC, Yoon SI (2017) Self-oligomerizing structure of the flagellarcap protein FliD and its implication in filament assembly. J Mol Biol 429(6):847–857. https://doi.org/10.1016/j.jmb.2017.02.001
Stocker BAD (1949) Measurement of the rate of mutation of flagellar antigenic phase in Salmonella typhimurium. J Hyg 47:398–413
Suzuki H, Yonekura K, Namba K (2004) Structure of the rotor of the bacterial flagellar motor revealed by electron cryomicroscopy and single-particle image analysis. J Mol Biol 337(1):105–113. https://doi.org/10.1016/j.jmb.2004.01.034
Suzuki Y, Morimoto YV, Oono K, Hayashi F, Oosawa K, Kudo S, Nakamura S (2019) Effect of the MotA(M206I) mutation on torque generation and stator assembly in the Salmonella H+-driven flagellar motor. J Bacteriol 201(6):e00727-e818. https://doi.org/10.1128/JB.00727-18
Takekawa N, Terahara N, Kato T, Gohara M, Mayanagi K, Hijikata A, Onoue Y, Kojima S, Shirai T, Namba K, Homma M (2016) The tetrameric MotA complex as the core of the flagellar motor stator from hyperthermophilic bacterium. Sci Rep 6:31526. https://doi.org/10.1038/srep31526
Terahara N, Kodera N, Uchihashi T, Ando T, Namba K, Minamino T (2017a) Na+-induced structural transition of MotPS for stator assembly of the Bacillus flagellar motor. Sci Adv 3(11):eaao4119. https://doi.org/10.1126/sciadv.aao4119
Terahara N, Noguchi Y, Nakamura S, Kami-Ike N, Ito M, Namba K, Minamino T (2017b) Load- and polysaccharide-dependent activation of the Na+-type MotPS stator in the Bacillus subtilis flagellar motor. Sci Rep 7:46081. https://doi.org/10.1038/srep46081
Terahara N, Inoue Y, Kodera N, Morimoto YV, Uchihashi T, Imada K, Ando T, Namba K, Minamino T (2018) Insight into structural remodeling of the FlhA ring responsible for bacterial flagellar type III protein export. Sci Adv 4(4):eaao7054. https://doi.org/10.1126/sciadv.aao7054
Thomas J, Stafford GP, Hughes C (2004) Docking of cytosolic chaperone-substrate complexes at the membrane ATPase during flagellar type III protein export. Proc Natl Acad Sci USA 101(11):3945–3950. https://doi.org/10.1073/pnas.0307223101
Tipping MJ, Delalez NJ, Lim R, Berry RM, Armitage JP (2013) Load-dependent assembly of the bacterial flagellar motor. mBio 4(4). https://doi.org/10.1128/mBio.00551-13
Ueno T, Oosawa K, Aizawa S (1992) M ring, S ring and proximal rod of the flagellar basal body of Salmonella typhimurium are composed of subunits of a single protein, FliF. J Mol Biol 227(3):672–677. https://doi.org/10.1016/0022-2836(92)90216-7
Vartanian AS, Paz A, Fortgang EA, Abramson J, Dahlquist FW (2012) Structure of flagellar motor proteins in complex allows for insights into motor structure and switching. J Biol Chem 287(43):35779–35783. https://doi.org/10.1074/jbc.C112.378380
Yamaguchi S, Aizawa S, Kihara M, Isomura M, Jones CJ, Macnab RM (1986) Genetic evidence for a switching and energy-transducing complex in the flagellar motor of Salmonella typhimurium. J Bacteriol 168(3):1172–1179. https://doi.org/10.1128/jb.168.3.1172-1179.1986
Yamaguchi T, Toma S, Terahara N, Miyata T, Ashihara M, Minamino T, Namba K, Kato T (2020) Structural and functional comparison of Salmonella flagellar filaments composed of FljB and FliC. Biomolecules 10(2):246. https://doi.org/10.3390/biom10020246
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):2148–2152. https://doi.org/10.1126/science.290.5499.2148
Yonekura K, Maki-Yonekura S, Namba K (2003) Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424(6949):643–650. https://doi.org/10.1038/nature01830
Yuan J, Berg HC (2008) Resurrection of the flagellar rotary motor near zero load. Proc Natl Acad Sci USA 105(4):1182–1185. https://doi.org/10.1073/pnas.0711539105
Zhou J, Fazzio RT, Blair DF (1995) Membrane topology of the MotA protein of Escherichia coli. J Mol Biol 251(2):237–242. https://doi.org/10.1006/jmbi.1995.0431
Zhou J, Lloyd SA, Blair DF (1998a) Electrostatic interactions between rotor and stator in the bacterial flagellar motor. Proc Natl Acad Sci USA 95(11):6436–6441. https://doi.org/10.1073/pnas.95.11.6436
Zhou J, Sharp LL, Tang HL, Lloyd SA, Billings S, Braun TF, Blair DF (1998b) Function of protonatable residues in the flagellar motor of Escherichia coli: a critical role for Asp 32 of MotB. J Bacteriol 180(10):2729–2735
Acknowledgements
We acknowledge Profs. Keiichi Namba and Takuo Yasunaga for continuous support and encouragement. Our research is supported in part by the Japan Society for Promotion and Science.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2021 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Morimoto, Y.V., Minamino, T. (2021). Architecture and Assembly of the Bacterial Flagellar Motor Complex. In: Harris, J.R., Marles-Wright, J. (eds) Macromolecular Protein Complexes III: Structure and Function. Subcellular Biochemistry, vol 96. Springer, Cham. https://doi.org/10.1007/978-3-030-58971-4_8
Download citation
DOI: https://doi.org/10.1007/978-3-030-58971-4_8
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-58970-7
Online ISBN: 978-3-030-58971-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)