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Abstract

Two of the most fascinating bacterial nanomachines—the broadly disseminated rotary flagellum at the heart of cellular motility and the eukaryotic cell–puncturing injectisome essential to specific pathogenic species—utilize at their core a conserved export machinery called the type III secretion system (T3SS). The T3SS not only secretes the components that self-assemble into their extracellular appendages but also, in the case of the injectisome, subsequently directly translocates modulating effector proteins from the bacterial cell into the infected host. The injectisome is thought to have evolved from the flagellum as a minimal secretory system lacking motility, with the subsequent acquisition of additional components tailored to its specialized role in manipulating eukaryotic hosts for pathogenic advantage. Both nanomachines have long been the focus of intense interest, but advances in structural and functional understanding have taken a significant step forward since 2015, facilitated by the revolutionary advances in cryo-electron microscopy technologies. With several seminal structures of each nanomachine now captured, we review here the molecular similarities and differences that underlie their diverse functions.

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2023-09-15
2024-04-23
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Literature Cited

  1. 1.
    Abby SS, Rocha EPC. 2012. The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems. PLOS Genet. 8:e1002983
    [Google Scholar]
  2. 2.
    Abrusci P, Vergara-Irigaray M, Johnson S, Beeby MD, Hendrixson DR et al. 2013. Architecture of the major component of the type III secretion system export apparatus. Nat. Struct. Mol. Biol. 20:99–104
    [Google Scholar]
  3. 3.
    Akeda Y, Galán JE. 2005. Chaperone release and unfolding of substrates in type III secretion. Nature 437:911–15
    [Google Scholar]
  4. 4.
    Al-Otaibi NS, Taylor AJ, Farrell DP, Tzokov SB, DiMaio F et al. 2020. The cryo-EM structure of the bacterial flagellum cap complex suggests a molecular mechanism for filament elongation. Nat. Commun. 11:3210
    [Google Scholar]
  5. 5.
    Barta ML, Dickenson NE, Patil M, Keightley A, Wyckoff GJ et al. 2012. The structures of coiled-coil domains from type III secretion system translocators reveal homology to pore-forming toxins. J. Mol. Biol. 417:395–405
    [Google Scholar]
  6. 6.
    Bastedo DP, Lo T, Laflamme B, Desveaux D, Guttman DS. 2020. Diversity and evolution of type III secreted effectors: a case study of three families. Curr. Top. Microbiol. Immunol. 427:201–30
    [Google Scholar]
  7. 7.
    Beeby M, Ribardo DA, Brennan CA, Ruby EG, Jensen GJ, Hendrixson DR. 2016. Diverse high-torque bacterial flagellar motors assemble wider stator rings using a conserved protein scaffold. PNAS 113:E1917–26
    [Google Scholar]
  8. 8.
    Berger C, Ravelli RBG, López-Iglesias C, Kudryashev M, Diepold A, Peters PJ. 2021. Structure of the Yersinia injectisome in intracellular host cell phagosomes revealed by cryo FIB electron tomography. J. Struct. Biol. 213:107701
    [Google Scholar]
  9. 9.
    Bergeron JR. 2016. Structural modeling of the flagellum MS ring protein FliF reveals similarities to the type III secretion system and sporulation complex. PeerJ 4:e1718
    [Google Scholar]
  10. 10.
    Bergeron JRC, Worrall LJ, De S, Sgourakis NG, Cheung AH et al. 2015. The modular structure of the inner-membrane ring component PrgK facilitates assembly of the type III secretion system basal body. Structure 23:161–72
    [Google Scholar]
  11. 11.
    Bergeron JRC, Worrall LJ, Sgourakis NG, DiMaio F, Pfuetzner RA et al. 2013. A refined model of the prototypical Salmonella SPI-1 T3SS basal body reveals the molecular basis for its assembly. PLOS Pathog. 9:e1003307
    [Google Scholar]
  12. 12.
    Bernal I, Bornicke J, Heidemann J, Svergun D, Horstmann JA et al. 2019. Molecular organization of soluble type III secretion system sorting platform complexes. J. Mol. Biol. 431:3787–803
    [Google Scholar]
  13. 13.
    Burkinshaw BJ, Deng WY, Lameignère E, Wasney GA, Zhu HZ et al. 2015. Structural analysis of a specialized type III secretion system peptidoglycan-cleaving enzyme. J. Biol. Chem. 290:10406–17
    [Google Scholar]
  14. 14.
    Butan C, Lara-Tejero M, Li WW, Liu J, Galán JE. 2019. High-resolution view of the type III secretion export apparatus in situ reveals membrane remodeling and a secretion pathway. PNAS 116:24786–95
    [Google Scholar]
  15. 15.
    Calladine CR, Luisi BF, Pratap JV. 2013. A “mechanistic” explanation of the multiple helical forms adopted by bacterial flagellar filaments. J. Mol. Biol. 425:914–28
    [Google Scholar]
  16. 16.
    Carroll BL, Liu J. 2020. Structural conservation and adaptation of the bacterial flagella motor. Biomolecules 10:1492
    [Google Scholar]
  17. 17.
    Chaban B, Coleman I, Beeby M. 2018. Evolution of higher torque in Campylobacter-type bacterial flagellar motors. Sci. Rep. 8:97
    [Google Scholar]
  18. 18.
    Chaban B, Hughes HV, Beeby M. 2015. The flagellum in bacterial pathogens: for motility and a whole lot more. Semin. Cell Dev. Biol. 46:91–103
    [Google Scholar]
  19. 19.
    Claret L, Calder SR, Higgins M, Hughes C. 2003. Oligomerization and activation of the FliI ATPase central to bacterial flagellum assembly. Mol. Microbiol. 48:1349–55
    [Google Scholar]
  20. 20.
    Deme JC, Johnson S, Vickery O, Aron A, Monkhouse H et al. 2020. Structures of the stator complex that drives rotation of the bacterial flagellum. Nat. Microbiol. 5:1553–64
    [Google Scholar]
  21. 21.
    Deng WY, Li YL, Hardwidge PR, Frey EA, Pfuetzner RA et al. 2005. Regulation of type III secretion hierarchy of translocators and effectors in attaching and effacing bacterial pathogens. Infect. Immun. 73:2135–46
    [Google Scholar]
  22. 22.
    Deng WY, Marshall NC, Rowland JL, McCoy JM, Worrall LJ et al. 2017. Assembly, structure, function and regulation of type III secretion systems. Nat. Rev. Microbiol. 15:323–37
    [Google Scholar]
  23. 23.
    Díaz-Guerrero M, Gaytán MO, Soto E, Espinosa N, García-Gómez E et al. 2021. CesL regulates type III secretion substrate specificity of the enteropathogenic E. coli injectisome. Microorganisms 9:1047
    [Google Scholar]
  24. 24.
    Diepold A, Kudryashev M, Delalez NJ, Berry RM, Armitage JP. 2015. Composition, formation, and regulation of the cytosolic C-ring, a dynamic component of the type III secretion injectisome. PLOS Biol. 13:e1002039
    [Google Scholar]
  25. 25.
    Diepold A, Sezgin E, Huseyin M, Mortimer T, Eggeling C, Armitage JP. 2017. A dynamic and adaptive network of cytosolic interactions governs protein export by the T3SS injectisome. Nat. Commun. 8:15940
    [Google Scholar]
  26. 26.
    Dunstan RA, Hay ID, Wilksch JJ, Schittenhelm RB, Purcell AW et al. 2015. Assembly of the secretion pores GspD, Wza and CsgG into bacterial outer membranes does not require the Omp85 proteins BamA or TamA. Mol. Microbiol. 97:616–29
    [Google Scholar]
  27. 27.
    Enninga J, Mounier J, Sansonetti P, Van Nhieu GT. 2005. Secretion of type III effectors into host cells in real time. Nat. Methods 2:959–65
    [Google Scholar]
  28. 28.
    Erhardt M, Mertens ME, Fabiani FD, Hughes KT. 2014. ATPase-independent type-III protein secretion in Salmonella enterica. PLOS Genet. 10:e1004800
    [Google Scholar]
  29. 29.
    Erhardt M, Wheatley P, Kim EA, Hirano T, Zhang Y et al. 2017. Mechanism of type-III protein secretion: regulation of FlhA conformation by a functionally critical charged-residue cluster. Mol. Microbiol. 104:234–49
    [Google Scholar]
  30. 30.
    Ferris HU, Furukawa Y, Minamino T, Kroetz MB, Kihara M et al. 2005. FlhB regulates ordered export of flagellar components via autocleavage mechanism. J. Biol. Chem. 280:41236–42
    [Google Scholar]
  31. 31.
    Fessl T, Watkins D, Oatley P, Allen WJ, Corey RA et al. 2018. Dynamic action of the Sec machinery during initiation, protein translocation and termination. eLife 7:e35112
    [Google Scholar]
  32. 32.
    Galán JE. 2001. Salmonella interactions with host cells: type III secretion at work. Annu. Rev. Cell Dev. Biol. 17:53–86
    [Google Scholar]
  33. 33.
    Green ER, Mecsas J. 2016. Bacterial secretion systems: an overview. Microbiol. Spectr. 4: https://doi.org/10.1128/microbiolspec.VMBF-0012-2015
    [Crossref] [Google Scholar]
  34. 34.
    Guo EZ, Desrosiers DC, Zalesak J, Tolchard J, Berbon M et al. 2019. A polymorphic helix of a Salmonella needle protein relays signals defining distinct steps in type III secretion. PLOS Biol. 17:e3000351
    [Google Scholar]
  35. 35.
    Guo EZ, Galán JE. 2021. Cryo-EM structure of the needle filament tip complex of the Salmonella type III secretion injectisome. PNAS 118:e2114552118
    [Google Scholar]
  36. 36.
    Hu B, Lara-Tejero M, Kong QK, Galán JE, Liu J. 2017. In situ molecular architecture of the Salmonella type III secretion machine. Cell 168:1065–74.e10
    [Google Scholar]
  37. 37.
    Hu B, Morado DR, Margolin W, Rohde JR, Arizmendi O et al. 2015. Visualization of the type III secretion sorting platform of Shigella flexneri. PNAS 112:1047–52
    [Google Scholar]
  38. 38.
    Hu J, Worrall LJ, Hong C, Vuckovic M, Atkinson CE et al. 2018. Cryo-EM analysis of the T3S injectisome reveals the structure of the needle and open secretin. Nat. Commun. 9:3840
    [Google Scholar]
  39. 39.
    Hu J, Worrall LJ, Vuckovic M, Hong C, Deng W et al. 2019. T3S injectisome needle complex structures in four distinct states reveal the basis of membrane coupling and assembly. Nat. Microbiol. 4:2010–19
    [Google Scholar]
  40. 40.
    Hueck CJ. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379–433
    [Google Scholar]
  41. 41.
    Hüsing S, Halte M, van Look U, Guse A, Gálvez EJC et al. 2021. Control of membrane barrier during bacterial type-III protein secretion. Nat. Commun. 12:3999
    [Google Scholar]
  42. 42.
    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. 18:277–82
    [Google Scholar]
  43. 43.
    Ide T, Laarmann S, Greune L, Schillers H, Oberleithner H, Schmidt MA. 2001. Characterization of translocation pores inserted into plasma membranes by type III–secreted Esp proteins of enteropathogenic Escherichia coli. Cell Microbiol. 3:669–79
    [Google Scholar]
  44. 44.
    Iino T. 1974. Assembly of Salmonella flagellin in vitro and in vivo. J. Supramol. Struct. 2:372–84
    [Google Scholar]
  45. 45.
    Imada K, Minamino T, Tahara A, Namba K. 2007. Structural similarity between the flagellar type III ATPase FliI and F1-ATPase subunits. PNAS 104:485–90
    [Google Scholar]
  46. 46.
    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. PNAS 113:3633–38
    [Google Scholar]
  47. 47.
    Jensen JL, Yamini S, Rietsch A, Spiller BW. 2020. The structure of the type III secretion system export gate with CdsO, an ATPase lever arm. PLOS Pathog. 16:e1008923
    [Google Scholar]
  48. 48.
    Johnson S, Fong YH, Deme JC, Furlong EJ, 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. 5:966–75
    [Google Scholar]
  49. 49.
    Johnson S, Furlong EJ, Deme JC, Nord AL, Caesar JJE et al. 2021. Molecular structure of the intact bacterial flagellar basal body. Nat. Microbiol. 6:712–21
    [Google Scholar]
  50. 50.
    Johnson S, Kuhlen L, Deme JC, Abrusci P, Lea SM. 2019. The structure of an injectisome export gate demonstrates conservation of architecture in the core export gate between flagellar and virulence type III secretion systems. mBio 10:e00818–19
    [Google Scholar]
  51. 51.
    Journet L, Agrain C, Broz P, Cornelis GR. 2003. The needle length of bacterial injectisomes is determined by a molecular ruler. Science 302:1757–60
    [Google Scholar]
  52. 52.
    Kaplan M, Sweredoski MJ, Rodrigues JPGL, Tocheva EI, Chang YW et al. 2020. Bacterial flagellar motor PL-ring disassembly subcomplexes are widespread and ancient. PNAS 117:8941–47
    [Google Scholar]
  53. 53.
    Kato T, Makino F, Miyata T, Horváth P, Namba K. 2019. Structure of the native supercoiled flagellar hook as a universal joint. Nat. Commun. 10:5295
    [Google Scholar]
  54. 54.
    Kawamoto A, Miyata T, Makino F, Kinoshita M, Minamino T et al. 2021. Native flagellar MS ring is formed by 34 subunits with 23-fold and 11-fold subsymmetries. Nat. Commun. 12:4223
    [Google Scholar]
  55. 55.
    Kenjale R, Wilson J, Zenk SF, Saurya S, Picking WL et al. 2005. The needle component of the type III secreton of Shigella regulates the activity of the secretion apparatus. J. Biol. Chem. 280:42929–37
    [Google Scholar]
  56. 56.
    Kojima S. 2015. Dynamism and regulation of the stator, the energy conversion complex of the bacterial flagellar motor. Curr. Opin. Microbiol. 28:66–71
    [Google Scholar]
  57. 57.
    Krissinel E, Henrick K. 2007. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372:774–97
    [Google Scholar]
  58. 58.
    Kucera J, Terentjev EM. 2020. FliI6-FliJ molecular motor assists with unfolding in the type III secretion export apparatus. Sci. Rep. 10:7127
    [Google Scholar]
  59. 59.
    Kuhlbrandt W. 2014. The resolution revolution. Science 343:1443–44
    [Google Scholar]
  60. 60.
    Kuhlen L, Abrusci P, Johnson S, Gault J, Deme J et al. 2018. Structure of the core of the type III secretion system export apparatus. Nat. Struct. Mol. Biol. 25:583–90
    [Google Scholar]
  61. 61.
    Kuhlen L, Johnson S, Cao J, Deme JC, Lea SM. 2021. Nonameric structures of the cytoplasmic domain of FlhA and SctV in the context of the full-length protein. PLOS ONE 16:e0252800
    [Google Scholar]
  62. 62.
    Kuhlen L, Johnson S, Zeitler A, Bäurle S, Deme JC et al. 2020. The substrate specificity switch FlhB assembles onto the export gate to regulate type three secretion. Nat. Commun. 11:1296
    [Google Scholar]
  63. 63.
    Lara-Tejero M, Kato J, Wagner S, Liu XY, Galán JE. 2011. A sorting platform determines the order of protein secretion in bacterial type III systems. Science 331:1188–91
    [Google Scholar]
  64. 64.
    Liu BW, Chan H, Bauda E, Contreras-Martel C, Bellard L et al. 2022. Structural insights into ring-building motif domains involved in bacterial sporulation. J. Struct. Biol. 214:107813
    [Google Scholar]
  65. 65.
    Liu G, Tarbet B, Song LZ, Reiserova L, Weaver B et al. 2011. Immunogenicity and efficacy of flagellin-fused vaccine candidates targeting 2009 pandemic H1N1 influenza in mice. PLOS ONE 6:e20928
    [Google Scholar]
  66. 66.
    Liu RY, Ochman H. 2007. Stepwise formation of the bacterial flagellar system. PNAS 104:7116–21
    [Google Scholar]
  67. 67.
    Lowe G, Meister M, Berg HC. 1987. Rapid rotation of flagellar bundles in swimming bacteria. Nature 325:637–40
    [Google Scholar]
  68. 68.
    Lunelli M, Kamprad A, Bürger J, Mielke T, Spahn CMT, Kolbe M. 2020. Cryo-EM structure of the Shigella type III needle complex. PLOS Pathog. 16:e1008263
    [Google Scholar]
  69. 69.
    Lynch MJ, Levenson R, Kim EA, Sircar R, Blair DF et al. 2017. Co-folding of a FliF-FliG split domain forms the basis of the MS:C ring interface within the bacterial flagellar motor. Structure 25:317–28
    [Google Scholar]
  70. 70.
    Lynch MJ, Miller M, James M, Zhang S, Zhang K et al. 2019. Structure and chemistry of lysinoalanine crosslinking in the spirochaete flagella hook. Nat. Chem. Biol. 15:959–65
    [Google Scholar]
  71. 71.
    Lyons BJE, Atkinson CE, Deng W, Serapio-Palacios A, Finlay BB, Strynadka NCJ. 2021. Cryo-EM structure of the EspA filament from enteropathogenic Escherichia coli: revealing the mechanism of effector translocation in the T3SS. Structure 29:479–87.e4
    [Google Scholar]
  72. 72.
    Magariyama Y, Sugiyama S, Kudo S. 2001. Bacterial swimming speed and rotation rate of bundled flagella. FEMS Microbiol. Lett. 199:125–29
    [Google Scholar]
  73. 73.
    Magariyama Y, Sugiyama S, Muramoto K, Kawagishi I, Imae Y, Kudo S. 1995. Simultaneous measurement of bacterial flagellar rotation rate and swimming speed. Biophys. J. 69:2154–62
    [Google Scholar]
  74. 74.
    Magariyama Y, Sugiyama S, Muramoto K, Maekawa Y, Kawagishi I et al. 1994. Very fast flagellar rotation. Nature 371:752
    [Google Scholar]
  75. 75.
    Majewski DD, Lyons BJE, Atkinson CE, Strynadka NCJ. 2020. Cryo-EM analysis of the SctV cytosolic domain from the enteropathogenic E. coli T3SS injectisome. J. Struct. Biol. 212:107660
    [Google Scholar]
  76. 76.
    Majewski DD, Okon M, Heinkel F, Robb CS, Vuckovic M et al. 2021. Characterization of the pilotin-secretin complex from the Salmonella enterica type III secretion system using hybrid structural methods. Structure 29:125–38.e5
    [Google Scholar]
  77. 77.
    Majewski DD, Worrall LJ, Hong C, Atkinson CE, Vuckovic M et al. 2019. Cryo-EM structure of the homohexameric T3SS ATPase-central stalk complex reveals rotary ATPase-like asymmetry. Nat. Commun. 10:626
    [Google Scholar]
  78. 78.
    Majewski DD, Worrall LJ, Strynadka NC. 2018. Secretins revealed: structural insights into the giant gated outer membrane portals of bacteria. Curr. Opin. Struct. Biol. 51:61–72
    [Google Scholar]
  79. 79.
    Maki-Yonekura S, Yonekura K, Namba K. 2010. Conformational change of flagellin for polymorphic supercoiling of the flagellar filament. Nat. Struct. Mol. Biol. 17:417–22
    [Google Scholar]
  80. 80.
    Mariano G, Faba-Rodriguez R, Bui S, Zhao WL, Ross J et al. 2022. Oligomerization of the FliF domains suggests a coordinated assembly of the bacterial flagellum MS ring. Front. Microbiol. 12:781960
    [Google Scholar]
  81. 81.
    Matthews-Palmer TRS, Gonzalez-Rodriguez N, Calcraft T, Lagercrantz S, Zachs T et al. 2021. Structure of the cytoplasmic domain of SctV (SsaV) from the Salmonella SPI-2 injectisome and implications for a pH sensing mechanism. J. Struct. Biol. 213:107729
    [Google Scholar]
  82. 82.
    Miletic S, Fahrenkamp D, Goessweiner-Mohr N, Wald J, Pantel M et al. 2021. Substrate-engaged type III secretion system structures reveal gating mechanism for unfolded protein translocation. Nat. Commun. 12:1546
    [Google Scholar]
  83. 83.
    Mills E, Baruch K, Charpentier X, Kobi S, Rosenshine I. 2008. Real-time analysis of effector translocation by the type III secretion system of enteropathogenic Escherichia coli. Cell Host Microbe 3:104–13
    [Google Scholar]
  84. 84.
    Minamino T, Kinoshita M, Namba K. 2022. Insight into distinct functional roles of the flagellar ATPase complex for flagellar assembly in Salmonella. Front. Microbiol. 13:864178
    [Google Scholar]
  85. 85.
    Minamino T, Morimoto YV, Hara N, Namba K. 2011. An energy transduction mechanism used in bacterial flagellar type III protein export. Nat. Commun. 2:475
    [Google Scholar]
  86. 86.
    Montemayor EJ, Ploscariu NT, Sanchez JC, Parrell D, Dillard RS et al. 2021. Flagellar structures from the bacterium Caulobacter crescentus and implications for phage ϕCbK predation of multi-flagellin bacteria. J. Bacteriol. 203:e00399–20
    [Google Scholar]
  87. 87.
    Nguyen VS, Jobichen C, Tan KW, Tan YW, Chan SL et al. 2015. Structure of AcrH-AopB chaperone-translocator complex reveals a role for membrane hairpins in type III secretion system translocon assembly. Structure 23:2022–31
    [Google Scholar]
  88. 88.
    Notti RQ, Bhattacharya S, Lilic M, Stebbins CE. 2015. A common assembly module in injectisome and flagellar type III secretion sorting platforms. Nat. Commun. 6:7125
    [Google Scholar]
  89. 89.
    Ohgita T, Hayashi N, Hama S, Tsuchiya H, Gotoh N, Kogure K. 2013. A novel effector secretion mechanism based on proton-motive force-dependent type III secretion apparatus rotation. FASEB J. 27:2862–72
    [Google Scholar]
  90. 90.
    Pallen MJ, Bailey CM, Beatson SA. 2006. 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. 15:935–41
    [Google Scholar]
  91. 91.
    Park D, Lara-Tejero M, Waxham MN, Li W, Hu B et al. 2018. Visualization of the type III secretion mediated Salmonella–host cell interface using cryo-electron tomography. eLife 7:e39514
    [Google Scholar]
  92. 92.
    Paul K, Erhardt M, Hirano T, Blair DF, Hughes KT. 2008. Energy source of flagellar type III secretion. Nature 451:489–92
    [Google Scholar]
  93. 93.
    Portaliou AG, Tsolis KC, Loos MS, Balabanidou V, Rayo J et al. 2017. Hierarchical protein targeting and secretion is controlled by an affinity switch in the type III secretion system of enteropathogenic Escherichia coli. EMBO J. 36:3517–31
    [Google Scholar]
  94. 94.
    Qin Z, Tu JG, Lin T, Norris SJ, Li C et al. 2018. Cryo-electron tomography of periplasmic flagella in Borrelia burgdorferi reveals a distinct cytoplasmic ATPase complex. PLOS Biol. 16:e3000050
    [Google Scholar]
  95. 95.
    Renault TT, Abraham AO, Bergmiller T, Paradis G, Rainville S et al. 2017. Bacterial flagella grow through an injection-diffusion mechanism. eLife 6:e23136
    [Google Scholar]
  96. 96.
    Rocha JM, Richardson CJ, Zhang MX, Darch CM, Cai E et al. 2018. Single-molecule tracking in live Yersinia enterocolitica reveals distinct cytosolic complexes of injectisome subunits. Integr. Biol. 10:502–15
    [Google Scholar]
  97. 97.
    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. PNAS 105:10348–53
    [Google Scholar]
  98. 98.
    Santiveri M, Roa-Eguiara A, Kühne C, Wadhwa N, Hu HD et al. 2020. Structure and function of stator units of the bacterial flagellar motor. Cell 183:244–257.e16
    [Google Scholar]
  99. 99.
    Schlumberger MC, Müller AJ, Ehrbar K, Winnen B, Duss I et al. 2005. Real-time imaging of type III secretion: Salmonella SipA injection into host cells. PNAS 102:12548–53
    [Google Scholar]
  100. 100.
    Shibata S, Takahashi N, Chevance FFV, Karlinsey JE, Hughes KT, Aizawa SI. 2007. FliK regulates flagellar hook length as an internal ruler. Mol. Microbiol. 64:1404–15
    [Google Scholar]
  101. 101.
    Silverman M, Zieg J, Simon M. 1979. Flagellar-phase variation:isolation of the rh1 gene. J. Bacteriol. 137:517–23
    [Google Scholar]
  102. 102.
    Spreter T, Yip CK, Sanowar S, André I, Kimbrough TG et al. 2009. A conserved structural motif mediates formation of the periplasmic rings in the type III secretion system. Nat. Struct. Mol. Biol. 16:468–76
    [Google Scholar]
  103. 103.
    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. 337:105–13
    [Google Scholar]
  104. 104.
    Takekawa N, Kawamoto A, Sakuma M, Kato T, Kojima S et al. 2021. Two distinct conformations in 34 FliF subunits generate three different symmetries within the flagellar MS-ring. mBio 12:e03199–20
    [Google Scholar]
  105. 105.
    Tan JX, Zhang X, Wang XF, Xu CH, Chang SH et al. 2021. Structural basis of assembly and torque transmission of the bacterial flagellar motor. Cell 184:2665–2679.e19
    [Google Scholar]
  106. 106.
    Taylor DN, Treanor JJ, Strout C, Johnson C, Fitzgerald T et al. 2011. Induction of a potent immune response in the elderly using the TLR-5 agonist, flagellin, with a recombinant hemagglutinin influenza-flagellin fusion vaccine (VAX125, STF2.HA1 SI). Vaccine 29:4897–902
    [Google Scholar]
  107. 107.
    Thiery S, Turowski P, Berleman JE, Kaimer C. 2022. The predatory soil bacterium Myxococcus xanthus combines a Tad- and an atypical type 3-like protein secretion system to kill bacterial cells. Cell Rep. 40:111340
    [Google Scholar]
  108. 108.
    Thomas DR, Francis NR, Xu C, DeRosier DJ. 2006. The three-dimensional structure of the flagellar rotor from a clockwise-locked mutant of Salmonella enterica serovar Typhimurium. J. Bacteriol. 188:7039–48
    [Google Scholar]
  109. 109.
    Torres-Vargas CE, Kronenberger T, Roos N, Dietsche T, Poso A, Wagner S. 2019. The inner rod of virulence-associated type III secretion systems constitutes a needle adapter of one helical turn that is deeply integrated into the system's export apparatus. Mol. Microbiol. 112:918–31
    [Google Scholar]
  110. 110.
    Troisfontaines P, Cornelis GR. 2005. Type III secretion: more systems than you think. Physiology 20:326–39
    [Google Scholar]
  111. 111.
    Veenendaal AKJ, Hodgkinson JL, Schwarzer L, Stabat D, Zenk SF, Blocker AJ. 2007. The type III secretion system needle tip complex mediates host cell sensing and translocon insertion. Mol. Microbiol. 63:1719–30
    [Google Scholar]
  112. 112.
    Wagner S, Diepold A. 2020. A unified nomenclature for injectisome-type type III secretion systems. Curr. Top. Microbiol. Immunol. 427:1–10
    [Google Scholar]
  113. 113.
    Wagner S, Königsmaier L, Lara-Tejero M, Lefebre M, Marlovits TC, Galán JE. 2010. Organization and coordinated assembly of the type III secretion export apparatus. PNAS 107:17745–50
    [Google Scholar]
  114. 114.
    Wilharm G, Lehmann V, Krauss K, Lehnert B, Richter S et al. 2004. Yersinia enterocolitica type III secretion depends on the proton motive force but not on the flagellar motor components MotA and MotB. Infect. Immun. 72:4004–9
    [Google Scholar]
  115. 115.
    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. 178:2960–70
    [Google Scholar]
  116. 116.
    Wimmi S, Balinovic A, Jeckel H, Selinger L, Lampaki D et al. 2021. Dynamic relocalization of cytosolic type III secretion system components prevents premature protein secretion at low external pH. Nat. Commun. 12:1625
    [Google Scholar]
  117. 117.
    Worrall LJ, Hong C, Vuckovic M, Deng W, Bergeron JRC et al. 2016. Near-atomic-resolution cryo-EM analysis of the Salmonella T3S injectisome basal body. Nature 540:597–601
    [Google Scholar]
  118. 118.
    Worrall LJ, Hu J, Strynadka NCJ. 2020. Aligning the symmetry of the type III secretion system needle complex. J. Chem. Inf. Model 60:2430–35
    [Google Scholar]
  119. 119.
    Xing Q, Shi K, Portaliou A, Rossi P, Economou A, Kalodimos CG. 2018. Structures of chaperone-substrate complexes docked onto the export gate in a type III secretion system. Nat. Commun. 9:1773
    [Google Scholar]
  120. 120.
    Yamaguchi T, Makino F, Miyata T, Minamino T, Kato T, Namba K. 2021. Structure of the molecular bushing of the bacterial flagellar motor. Nat. Commun. 12:4469
    [Google Scholar]
  121. 121.
    Yin M, Yan ZF, Li XM. 2018. Structural insight into the assembly of the type II secretion system pilotin-secretin complex from enterotoxigenic Escherichia coli. Nat. Microbiol. 3:581–87
    [Google Scholar]
  122. 122.
    Yonekura K, Maki-Yonekura S, Namba K. 2002. Growth mechanism of the bacterial flagellar filament. Res. Microbiol. 153:191–97
    [Google Scholar]
  123. 123.
    Yonekura K, Maki-Yonekura S, Namba K. 2003. Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature 424:643–50
    [Google Scholar]
  124. 124.
    Young HS, Dang HY, Lai YM, DeRosier DJ, Khan S. 2003. Variable symmetry in Salmonella typhimurium flagellar motors. Biophys. J. 84:571–77
    [Google Scholar]
  125. 125.
    Yuan B, Portaliou AG, Parakra R, Smit JH, Wald J et al. 2021. Structural dynamics of the functional nonameric type III translocase export gate. J. Mol. Biol. 433:167188
    [Google Scholar]
  126. 126.
    Zarivach R, Vuckovic M, Deng WY, Finlay BB, Strynadka NCJ. 2007. Structural analysis of a prototypical ATPase from the type III secretion system. Nat. Struct. Mol. Biol. 14:131–37
    [Google Scholar]
  127. 127.
    Zeytuni N, Hong C, Flanagan KA, Worrall LJ, Theiltges KA et al. 2017. Near-atomic resolution cryoelectron microscopy structure of the 30-fold homooligomeric SpoIIIAG channel essential to spore formation in Bacillus subtilis. PNAS 114:E7073–81
    [Google Scholar]
  128. 128.
    Zeytuni N, Strynadka NCJ. 2019. A hybrid secretion system facilitates bacterial sporulation: a structural perspective. Microbiol. Spectr. 7: https://doi.org/10.1128/microbiolspec.PSIB-0013-2018
    [Google Scholar]
  129. 129.
    Zhang YD, Lara-Tejero M, Bewersdorf J, Galán JE. 2017. Visualization and characterization of individual type III protein secretion machines in live bacteria. PNAS 114:6098–103
    [Google Scholar]
  130. 130.
    Zheng WL, Peña A, Ilangovan A, Clark JNB, Frankel G et al. 2021. Cryoelectron-microscopy structure of the enteropathogenic Escherichia coli type III secretion system EspA filament. PNAS 118:e2022826118
    [Google Scholar]
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