1887

Chapter 16 : Architecture and Assembly of Periplasmic Flagellum

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in
Zoomout

Architecture and Assembly of Periplasmic Flagellum, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781683670285/9781683670278_Chap16-1.gif /docserver/preview/fulltext/10.1128/9781683670285/9781683670278_Chap16-2.gif

Abstract:

The flagellum is a major organelle for motility in many bacterial species. It confers locomotion and is often associated with virulence of bacterial pathogens. Flagella from different species share a conserved core but also exhibit profound variations in flagellar structure, flagellar number, and placement ( ), resulting in distinct flagella that appear to be adapted to the specific environments that the bacteria encounter. While many bacteria possess multiple peritrichous flagella, such as those found in and , other bacteria, such as spp. and , normally have a single flagellum at one cell pole ( Fig. 1 ). Spirochetes uniquely assemble flagella that are embedded in periplasmic space between their inner and outer membranes, thus called periplasmic flagella ( ). Although the flagella of and have been extensively studied for several decades, periplasmic flagella are less understood, despite their profound impact on the distinctive morphology and motility of spirochetes. In this chapter, many aspects of periplasmic flagella are discussed, with particular focus on their structure and assembly.

Citation: Chang Y, Liu J. 2019. Architecture and Assembly of Periplasmic Flagellum, p 189-199. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0030-2019
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of Figure 1
Figure 1

Distinctive placement of bacterial flagellum. Bacteria with flagella distributed all over the cell (e.g., ) are peritrichous. Monotrichous bacteria, such as , , and , have a single flagellum present at one end of the cell. Spirochetes, including species of , , and , possess specialized flagella located within the periplasmic space. The rotation of the periplasmic flagella allows the bacterium to swim forward in a corkscrew-like motion.

Citation: Chang Y, Liu J. 2019. Architecture and Assembly of Periplasmic Flagellum, p 189-199. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0030-2019
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Comparison of motor structures from , , , and . A central section of an flagellar motor. A central section from a nonsheathed flagellar motor. A central section from a sheathed flagellar motor. A central section from a sheathed flagellar motor of . A central section from a flagellar motor. Schematic models derived from the central sections shown in panels A to E, respectively. Adapted from prior publications ( ), with permission.

Citation: Chang Y, Liu J. 2019. Architecture and Assembly of Periplasmic Flagellum, p 189-199. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0030-2019
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

Characterization of the unique features in periplasmic flagella, as examined through mutational analysis. Central section from a mutant lacking FlbB. Central section from a mutant lacking BB0236. Central section from a class average of a mutant lacking FliL. Central section from another class average of a mutant lacking FliL. A central section from wild-type flagellar motor. Schematic models derived from panels A to E, respectively. Adapted from a prior publication ( ), with permission.

Citation: Chang Y, Liu J. 2019. Architecture and Assembly of Periplasmic Flagellum, p 189-199. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0030-2019
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4
Figure 4

Comparison of the fT3SS from and the vT3SS from . A central section from the motor. The fT3SS in the spirochete motor includes the ATPase complex (orange) and the export apparatus (purple) underneath the MS ring. The vT3SS from the injectisome is modeled in a similar color scheme. The difference between the two T3SSs is striking in a comparison of the cross sections of their ATPase complexes. Note that the C ring from the motor is a continuous ring with ∼46 copies of FliN tetramer. There are 23 visible FliH spokes . There are six pods in the injectisome. Only six spokes of the FliH homolog OrgB connect the ATPase complex to the SpaO molecules that compose the pod of the injectisome. Adapted from a prior publication ( ), with permission.

Citation: Chang Y, Liu J. 2019. Architecture and Assembly of Periplasmic Flagellum, p 189-199. In Sandkvist M, Cascales E, Christie P (ed), Protein Secretion in Bacteria. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.PSIB-0030-2019
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781683670285.chap16
1. Chen S,, Beeby M,, Murphy GE,, Leadbetter JR,, Hendrixson DR,, Briegel A,, Li Z,, Shi J,, Tocheva EI,, Müller A,, Dobro MJ,, Jensen GJ . 2011. Structural diversity of bacterial flagellar motors. EMBO J 30 : 2972 2981.[CrossRef]
2. Zhao X,, Norris SJ,, Liu J . 2014. Molecular architecture of the bacterial flagellar motor in cells. Biochemistry 53 : 4323 4333.[CrossRef]
3. Charon NW,, Cockburn A,, Li C,, Liu J,, Miller KA,, Miller MR,, Motaleb MA,, Wolgemuth CW . 2012. The unique paradigm of spirochete motility and chemotaxis. Annu Rev Microbiol 66 : 349 370.[CrossRef]
4. Radolf JD,, Caimano MJ,, Stevenson B,, Hu LT . 2012. Of ticks, mice and men: understanding the dual-host lifestyle of Lyme disease spirochaetes. Nat Rev Microbiol 10 : 87 99.[CrossRef]
5. Sultan SZ,, Sekar P,, Zhao X,, Manne A,, Liu J,, Wooten RM,, Motaleb MA . 2015. Motor rotation is essential for the formation of the periplasmic flagellar ribbon, cellular morphology, and Borrelia burgdorferi persistence within Ixodes scapularis tick and murine hosts. Infect Immun 83 : 1765 1777.[CrossRef]
6. Motaleb MA,, Liu J,, Wooten RM . 2015. Spirochetal motility and chemotaxis in the natural enzootic cycle and development of Lyme disease. Curr Opin Microbiol 28 : 106 113.[CrossRef]
7. Li C,, Xu H,, Zhang K,, Liang FT . 2010. Inactivation of a putative flagellar motor switch protein FliG1 prevents Borrelia burgdorferi from swimming in highly viscous media and blocks its infectivity. Mol Microbiol 75 : 1563 1576.[CrossRef]
8. Sultan SZ,, Manne A,, Stewart PE,, Bestor A,, Rosa PA,, Charon NW,, Motaleb MA . 2013. Motility is crucial for the infectious life cycle of Borrelia burgdorferi. Infect Immun 81 : 2012 2021.[CrossRef]
9. Motaleb MA,, Corum L,, Bono JL,, Elias AF,, Rosa P,, Samuels DS,, Charon NW . 2000. Borrelia burgdorferi periplasmic flagella have both skeletal and motility functions. Proc Natl Acad Sci U S A 97 : 10899 10904.[CrossRef]
10. Moon KH,, Zhao X,, Manne A,, Wang J,, Yu Z,, Liu J,, Motaleb MA . 2016. Spirochetes flagellar collar protein FlbB has astounding effects in orientation of periplasmic flagella, bacterial shape, motility, and assembly of motors in Borrelia burgdorferi. Mol Microbiol 102 : 336 348.[CrossRef]
11. Kudryashev M,, Cyrklaff M,, Baumeister W,, Simon MM,, Wallich R,, Frischknecht F . 2009. Comparative cryo-electron tomography of pathogenic Lyme disease spirochetes. Mol Microbiol 71 : 1415 1434.[CrossRef]
12. Liu J,, Lin T,, Botkin DJ,, McCrum E,, Winkler H,, Norris SJ . 2009. Intact flagellar motor of Borrelia burgdorferi revealed by cryo-electron tomography: evidence for stator ring curvature and rotor/C-ring assembly flexion. J Bacteriol 191 : 5026 5036.[CrossRef]
13. Murphy GE,, Leadbetter JR,, Jensen GJ . 2006. In situ structure of the complete Treponema primitia flagellar motor. Nature 442 : 1062 1064.[CrossRef]
14. Miller MR,, Miller KA,, Bian J,, James ME,, Zhang S,, Lynch MJ,, Callery PS,, Hettick JM,, Cockburn A,, Liu J,, Li C,, Crane BR,, Charon NW . 2016. Spirochaete flagella hook proteins self-catalyse a lysinoalanine covalent crosslink for motility. Nat Microbiol 1 : 16134.[CrossRef]
15. Charon NW,, Goldstein SF,, Marko M,, Hsieh C,, Gebhardt LL,, Motaleb MA,, Wolgemuth CW,, Limberger RJ,, Rowe N . 2009. The flat-ribbon configuration of the periplasmic flagella of Borrelia burgdorferi and its relationship to motility and morphology. J Bacteriol 191 : 600 607.[CrossRef]
16. Zhao X,, Zhang K,, Boquoi T,, Hu B,, Motaleb MA,, Miller KA,, James ME,, Charon NW,, Manson MD,, Norris SJ,, Li C,, Liu J . 2013. Cryoelectron tomography reveals the sequential assembly of bacterial flagella in Borrelia burgdorferi. Proc Natl Acad Sci U S A 110 : 14390 14395.[CrossRef]
17. Moon KH,, Zhao X,, Xu H,, Liu J,, Motaleb MA . 2018. A tetratricopeptide repeat domain protein has profound effects on assembly of periplasmic flagella, morphology and motility of the Lyme disease spirochete Borrelia burgdorferi. Mol Microbiol 110 : 634 647.[CrossRef]
18. Leake MC,, Chandler JH,, Wadhams GH,, Bai F,, Berry RM,, Armitage JP . 2006. Stoichiometry and turnover in single, functioning membrane protein complexes. Nature 443 : 355 358.[CrossRef]
19. 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 : 825 835.[CrossRef]
20. Paulick A,, Koerdt A,, Lassak J,, Huntley S,, Wilms I,, Narberhaus F,, Thormann KM . 2009. Two different stator systems drive a single polar flagellum in Shewanella oneidensis MR-1. Mol Microbiol 71 : 836 850.[CrossRef]
21. Liu J,, Howell JK,, Bradley SD,, Zheng Y,, Zhou ZH,, Norris SJ . 2010. Cellular architecture of Treponema pallidum: novel flagellum, periplasmic cone, and cell envelope as revealed by cryo electron tomography. J Mol Biol 403 : 546 561.[CrossRef]
22. Raddi G,, Morado DR,, Yan J,, Haake DA,, Yang XF,, Liu J . 2012. Three-dimensional structures of pathogenic and saprophytic Leptospira species revealed by cryo-electron tomography. J Bacteriol 194 : 1299 1306.[CrossRef]
23. Kudryashev M,, Cyrklaff M,, Wallich R,, Baumeister W,, Frischknecht F . 2010. Distinct in situ structures of the Borrelia flagellar motor. J Struct Biol 169 : 54 61.[CrossRef]
24. 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 : 8787 8791.[CrossRef]
25. Cluzel P,, Surette M,, Leibler S . 2000. An ultrasensitive bacterial motor revealed by monitoring signaling proteins in single cells. Science 287 : 1652 1655.[CrossRef]
26. Bai F,, Branch RW,, Nicolau DV Jr,, Pilizota T,, Steel BC,, Maini PK,, Berry RM . 2010. Conformational spread as a mechanism for cooperativity in the bacterial flagellar switch. Science 327 : 685 689.[CrossRef]
27. Yuan J,, Branch RW,, Hosu BG,, Berg HC . 2012. Adaptation at the output of the chemotaxis signalling pathway. Nature 484 : 233 236.[CrossRef]
28. Lele PP,, Branch RW,, Nathan VSJ,, Berg HC . 2012. Mechanism for adaptive remodeling of the bacterial flagellar switch. Proc Natl Acad Sci U S A 109 : 20018 20022.[CrossRef]
29. Charon NW,, Goldstein SF . 2002. Genetics of motility and chemotaxis of a fascinating group of bacteria: the spirochetes. Annu Rev Genet 36 : 47 73.[CrossRef]
30. Li C,, Bakker RG,, Motaleb MA,, Sartakova ML,, Cabello FC,, Charon NW . 2002. Asymmetrical flagellar rotation in Borrelia burgdorferi nonchemotactic mutants. Proc Natl Acad Sci U S A 99 : 6169 6174.[CrossRef]
31. Motaleb MA,, Miller MR,, Li C,, Bakker RG,, Goldstein SF,, Silversmith RE,, Bourret RB,, Charon NW . 2005. CheX is a phosphorylated CheY phosphatase essential for Borrelia burgdorferi chemotaxis. J Bacteriol 187 : 7963 7969.[CrossRef]
32. Motaleb MA,, Sultan SZ,, Miller MR,, Li C,, Charon NW . 2011. CheY3 of Borrelia burgdorferi is the key response regulator essential for chemotaxis and forms a long-lived phosphorylated intermediate. J Bacteriol 193 : 3332 3341.[CrossRef]
33. Chevance FF,, Hughes KT . 2008. Coordinating assembly of a bacterial macromolecular machine. Nat Rev Microbiol 6 : 455 465.[CrossRef]
34. Macnab RM . 2003. How bacteria assemble flagella. Annu Rev Microbiol 57 : 77 100.[CrossRef]
35. 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 : 105 113.[CrossRef]
36. Minamino T,, Imada K,, Kinoshita M,, Nakamura S,, Morimoto YV,, Namba K . 2011. Structural insight into the rotational switching mechanism of the bacterial flagellar motor. PLoS Biol 9 : e1000616.[CrossRef]
37. Lee LK,, Ginsburg MA,, Crovace C,, Donohoe M,, Stock D . 2010. Structure of the torque ring of the flagellar motor and the molecular basis for rotational switching. Nature 466 : 996 1000.[CrossRef]
38. Delalez NJ,, Berry RM,, Armitage JP . 2014. Stoichiometry and turnover of the bacterial flagellar switch protein FliN. mBio 5 : e01216-14.[CrossRef]
39. Brown PN,, Mathews MAA,, Joss LA,, Hill CP,, Blair DF . 2005. Crystal structure of the flagellar rotor protein FliN from Thermotoga maritima. J Bacteriol 187 : 2890 2902.[CrossRef]
40. Zhang K,, Qin Z,, Chang Y,, Liu J,, Malkowski MG,, Shipa S,, Li L,, Qiu W,, Zhang J-R,, Li C . 2019. Analysis of a flagellar filament cap mutant reveals that HtrA serine protease degrades unfolded flagellin protein in the periplasm of Borrelia burgdorferi. Mol Microbiol 111 : 1652 1670.
41. Fraser GM,, González-Pedrajo B,, Tame JR,, Macnab RM . 2003. Interactions of FliJ with the Salmonella type III flagellar export apparatus. J Bacteriol 185 : 5546 5554.[CrossRef]
42. Minamino T,, Imada K . 2015. The bacterial flagellar motor and its structural diversity. Trends Microbiol 23 : 267 274.[CrossRef]
43. 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 : 277 282.[CrossRef]
44. 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 U S A 104 : 485 490.[CrossRef]
45. 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 : 583 590.[CrossRef]
46. Abby SS,, Rocha EP . 2012. The non-flagellar type III secretion system evolved from the bacterial flagellum and diversified into host-cell adapted systems. PLoS Genet 8 : e1002983.[CrossRef]
47. Hu B,, Lara-Tejero M,, Kong Q,, Galan JE,, Liu J . 2017. In situ molecular architecture of the Salmonella type III secretion machine. Cell 168 : 1065 1074.e1010.
48. Hu B,, Morado DR,, Margolin W,, Rohde JR,, Arizmendi O,, Picking WL,, Picking WD,, Liu J . 2015. Visualization of the type III secretion sorting platform of Shigella flexneri. Proc Natl Acad Sci U S A 112 : 1047 1052.[CrossRef]
49. 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.[CrossRef]
50. Zhu S,, Nishikino T,, Hu B,, Kojima S,, Homma M,, Liu J . 2017. Molecular architecture of the sheathed polar flagellum in Vibrio alginolyticus. Proc Natl Acad Sci U S A 114 : 10966 10971.[CrossRef]
51. Qin Z,, Lin WT,, Zhu S,, Franco AT,, Liu J . 2017. Imaging the motility and chemotaxis machineries in Helicobacter pylori by cryo-electron tomography. J Bacteriol 199 : e00695-16.
52. Qin Z,, Tu J,, Lin T,, Norris SJ,, Li C,, Motaleb MA,, Liu J . 2018. Cryo-electron tomography of periplasmic flagella in Borrelia burgdorferi reveals a distinct cytoplasmic ATPase complex. PLoS Biol 16 : e3000050.[CrossRef]

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error