Home LiteratureArticle Details
PMID: 15805535 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Crystal structure of the flagellar rotor protein FliN from Thermotoga maritima.

Journal of bacteriology ·Vol. 187 ·No. 8 ·2005-04-00 ·Pages 2890-902

Brown PN, Mathews MA, Joss LA, Hill CP, Blair DF

Abstract

FliN is a component of the bacterial flagellum that is present at levels of more than 100 copies and forms the bulk of the C ring, a drum-shaped structure at the inner end of the basal body. FliN interacts with FliG and FliM to form the rotor-mounted switch complex that controls clockwise-counterclockwise switching of the motor. In addition to its functions in motor rotation and switching, FliN is thought to have a role in the export of proteins that form the exterior structures of the flagellum (the rod, hook, and filament). Here, we describe the crystal structure of most of the FliN protein of Thermotoga maritima. FliN is a tightly intertwined dimer composed mostly of beta sheet. Several well-conserved hydrophobic residues form a nonpolar patch on the surface of the molecule. A mutation in the hydrophobic patch affected both flagellar assembly and switching, showing that this surface feature is important for FliN function. The association state of FliN in solution was studied by analytical ultracentrifugation, which provided clues to the higher-level organization of the protein. T. maritima FliN is primarily a dimer in solution, and T. maritima FliN and FliM together form a stable FliM(1)-FliN(4) complex. Escherichia coli FliN forms a stable tetramer in solution. The arrangement of FliN subunits in the tetramer was modeled by reference to the crystal structure of tetrameric HrcQB(C), a related protein that functions in virulence factor secretion in Pseudomonas syringae. The modeled tetramer is elongated, with approximate dimensions of 110 by 40 by 35 Angstroms, and it has a large hydrophobic cleft formed from the hydrophobic patches on the dimers. On the basis of the present data and available electron microscopic images, we propose a model for the organization of FliN subunits in the C ring.

MeSH Terms
Amino Acid Motifs Amino Acid Sequence Bacterial Proteins/chemistry Flagella/chemistry Protein Conformation Protein Structure, Tertiary Thermotoga maritima/chemistry,genetics
Chemicals
Bacterial Proteins FliN protein, Bacteria
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Brown Perry N
Department of Biology, University of Utah, Salt Lake City, UT 84132, USA.
Mathews Michael A A
Joss Lisa A
Hill Christopher P
Blair David F
References (75)
75 references, click to expand
  1. Salmonella typhimurium fliG and fliN mutations causing defects in assembly, rotation, and switching of the flagellar motor.
    J Bacteriol. 1993 Feb;175(3):802-10 PMID: 8423152
  2. Genetic and biochemical analysis of Salmonella typhimurium FliI, a flagellar protein related to the catalytic subunit of the F0F1 ATPase and to virulence proteins of mammalian and plant pathogens.
    J Bacteriol. 1993 May;175(10):3131-8 PMID: 8491729
  3. Main-chain bond lengths and bond angles in protein structures.
    J Mol Biol. 1993 Jun 20;231(4):1049-67 PMID: 8515464
  4. Phosphorylation-dependent binding of a signal molecule to the flagellar switch of bacteria.
    Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):8787-91 PMID: 8415608
  5. Isolation, characterization and structure of bacterial flagellar motors containing the switch complex.
    J Mol Biol. 1994 Jan 28;235(4):1261-70 PMID: 8308888
  6. Overproduction of the bacterial flagellar switch proteins and their interactions with the MS ring complex in vitro.
    J Bacteriol. 1994 Jun;176(12):3683-91 PMID: 8206846
  7. Combining evolutionary information and neural networks to predict protein secondary structure.
    Proteins. 1994 May;19(1):55-72 PMID: 8066087
  8. Regulated underexpression of the FliM protein of Escherichia coli and evidence for a location in the flagellar motor distinct from the MotA/MotB torque generators.
    J Bacteriol. 1995 Jun;177(12):3485-95 PMID: 7768858
  9. Regulated underexpression and overexpression of the FliN protein of Escherichia coli and evidence for an interaction between FliN and FliM in the flagellar motor.
    J Bacteriol. 1995 Jun;177(12):3496-503 PMID: 7768859
  10. RASMOL: biomolecular graphics for all.
    Trends Biochem Sci. 1995 Sep;20(9):374 PMID: 7482707
  11. Torque generation in the flagellar motor of Escherichia coli: evidence of a direct role for FliG but not for FliM or FliN.
    J Bacteriol. 1996 Jan;178(1):223-31 PMID: 8550421
  12. Supramolecular structure of the Salmonella typhimurium type III protein secretion system.
    Science. 1998 Apr 24;280(5363):602-5 PMID: 9554854
  13. Function of protonatable residues in the flagellar motor of Escherichia coli: a critical role for Asp 32 of MotB.
    J Bacteriol. 1998 May;180(10):2729-35 PMID: 9573160
  14. Type III protein secretion systems in bacterial pathogens of animals and plants.
    Microbiol Mol Biol Rev. 1998 Jun;62(2):379-433 PMID: 9618447
  15. Crystal structure of a small heat-shock protein.
    Nature. 1998 Aug 6;394(6693):595-9 PMID: 9707123
  16. Crystallography & NMR system: A new software suite for macromolecular structure determination.
    Acta Crystallogr D Biol Crystallogr. 1998 Sep 1;54(Pt 5):905-21 PMID: 9757107
  17. Architectural features of the Salmonella typhimurium flagellar motor switch revealed by disrupted C-rings.
    J Struct Biol. 1998;122(3):311-9 PMID: 9774535
  18. Domain analysis of the FliM protein of Escherichia coli.
    J Bacteriol. 1998 Nov;180(21):5580-90 PMID: 9791106
  19. Length of the flagellar hook and the capacity of the type III export apparatus.
    Science. 2001 Mar 23;291(5512):2411-3 PMID: 11264537
  20. Implementation of molecular replacement in AMoRe.
    Acta Crystallogr D Biol Crystallogr. 2001 Oct;57(Pt 10):1367-72 PMID: 11567147
  21. Structures of bacterial flagellar motors from two FliF-FliG gene fusion mutants.
    J Bacteriol. 2001 Nov;183(21):6404-12 PMID: 11591685
  22. Crystal structure and assembly of a eukaryotic small heat shock protein.
    Nat Struct Biol. 2001 Dec;8(12):1025-30 PMID: 11702068
  23. 50 million years of genomic stasis in endosymbiotic bacteria.
    Science. 2002 Jun 28;296(5577):2376-9 PMID: 12089438
  24. Crystal structure of the middle and C-terminal domains of the flagellar rotor protein FliG.
    EMBO J. 2002 Jul 1;21(13):3225-34 PMID: 12093724
  25. Variable symmetry in Salmonella typhimurium flagellar motors.
    Biophys J. 2003 Jan;84(1):571-7 PMID: 12524310
  26. Role of the cytoplasmic C terminus of the FliF motor protein in flagellar assembly and rotation.
    J Bacteriol. 2003 Mar;185(5):1624-33 PMID: 12591880
  27. Type III secretion systems and bacterial flagella: insights into their function from structural similarities.
    Proc Natl Acad Sci U S A. 2003 Mar 18;100(6):3027-30 PMID: 12631703
  28. The type III secretion chaperone FlgN regulates flagellar assembly via a negative feedback loop containing its chaperone substrates FlgK and FlgL.
    Mol Microbiol. 2003 Sep;49(5):1333-45 PMID: 12940991
  29. Similar modes of polypeptide recognition by export chaperones in flagellar biosynthesis and type III secretion.
    Nat Struct Biol. 2003 Oct;10(10):789-93 PMID: 12958592
  30. The rotary motor of bacterial flagella.
    Annu Rev Biochem. 2003;72:19-54 PMID: 12500982
  31. How bacteria assemble flagella.
    Annu Rev Microbiol. 2003;57:77-100 PMID: 12730325
  32. Structure of HrcQB-C, a conserved component of the bacterial type III secretion systems.
    Proc Natl Acad Sci U S A. 2004 Jan 6;101(1):70-5 PMID: 14694203
  33. The bacterial flagellar motor: structure and function of a complex molecular machine.
    Int Rev Cytol. 2004;233:93-134 PMID: 15037363
  34. Incomplete flagellar structures in nonflagellate mutants of Salmonella typhimurium.
    J Bacteriol. 1978 Feb;133(2):904-15 PMID: 342514
  35. Incomplete flagellar structures in Escherichia coli mutants.
    J Bacteriol. 1981 Feb;145(2):1036-41 PMID: 7007337
  36. Silver stain for proteins in polyacrylamide gels: a modified procedure with enhanced uniform sensitivity.
    Anal Biochem. 1981 Nov 1;117(2):307-10 PMID: 6172996
  37. Subdivision of flagellar genes of Salmonella typhimurium into regions responsible for assembly, rotation, and switching.
    J Bacteriol. 1986 Apr;166(1):187-93 PMID: 3007433
  38. Genetic evidence for a switching and energy-transducing complex in the flagellar motor of Salmonella typhimurium.
    J Bacteriol. 1986 Dec;168(3):1172-9 PMID: 3536867
  39. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes.
    J Mol Biol. 1986 May 5;189(1):113-30 PMID: 3537305
  40. Identification of the M-ring protein of the flagellar motor of Salmonella typhimurium.
    Proc Natl Acad Sci U S A. 1987 Nov;84(21):7483-7 PMID: 3313394
  41. Structure of the core and central channel of bacterial flagella.
    Nature. 1989 Dec 7;342(6250):648-54 PMID: 2687696
  42. FliG and FliM distribution in the Salmonella typhimurium cell and flagellar basal bodies.
    J Bacteriol. 1996 Jan;178(1):258-65 PMID: 8550426
  43. Improved high-level expression system for eukaryotic genes in Escherichia coli using T7 RNA polymerase and rare ArgtRNAs.
    Biotechniques. 1995 Aug;19(2):196-8, 200 PMID: 8527135
  44. Geometry of the flagellar motor in the cytoplasmic membrane of Salmonella typhimurium as determined by stereo-photogrammetry of quick-freeze deep-etch replica images.
    J Mol Biol. 1996 Jan 26;255(3):458-75 PMID: 8568890
  45. Interacting components of the flagellar motor of Escherichia coli revealed by the two-hybrid system in yeast.
    J Mol Biol. 1996 Mar 1;256(3):564-76 PMID: 8604139
  46. A mutational analysis of the interaction between FliG and FliM, two components of the flagellar motor of Escherichia coli.
    J Bacteriol. 1996 Mar;178(5):1289-94 PMID: 8631704
  47. FliN is a major structural protein of the C-ring in the Salmonella typhimurium flagellar basal body.
    J Mol Biol. 1996 Aug 16;261(2):195-208 PMID: 8757287
  48. Components of the Salmonella flagellar export apparatus and classification of export substrates.
    J Bacteriol. 1999 Mar;181(5):1388-94 PMID: 10049367
  49. Efficient anisotropic refinement of macromolecular structures using FFT.
    Acta Crystallogr D Biol Crystallogr. 1999 Jan;55(Pt 1):247-55 PMID: 10089417
  50. Substrate-specific binding of hook-associated proteins by FlgN and FliT, putative chaperones for flagellum assembly.
    Mol Microbiol. 1999 May;32(3):569-80 PMID: 10320579
  51. Evidence for lateral gene transfer between Archaea and bacteria from genome sequence of Thermotoga maritima.
    Nature. 1999 May 27;399(6734):323-9 PMID: 10360571
  52. Rotational symmetry of the C ring and a mechanism for the flagellar rotary motor.
    Proc Natl Acad Sci U S A. 1999 Aug 31;96(18):10134-9 PMID: 10468575
  53. The bacterial flagellum: reversible rotary propellor and type III export apparatus.
    J Bacteriol. 1999 Dec;181(23):7149-53 PMID: 10572114
  54. From flagellum assembly to virulence: the extended family of type III export chaperones.
    Trends Microbiol. 2000 May;8(5):202-4 PMID: 10785634
  55. Deletion analysis of the flagellar switch protein FliG of Salmonella.
    J Bacteriol. 2000 Jun;182(11):3022-8 PMID: 10809678
  56. FliH, a soluble component of the type III flagellar export apparatus of Salmonella, forms a complex with FliI and inhibits its ATPase activity.
    Mol Microbiol. 2000 Sep;37(6):1494-503 PMID: 10998179
  57. An approach to multi-copy search in molecular replacement.
    Acta Crystallogr D Biol Crystallogr. 2000 Dec;56(Pt 12):1622-4 PMID: 11092928
  58. Substrate complexes and domain organization of the Salmonella flagellar export chaperones FlgN and FliT.
    Mol Microbiol. 2001 Feb;39(3):781-91 PMID: 11169117
  59. Motility protein complexes in the bacterial flagellar motor.
    J Mol Biol. 1996 Aug 16;261(2):209-21 PMID: 8757288
  60. Enzymatic characterization of FliI. An ATPase involved in flagellar assembly in Salmonella typhimurium.
    J Biol Chem. 1996 Dec 13;271(50):31981-8 PMID: 8943245
  61. Deletion analysis of the FliM flagellar switch protein of Salmonella typhimurium.
    J Bacteriol. 1996 Dec;178(24):7069-79 PMID: 8955386
  62. Evidence that the Pseudomonas syringae pv. syringae hrp-linked hrmA gene encodes an Avr-like protein that acts in an hrp-dependent manner within tobacco cells.
    Mol Plant Microbe Interact. 1997 Jul;10(5):580-8 PMID: 9204563
  63. Distinct regions of bacterial flagellar switch protein FliM interact with FliG, FliN and CheY.
    J Mol Biol. 1997 Oct 31;273(3):623-34 PMID: 9356251
  64. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling.
    Electrophoresis. 1997 Dec;18(15):2714-23 PMID: 9504803
  65. The complete genome of the hyperthermophilic bacterium Aquifex aeolicus.
    Nature. 1998 Mar 26;392(6674):353-8 PMID: 9537320
  66. Flagellar assembly in Salmonella typhimurium: analysis with temperature-sensitive mutants.
    J Bacteriol. 1990 Mar;172(3):1327-39 PMID: 2407720
  67. Improved methods for building protein models in electron density maps and the location of errors in these models.
    Acta Crystallogr A. 1991 Mar 1;47 ( Pt 2):110-9 PMID: 2025413
  68. Salmonella typhimurium mutants defective in flagellar filament regrowth and sequence similarity of FliI to F0F1, vacuolar, and archaebacterial ATPase subunits.
    J Bacteriol. 1991 Jun;173(11):3564-72 PMID: 1646201
  69. Molecular analysis of the flagellar switch protein FliM of Salmonella typhimurium.
    J Bacteriol. 1992 Feb;174(3):793-806 PMID: 1732214
  70. The cytoplasmic component of the bacterial flagellar motor.
    Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):5956-60 PMID: 1631080
  71. Localization of the Salmonella typhimurium flagellar switch protein FliG to the cytoplasmic M-ring face of the basal body.
    Proc Natl Acad Sci U S A. 1992 Jul 15;89(14):6304-8 PMID: 1631122
  72. Morphological pathway of flagellar assembly in Salmonella typhimurium.
    J Mol Biol. 1992 Jul 20;226(2):433-46 PMID: 1640458
  73. 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. 1992 Oct 5;227(3):672-7 PMID: 1404383
  74. Boundary analysis in sedimentation transport experiments: a procedure for obtaining sedimentation coefficient distributions using the time derivative of the concentration profile.
    Anal Biochem. 1992 Jun;203(2):295-301 PMID: 1416025
  75. Identification and characterization of FliY, a novel component of the Bacillus subtilis flagellar switch complex.
    Mol Microbiol. 1992 Sep;6(18):2715-23 PMID: 1447979
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
2005-04-00
Pages
2890-902
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC1070373
Subset
IM
Grants
NIGMS NIH HHS · T32 GM008537 · United States
NIGMS NIH HHS · R01-GM61145 · United States
NIGMS NIH HHS · 5T32-GM08537 · United States
NCI NIH HHS · 5P30 CA42014 · United States
NCI NIH HHS · P30 CA042014 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]