Bacterial nanomachines: the flagellum and type III injectisome.

The bacterial flagellum and the virulence-associated injectisome are complex, structurally related nanomachines that bacteria use for locomotion or the translocation of virulence factors into eukaryotic host cells. The assembly of both structures and the transfer of extracellular proteins is mediated by a unique, multicomponent transport apparatus, the type III secretion system. Here, we discuss the significant progress that has been made in recent years in the visualization and functional characterization of many components of the type III secretion system, the structure of the bacterial flagellum, and the injectisome complex.

[1]  R M Macnab,et al.  Salmonella typhimurium mutants defective in flagellar filament regrowth and sequence similarity of FliI to F0F1, vacuolar, and archaebacterial ATPase subunits , 1991, Journal of bacteriology.

[2]  F. Cordes,et al.  Helical Structure of the Needle of the Type III Secretion System of Shigella flexneri * , 2003, The Journal of Biological Chemistry.

[3]  D. DeRosier,et al.  Structures of Bacterial Flagellar Motors from Two FliF-FliG Gene Fusion Mutants , 2001, Journal of bacteriology.

[4]  Katsumi Imada,et al.  Molecular motors of the bacterial flagella. , 2008, Current opinion in structural biology.

[5]  C. Calladine.  Construction of bacterial flagella , 1975, Nature.

[6]  Shin-Ichi Aizawa,et al.  Type III secretion systems and bacterial flagella: Insights into their function from structural similarities , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[7]  K. Hughes,et al.  Coordinating assembly of a bacterial macromolecular machine , 2008, Nature Reviews Microbiology.

[8]  M. Simon,et al.  Flagellar rotation and the mechanism of bacterial motility , 1974, Nature.

[9]  Samuel I. Miller,et al.  Structural characterization of the molecular platform for type III secretion system assembly , 2005, Nature.

[10]  F. Cordes,et al.  Molecular model of a type III secretion system needle: Implications for host-cell sensing , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[11]  J. Adler,et al.  Purification of Intact Flagella from Escherichia coli and Bacillus subtilis , 1971, Journal of bacteriology.

[12]  R M Macnab,et al.  Normal-to-curly flagellar transitions and their role in bacterial tumbling. Stabilization of an alternative quaternary structure by mechanical force. , 1977, Journal of molecular biology.

[13]  C. R. Calldine.  Change of waveform in bacterial flagella : the role of mechanics at the molecular level , 1978 .

[14]  N. Strynadka,et al.  Piecing together the type III injectisome of bacterial pathogens. , 2008, Current opinion in structural biology.

[15]  R M Macnab,et al.  Molecular analysis of the flagellar switch protein FliM of Salmonella typhimurium , 1992, Journal of bacteriology.

[16]  B. Stocker,et al.  A new fla gene in Salmonella typhimurium—flaR—and its mutant phenotype-superhooks , 1973, Archiv für Mikrobiologie.

[17]  K. Hughes,et al.  Type III secretion: a secretory pathway serving both motility and virulence (Review) , 2005, Molecular membrane biology.

[18]  K. Namba,et al.  Role of the N‐terminal domain of FliI ATPase in bacterial flagellar protein export , 2009, FEBS letters.

[19]  Hans Wolf-Watz,et al.  Protein delivery into eukaryotic cells by type III secretion machines , 2006, Nature.

[20]  R. Macnab,et al.  The flaFIX gene product of Salmonella typhimurium is a flagellar basal body component with a signal peptide for export , 1987, Journal of bacteriology.

[21]  C. Parsot,et al.  The various and varying roles of specific chaperones in type III secretion systems. , 2003, Current opinion in microbiology.

[22]  K. Hughes,et al.  Energy source of flagellar type III secretion , 2008, Nature.

[23]  Seiji Kojima,et al.  The bacterial flagellar motor: structure and function of a complex molecular machine. , 2004, International review of cytology.

[24]  T. Lino.  Assembly of Salmonella flagellin in vitro and in vivo. , 1974 .

[25]  G. Cornelis,et al.  The type III secretion injectisome , 2006, Nature Reviews Microbiology.

[26]  D. Blair,et al.  Mutational Analysis of the Flagellar Protein FliG: Sites of Interaction with FliM and Implications for Organization of the Switch Complex , 2006, Journal of bacteriology.

[27]  C. Hill,et al.  Crystal structure of the middle and C‐terminal domains of the flagellar rotor protein FliG , 2002, The EMBO journal.

[28]  G. Cornelis,et al.  Assembly and function of type III secretory systems. , 2000, Annual review of microbiology.

[29]  K Namba,et al.  The structure of the R-type straight flagellar filament of Salmonella at 9 A resolution by electron cryomicroscopy. , 1995, Journal of molecular biology.

[30]  U. Gophna,et al.  Bacterial type III secretion systems are ancient and evolved by multiple horizontal-transfer events. , 2003, Gene.

[31]  R. Macnab,et al.  Flagellar hook and hook-associated proteins of Salmonella typhimurium and their relationship to other axial components of the flagellum. , 1990, Journal of molecular biology.

[32]  S. Müller,et al.  The V-Antigen of Yersinia Forms a Distinct Structure at the Tip of Injectisome Needles , 2005, Science.

[33]  L. Claret,et al.  Oligomerization and activation of the FliI ATPase central to bacterial flagellum assembly , 2003, Molecular microbiology.

[34]  J. Galán,et al.  Molecular characterization and assembly of the needle complex of the Salmonella typhimurium type III protein secretion system. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[35]  C. Hueck,et al.  Type III Protein Secretion Systems in Bacterial Pathogens of Animals and Plants , 1998, Microbiology and Molecular Biology Reviews.

[36]  S. Aizawa.  Flagellar assembly in Salmonella typhimurium , 1996, Molecular microbiology.

[37]  H. Stahlberg,et al.  Type III Protein Translocase , 2003, Journal of Biological Chemistry.

[38]  K. Namba,et al.  Transition of bacterial flagella from helical to straight forms with different subunit arrangements. , 1979, Journal of molecular biology.

[39]  K. Hughes,et al.  Sensing structural intermediates in bacterial flagellar assembly by export of a negative regulator. , 1993, Science.

[40]  T. Minamino,et al.  Flipping the switch: bringing order to flagellar assembly. , 2006, Trends in microbiology.

[41]  D. DeRosier.  Bacterial Flagellum: Visualizing the Complete Machine In Situ , 2006, Current Biology.

[42]  R. Macnab,et al.  Domain organization of the subunit of the Salmonella typhimurium flagellar hook. , 1993, Journal of molecular biology.

[43]  D G Morgan,et al.  The bacterial flagellar cap as the rotary promoter of flagellin self-assembly. , 2000, Science.

[44]  K. Namba,et al.  Mechanisms of type III protein export for bacterial flagellar assembly. , 2008, Molecular bioSystems.

[45]  T. Iino.  Assembly of Salmonella flagellin in vitro and in vivo. , 1974, Journal of supramolecular structure.

[46]  J. Adler,et al.  Fine Structure and Isolation of the Hook-Basal Body Complex of Flagella from Escherichia coli and Bacillus subtilis , 1971, Journal of bacteriology.

[47]  J. Tommassen,et al.  The outer membrane component, YscC, of the Yop secretion machinery of Yersinia enterocolitica forms a ring‐shaped multimeric complex , 1997, Molecular microbiology.

[48]  J. Galán,et al.  Chaperone release and unfolding of substrates in type III secretion , 2005, Nature.

[49]  R. Macnab.  Type III flagellar protein export and flagellar assembly , 2004 .

[50]  R. Macnab,et al.  Interaction between FliE and FlgB, a Proximal Rod Component of the Flagellar Basal Body ofSalmonella , 2000, Journal of bacteriology.

[51]  K. Namba,et al.  Distinct roles of the FliI ATPase and proton motive force in bacterial flagellar protein export , 2008, Nature.

[52]  T. Marlovits,et al.  Structural Insights into the Assembly of the Type III Secretion Needle Complex , 2004, Science.

[53]  K. Namba,et al.  Characterization of the Periplasmic Domain of MotB and Implications for Its Role in the Stator Assembly of the Bacterial Flagellar Motor , 2008, Journal of bacteriology.

[54]  K. Namba,et al.  Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy , 2003, Nature.

[55]  H. Berg.  The rotary motor of bacterial flagella. , 2003, Annual review of biochemistry.

[56]  T. Kimbrough,et al.  Contribution of Salmonella typhimurium type III secretion components to needle complex formation. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[57]  Katsumi Imada,et al.  Structure of the bacterial flagellar hook and implication for the molecular universal joint mechanism , 2004, Nature.

[58]  K Namba,et al.  Molecular architecture of bacterial flagellum , 1997, Quarterly Reviews of Biophysics.

[59]  R. Macnab,et al.  Components of the Salmonella Flagellar Export Apparatus and Classification of Export Substrates , 1999, Journal of bacteriology.

[60]  D J DeRosier,et al.  Rotational symmetry of the C ring and a mechanism for the flagellar rotary motor. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[61]  B. Finlay,et al.  Structural analysis of a prototypical ATPase from the type III secretion system , 2007, Nature Structural &Molecular Biology.

[62]  D. Blair,et al.  Torque generation in the flagellar motor of Escherichia coli: evidence of a direct role for FliG but not for FliM or FliN , 1996, Journal of bacteriology.

[63]  R. Macnab,et al.  Enzymatic Characterization of FliI , 1996, The Journal of Biological Chemistry.

[64]  C. Hill,et al.  Crystal Structure of the Flagellar Rotor Protein FliN from Thermotoga maritima , 2005, Journal of bacteriology.

[65]  J. Galán,et al.  Supramolecular structure of the Salmonella typhimurium type III protein secretion system. , 1998, Science.

[66]  H. Stahlberg,et al.  Type III protein translocase: HrcN is a peripheral ATPase that is activated by oligomerization. , 2003, The Journal of biological chemistry.

[67]  K. Oosawa,et al.  Roles of FliK and FlhB in determination of flagellar hook length in Salmonella typhimurium , 1994, Journal of bacteriology.

[68]  J. Shioi,et al.  Motility in Bacillus subtilis driven by an artificial protonmotive force , 1977, FEBS letters.

[69]  S. Asakura.  Polymerization of flagellin and polymorphism of flagella. , 1970, Advances in biophysics.

[70]  S. Phillips,et al.  Structure of HrcQB-C, a conserved component of the bacterial type III secretion systems , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[71]  H. Berg,et al.  Bacteria Swim by Rotating their Flagellar Filaments , 1973, Nature.

[72]  J. Wall,et al.  Corrigendum: Three-dimensional reconstruction of the Shigella T3SS transmembrane regions reveals 12-fold symmetry and novel features throughout , 2009, Nature Structural &Molecular Biology.

[73]  H. Berg,et al.  A protonmotive force drives bacterial flagella. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[74]  L. Journet,et al.  The Needle Length of Bacterial Injectisomes Is Determined by a Molecular Ruler , 2003, Science.

[75]  D. Blair,et al.  Organization of FliN Subunits in the Flagellar Motor of Escherichia coli , 2006, Journal of bacteriology.

[76]  K. Namba,et al.  Structural similarity between the flagellar type III ATPase FliI and F1-ATPase subunits , 2007, Proceedings of the National Academy of Sciences.

[77]  K. Namba.  Roles of partly unfolded conformations in macromolecular self‐assembly , 2001, Genes to cells : devoted to molecular & cellular mechanisms.

[78]  K. Namba,et al.  A partial atomic structure for the flagellar hook of Salmonella typhimurium. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[79]  J. Galán,et al.  Type III Secretion Machines: Bacterial Devices for Protein Delivery into Host Cells , 1999 .

[80]  D. DeRosier,et al.  The Three-Dimensional Structure of the Flagellar Rotor from a Clockwise-Locked Mutant of Salmonella enterica Serovar Typhimurium , 2006, Journal of bacteriology.

[81]  Takashi Kumasaka,et al.  Structure of the bacterial flagellar protofilament and implications for a switch for supercoiling , 2001, Nature.

[82]  Domain movements of HAP2 in the cap–filament complex formation and growth process of the bacterial flagellum , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[83]  R. Macnab,et al.  FliH, a soluble component of the type III flagellar export apparatus of Salmonella, forms a complex with FliI and inhibits its ATPase activity , 2000, Molecular microbiology.

[84]  R. Macnab,et al.  How bacteria assemble flagella. , 2003, Annual review of microbiology.

[85]  J. Heesemann,et al.  Yersinia enterocolitica Type III Secretion Depends on the Proton Motive Force but Not on the Flagellar Motor Components MotA and MotB , 2004, Infection and Immunity.

[86]  M. Kokkinidis,et al.  Conserved features of type III secretion , 2004, Cellular microbiology.