Single-Molecule Studies of Rotary Molecular Motors

Rotary molecular motors are protein complexes that transform chemical or electrochemical energy into mechanical work. There are five known rotary molecular motors in nature; the bacterial flagellar motor, and two motors in each of ATP-synthase and V-ATPase. Rotation of the flagellar motor drives a helical propeller that powers bacterial swimming. The function of the other rotary motors is to couple electrochemical ion gradients to synthesis or hydrolysis of ATP, and rotation is a detail of the coupling mechanism rather than the ultimate purpose of the motors. Much has been learned about the mechanism of the F1 part of ATP-synthase and the flagellar motor by measuring the rotation of single motors with a variety of techniques under a wide range of conditions. This chapter will review the structures of ATP-synthase and the flagellar motor, and what has been learned about their mechanisms using single molecule techniques.

[1]  W. Junge,et al.  F1-ATPase, the C-terminal End of Subunit γ Is Not Required for ATP Hydrolysis-driven Rotation* , 2002, The Journal of Biological Chemistry.

[2]  R. Henderson,et al.  Structure of the mitochondrial ATP synthase by electron cryomicroscopy , 2003, The EMBO journal.

[3]  Kazuhiko Kinosita,et al.  F1-ATPase Is a Highly Efficient Molecular Motor that Rotates with Discrete 120° Steps , 1998, Cell.

[4]  Hiroyasu Itoh,et al.  Coupling of Rotation and Catalysis in F1-ATPase Revealed by Single-Molecule Imaging and Manipulation , 2007, Cell.

[5]  M. A. Kozlova,et al.  The proton-driven rotor of ATP synthase: ohmic conductance (10 fS), and absence of voltage gating. , 2004, Biophysical journal.

[6]  A. Yamamoto,et al.  Subunit rotation of ATP synthase embedded in membranes: a or β subunit rotation relative to the c subunit ring , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[7]  J. Adler,et al.  Chemomechanical coupling without ATP: the source of energy for motility and chemotaxis in bacteria. , 1974, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Henning Stahlberg,et al.  Structural biology: Proton-powered turbine of a plant motor , 2000, Nature.

[9]  T. Hamamoto,et al.  pH dependence of H+ conduction through the membrane moiety of the H+-ATPase (F0 . F1) and effects of tyrosyl residue modification. , 1981, The Journal of biological chemistry.

[10]  W. Junge,et al.  Intersubunit rotation in active F-ATPase , 1996, Nature.

[11]  Kazuhiko Kinosita,et al.  Direct Observation of the Rotation of ε Subunit in F1-ATPase* , 1998, The Journal of Biological Chemistry.

[12]  Michael Börsch,et al.  Proton-powered subunit rotation in single membrane-bound F0F1-ATP synthase , 2004, Nature Structural &Molecular Biology.

[13]  Masasuke Yoshida,et al.  Stepping rotation of F1-ATPase visualized through angle-resolved single-fluorophore imaging. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Thomas Meier,et al.  Evidence for structural integrity in the undecameric c-rings isolated from sodium ATP synthases. , 2003, Journal of molecular biology.

[15]  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.

[16]  H. Berg,et al.  Mechanical limits of bacterial flagellar motors probed by electrorotation. , 1995, Biophysical journal.

[17]  Y Imae,et al.  Quantitative measurements of proton motive force and motility in Bacillus subtilis , 1980, Journal of bacteriology.

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

[19]  R. Fazzio,et al.  Membrane topology of the MotA protein of Escherichia coli. , 1995, Journal of Molecular Biology.

[20]  G. Wadhams,et al.  Making sense of it all: bacterial chemotaxis , 2004, Nature Reviews Molecular Cell Biology.

[21]  H. Berg,et al.  Torque generated by the flagellar motor of Escherichia coli while driven backward. , 1999, Biophysical journal.

[22]  R. Wagner,et al.  Single channel H+ currents through reconstituted chloroplast ATP synthase CF0‐CF1. , 1989, The EMBO journal.

[23]  Y Imae,et al.  High-speed rotation and speed stability of the sodium-driven flagellar motor in Vibrio alginolyticus. , 1995, Journal of molecular biology.

[24]  Hiroyasu Itoh,et al.  Resolution of distinct rotational substeps by submillisecond kinetic analysis of F1-ATPase , 2001, Nature.

[25]  H. Berg,et al.  Torque generated by the flagellar motor of Escherichia coli. , 1993, Biophysical journal.

[26]  Andrew G. W. Leslie,et al.  The structure of the central stalk in bovine F1-ATPase at 2.4 Å resolution , 2000, Nature Structural Biology.

[27]  Alois Renn,et al.  Coupled rotation within single F0F1 enzyme complexes during ATP synthesis or hydrolysis , 2002, FEBS letters.

[28]  D. Blair,et al.  Electrostatic interactions between rotor and stator in the bacterial flagellar motor. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[29]  R. Berry,et al.  Fluorescence measurement of intracellular sodium concentration in single Escherichia coli cells. , 2006, Biophysical journal.

[30]  M. Simon,et al.  The identification of the mot gene product with Escherichia coli-lambda hybrids. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Steven M. Block,et al.  Compliance of bacterial flagella measured with optical tweezers , 1989, Nature.

[32]  R. Macnab,et al.  Subdivision of flagellar genes of Salmonella typhimurium into regions responsible for assembly, rotation, and switching , 1986, Journal of bacteriology.

[33]  E. Schneider,et al.  ATP synthetase (F1F0) of Escherichia coli K-12. High-yield preparation of functional F0 by hydrophobic affinity chromatography. , 1982, European journal of biochemistry.

[34]  Kazuhiko Kinosita,et al.  Direct observation of the rotation of F1-ATPase , 1997, Nature.

[35]  Masasuke Yoshida,et al.  Axle-Less F1-ATPase Rotates in the Correct Direction , 2008, Science.

[36]  H. Berg,et al.  Mutations in the MotA protein of Escherichia coli reveal domains critical for proton conduction. , 1991, Journal of molecular biology.

[37]  J. Mason,et al.  A gene cluster in the spinach and pea chloroplast genomes encoding one CF1 and three CF0 subunits of the H+-ATP synthase complex and the ribosomal protein S2. , 1987, Journal of molecular biology.

[38]  Daniel J. Cipriano,et al.  Stochastic High-speed Rotation of Escherichia coli ATP Synthase F1 Sector , 2006, Journal of Biological Chemistry.

[39]  D. Blair,et al.  Function of Proline Residues of MotA in Torque Generation by the Flagellar Motor of Escherichia coli , 1999, Journal of bacteriology.

[40]  D. Blair,et al.  Tryptophan-scanning mutagenesis of MotB, an integral membrane protein essential for flagellar rotation in Escherichia coli. , 1995, Biochemistry.

[41]  Kazuhiko Kinosita,et al.  Catalysis and rotation of F1 motor: Cleavage of ATP at the catalytic site occurs in 1 ms before 40° substep rotation , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[42]  R. Macnab,et al.  Salmonella typhimurium fliG and fliN mutations causing defects in assembly, rotation, and switching of the flagellar motor , 1993, Journal of bacteriology.

[43]  H. Berg,et al.  Force-extension measurements on bacterial flagella: triggering polymorphic transformations. , 2007, Biophysical journal.

[44]  M. Homma,et al.  Roles of Charged Residues of Rotor and Stator in Flagellar Rotation: Comparative Study using H+-Driven and Na+-Driven Motors in Escherichia coli , 2006, Journal of bacteriology.

[45]  V. V. Bulygin,et al.  Rotation of subunits during catalysis by Escherichia coli F1-ATPase. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Daniel J. Muller,et al.  An intermediate step in the evolution of ATPases – a hybrid F0–V0 rotor in a bacterial Na+ F1F0 ATP synthase , 2008, The FEBS journal.

[47]  David Spetzler,et al.  Microsecond time scale rotation measurements of single F1-ATPase molecules. , 2006, Biochemistry.

[48]  William S. Ryu,et al.  Real-Time Imaging of Fluorescent Flagellar Filaments , 2000, Journal of bacteriology.

[49]  J. Vanderleyden,et al.  A conserved surface-exposed domain in major outer membrane proteins of pathogenic Pseudomonas and Branhamella species shares sequence homology with the calcium-binding repeats of the eukaryotic extracellular matrix protein thrombospondin. , 1994, Molecular microbiology.

[50]  Howard C. Berg,et al.  On Torque and Tumbling in Swimming Escherichia coli , 2006, Journal of bacteriology.

[51]  D. Blair,et al.  How bacteria sense and swim. , 1995, Annual review of microbiology.

[52]  M. Futai,et al.  Nucleotide sequence of the genes coding for α, β and γ subunits of the proton-translocating ATPase of Escherichia coli , 1981 .

[53]  J. Armitage,et al.  The maximum number of torque-generating units in the flagellar motor of Escherichia coli is at least 11. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[54]  R. Berry,et al.  Nonequivalence of membrane voltage and ion-gradient as driving forces for the bacterial flagellar motor at low load. , 2007, Biophysical journal.

[55]  Hiroyuki Fujita,et al.  Highly coupled ATP synthesis by F1-ATPase single molecules , 2005, Nature.

[56]  Masasuke Yoshida,et al.  Mechanically driven ATP synthesis by F1-ATPase , 2004, Nature.

[57]  H. Berg,et al.  Powering the flagellar motor of Escherichia coli with an external voltage source , 1995, Nature.

[58]  H. Berg,et al.  The speed of the flagellar rotary motor of Escherichia coli varies linearly with protonmotive force , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[59]  M. Müller,et al.  Inter‐subunit rotation and elastic power transmission in F0F1‐ATPase , 2001, FEBS letters.

[60]  H C Berg,et al.  Fluctuation analysis of rotational speeds of the bacterial flagellar motor. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

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

[62]  H. Hotani.  Light microscope study of mixed helices in reconstituted Salmonella flagella. , 1976, Journal of molecular biology.

[63]  Masasuke Yoshida,et al.  ATP synthase — a marvellous rotary engine of the cell , 2001, Nature Reviews Molecular Cell Biology.

[64]  Masasuke Yoshida,et al.  Purine but Not Pyrimidine Nucleotides Support Rotation of F1-ATPase* , 2001, The Journal of Biological Chemistry.

[65]  Michael Börsch,et al.  Stepwise rotation of the γ‐subunit of EF0F1‐ATP synthase observed by intramolecular single‐molecule fluorescence resonance energy transfer 1 , 2002 .

[66]  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.

[67]  P. Mitchell.  Coupling of Phosphorylation to Electron and Hydrogen Transfer by a Chemi-Osmotic type of Mechanism , 1961, Nature.

[68]  K. Oosawa,et al.  Domain structures of the MS ring component protein (FliF) of the flagellar basal body of Salmonella typhimurium. , 1994, Journal of molecular biology.

[69]  Fan Bai,et al.  A programmable optical angle clamp for rotary molecular motors. , 2007, Biophysical journal.

[70]  H. Berg,et al.  Energetics of flagellar rotation in bacteria. , 1980, Journal of molecular biology.

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

[72]  R. H. Fillingame,et al.  Cross-linking between Helices within Subunit a of Escherichia coli ATP Synthase Defines the Transmembrane Packing of a Four-helix Bundle* , 2006, Journal of Biological Chemistry.

[73]  Kazuhiko Kinosita,et al.  Activation of pausing F1 motor by external force. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[74]  T. Stevens,et al.  Molecular Characterization of the Yeast Vacuolar H+-ATPase Proton Pore* , 2000, The Journal of Biological Chemistry.

[75]  Hiroyasu Itoh,et al.  The ATP-waiting conformation of rotating F1-ATPase revealed by single-pair fluorescence resonance energy transfer , 2003, Proceedings of the National Academy of Sciences of the United States of America.

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

[77]  W. Junge,et al.  The proton channel, CF0, in thylakoid membranes. Only a low proportion of CF1-lacking CF0 is active with a high unit conductance (169 fS). , 1986, European journal of biochemistry.

[78]  Fang Xiaohong,et al.  Rotary torque produced by proton motive force in FoF1 motor. , 2005, Biochemical and biophysical research communications.

[79]  Michio Homma,et al.  Torque-speed relationships of Na+-driven chimeric flagellar motors in Escherichia coli. , 2008, Journal of molecular biology.

[80]  H. Berg,et al.  Torque-speed relationship of the flagellar rotary motor of Escherichia coli. , 2000, Biophysical journal.

[81]  H. Berg,et al.  Solvent-isotope and pH effects on flagellar rotation in Escherichia coli. , 2000, Biophysical journal.

[82]  Masasuke Yoshida,et al.  Stepping Rotation of F1-ATPase with One, Two, or Three Altered Catalytic Sites That Bind ATP Only Slowly* , 2002, The Journal of Biological Chemistry.

[83]  Masasuke Yoshida,et al.  F1-ATPase rotates by an asymmetric, sequential mechanism using all three catalytic subunits , 2007, Nature Structural &Molecular Biology.

[84]  W. Tucker,et al.  The 20 C-terminal Amino Acid Residues of the Chloroplast ATP Synthase γ Subunit Are Not Essential for Activity* , 1999, The Journal of Biological Chemistry.

[85]  Kazuhiko Kinosita,et al.  Chemomechanical coupling in F1-ATPase revealed by simultaneous observation of nucleotide kinetics and rotation , 2004, Nature Structural &Molecular Biology.

[86]  William S Ryu,et al.  The thermal impulse response of Escherichia coli , 2008, Proceedings of the National Academy of Sciences.

[87]  N. Hirota,et al.  Na+-driven flagellar motors of an alkalophilic Bacillus strain YN-1. , 1983, The Journal of biological chemistry.

[88]  Masasuke Yoshida,et al.  The presence of phosphate at a catalytic site suppresses the formation of the MgADP-inhibited form of F(1)-ATPase. , 2002, European journal of biochemistry.

[89]  A. Leslie,et al.  Ground State Structure of F1-ATPase from Bovine Heart Mitochondria at 1.9 Å Resolution* , 2007, Journal of Biological Chemistry.

[90]  D. Blair,et al.  Structure of FliM provides insight into assembly of the switch complex in the bacterial flagella motor , 2006, Proceedings of the National Academy of Sciences.

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

[92]  T. Yanagida,et al.  Mechanical rotation of the c subunit oligomer in ATP synthase (F0F1): direct observation. , 1999, Science.

[93]  Masasuke Yoshida,et al.  The Role of the DELSEED Motif of the β Subunit in Rotation of F1-ATPase* , 2000, The Journal of Biological Chemistry.

[94]  Seth Lloyd,et al.  Obituary: Rolf Landauer (1927-99) , 1999, Nature.

[95]  H. Berg,et al.  Resurrection of the flagellar rotary motor near zero load , 2008, Proceedings of the National Academy of Sciences.

[96]  H. Arai,et al.  Topography and subunit stoichiometry of the coated vesicle proton pump. , 1988, The Journal of biological chemistry.

[97]  M. Homma,et al.  The conserved charged residues of the C-terminal region of FliG, a rotor component of the Na+-driven flagellar motor. , 2003, Journal of molecular biology.

[98]  Kazuhiko Kinosita,et al.  Pause and rotation of F1-ATPase during catalysis , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[99]  G. Murphy,et al.  In situ structure of the complete Treponema primitia flagellar motor , 2006, Nature.

[100]  A G Leslie,et al.  Molecular architecture of the rotary motor in ATP synthase. , 1999, Science.

[101]  H. Berg,et al.  Torque generated by the bacterial flagellar motor close to stall. , 1996, Biophysical journal.

[102]  Ichiro Yamato,et al.  Structure of the Rotor of the V-Type Na+-ATPase from Enterococcus hirae , 2005, Science.

[103]  M. Sherman,et al.  A novel type of energetics in a marine alkali‐tolerant bacterium , 1983 .

[104]  A. Mulkidjanian,et al.  Chromatophore vesicles of Rhodobacter capsulatus contain on average one F(O)F(1)-ATP synthase each. , 2002, Biophysical journal.

[105]  Howard C. Berg,et al.  Rapid rotation of flagellar bundles in swimming bacteria , 1987, Nature.

[106]  E. R. Kashket,et al.  Proton Motive Force During Growth of Streptococcus lactis Cells , 1980, Journal of bacteriology.

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

[108]  William S. Ryu,et al.  Torque-generating units of the flagellar motor of Escherichia coli have a high duty ratio , 2000, Nature.

[109]  W. Junge,et al.  Viscoelastic dynamics of actin filaments coupled to rotary F-ATPase: angular torque profile of the enzyme. , 2001, Biophysical journal.

[110]  C. Giersch,et al.  The stoichiometry of the chloroplast ATP synthase oligomer III in Chlamydomonas reinhardtii is not affected by the metabolic state. , 2004, Biochimica et biophysica acta.

[111]  M. Homma,et al.  Multimeric structure of the PomA/PomB channel complex in the Na+-driven flagellar motor of Vibrio alginolyticus. , 2004, Journal of biochemistry.

[112]  M. Homma,et al.  Ion-coupling determinants of Na+-driven and H+-driven flagellar motors. , 2003, Journal of molecular biology.

[113]  R. Macnab,et al.  Genetic evidence for a switching and energy-transducing complex in the flagellar motor of Salmonella typhimurium , 1986, Journal of bacteriology.

[114]  A. E. Senior,et al.  The properties of hybrid F1-ATPase enzymes suggest that a cyclical catalytic mechanism involving three catalytic sites occurs. , 1987, The Journal of biological chemistry.

[115]  Michael Börsch,et al.  Movements of the ε‐subunit during catalysis and activation in single membrane‐bound H+‐ATP synthase , 2005 .

[116]  C. Slayman,et al.  Quantitative measurements of membrane potential in Escherichia coli. , 1980, Biochemistry.

[117]  H. Berg,et al.  Successive incorporation of force-generating units in the bacterial rotary motor , 1984, Nature.

[118]  G. Wadhams,et al.  Stoichiometry and turnover in single, functioning membrane protein complexes , 2006, Nature.

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

[120]  M. Washizu,et al.  Dielectrophoretic measurement of bacterial motor characteristics , 1991, Conference Record of the 1991 IEEE Industry Applications Society Annual Meeting.

[121]  C. Hill,et al.  Structure of the C-terminal domain of FliG, a component of the rotor in the bacterial flagellar motor , 1999, Nature.

[122]  P. Boyer,et al.  The binding change mechanism for ATP synthase--some probabilities and possibilities. , 1993, Biochimica et biophysica acta.

[123]  R. H. Fillingame,et al.  Energy-transducing H+-ATPase of Escherichia coli. Reconstitution of proton translocation activity of the intrinsic membrane sector. , 1980, The Journal of biological chemistry.

[124]  A. Leslie,et al.  Structure of Bovine Mitochondrial F1-ATPase with Nucleotide Bound to All Three Catalytic Sites Implications for the Mechanism of Rotary Catalysis , 2001, Cell.

[125]  H C Berg,et al.  Torque-generating units of the bacterial flagellar motor step independently. , 1996, Biophysical journal.

[126]  Jan Pieter Abrahams,et al.  The crystal structure of the nucleotide-free α3β3 subcomplex of F1-ATPase from the thermophilic Bacillus PS3 is a symmetric trimer , 1997 .

[127]  N. Hirota,et al.  Flagellar motors of alkalophilic bacillus are powered by an electrochemical potential gradient of Na+ , 1981 .

[128]  M. Homma,et al.  Multimeric Structure of PomA, a Component of the Na+-driven Polar Flagellar Motor of Vibrio alginolyticus * , 2000, The Journal of Biological Chemistry.

[129]  Robert R. Ishmukhametov,et al.  Abundance of Escherichia coli F1-ATPase molecules observed to rotate via single-molecule microscopy with gold nanorod probes , 2007, Journal of bioenergetics and biomembranes.

[130]  H. Stahlberg,et al.  Bacterial Na+‐ATP synthase has an undecameric rotor , 2001, EMBO reports.

[131]  J. Walker,et al.  Primary structure and subunit stoichiometry of F1-ATPase from bovine mitochondria. , 1985, Journal of molecular biology.

[132]  P. Friedl,et al.  The isolated of F0 of escherichia coli ATP‐synthase is reconstitutively active in H+‐conduction and ATP‐dependent energy‐transduction , 1981, FEBS letters.

[133]  H. Berg,et al.  Constraints on flagellar rotation. , 1985, Journal of molecular biology.

[134]  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.

[135]  Daniel J. Muller,et al.  The c15 ring of the Spirulina platensis F‐ATP synthase: F1/F0 symmetry mismatch is not obligatory , 2005, EMBO reports.

[136]  J. Findlay,et al.  Evidence for a common structure for a class of membrane channels. , 1993, European journal of biochemistry.

[137]  S. Dunn,et al.  Localization of the delta subunit in the Escherichia coli F(1)F(0)-ATPsynthase by immuno electron microscopy: the delta subunit binds on top of the F(1). , 2000, Journal of molecular biology.

[138]  W. Junge,et al.  Proton channel of the chloroplast ATP synthase, CF0: Its time-averaged single-channel conductance as function of pH, temperature, isotopic and ionic medium composition , 1989, The Journal of Membrane Biology.

[139]  T. Nishi,et al.  The vacuolar (H+)-ATPases — nature's most versatile proton pumps , 2002, Nature Reviews Molecular Cell Biology.

[140]  Michio Homma,et al.  Torque-speed relationship of the Na+-driven flagellar motor of Vibrio alginolyticus. , 2003, Journal of molecular biology.

[141]  D. Blair,et al.  Charged residues of the rotor protein FliG essential for torque generation in the flagellar motor of Escherichia coli. , 1997, Journal of molecular biology.

[142]  P. Mitchell.  CHEMIOSMOTIC COUPLING IN OXIDATIVE AND PHOTOSYNTHETIC PHOSPHORYLATION , 1966, Biological reviews of the Cambridge Philosophical Society.

[143]  Masasuke Yoshida,et al.  One rotary mechanism for F1-ATPase over ATP concentrations from millimolar down to nanomolar. , 2005, Biophysical journal.

[144]  D. Blair,et al.  Residues of the cytoplasmic domain of MotA essential for torque generation in the bacterial flagellar motor. , 1997, Journal of molecular biology.

[145]  James R. Williams,et al.  Effects of Carbon Source on Expression of Fo Genes and on the Stoichiometry of the c Subunit in the F1Fo ATPase of Escherichia coli , 1998, Journal of bacteriology.

[146]  H. Berg,et al.  Restoration of torque in defective flagellar motors. , 1988, Science.

[147]  A. Mulkidjanian,et al.  Coupling of proton flow to ATP synthesis in Rhodobacter capsulatus: F(0)F(1)-ATP synthase is absent from about half of chromatophores. , 2001, Biochimica et biophysica acta.

[148]  H. Berg,et al.  The stall torque of the bacterial flagellar motor. , 1987, Biophysical journal.

[149]  Hirofumi Suzuki,et al.  Structure of the rotor of the bacterial flagellar motor revealed by electron cryomicroscopy and single-particle image analysis. , 2004, Journal of molecular biology.

[150]  W. Junge,et al.  Viscoelastic dynamics of actin filaments coupled to rotary F-ATPase: curvature as an indicator of the torque. , 2001, Biophysical journal.

[151]  G. Oster,et al.  Reverse engineering a protein: the mechanochemistry of ATP synthase. , 2000, Biochimica et biophysica acta.

[152]  M. Futai,et al.  H(+)-ATPase gamma subunit of Escherichia coli. Role of the conserved carboxyl-terminal region. , 1990, The Journal of biological chemistry.

[153]  T. Noumi,et al.  Nucleotide sequence of the genes for F0 components of the proton-translocating ATPase from Escherichia coli: prediction of the primary structure of F0 subunits. , 1981, Biochemical and biophysical research communications.

[154]  H. Berg,et al.  Absence of a barrier to backwards rotation of the bacterial flagellar motor demonstrated with optical tweezers. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

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

[156]  D. Blair,et al.  Function of Protonatable Residues in the Flagellar Motor of Escherichia coli: a Critical Role for Asp 32 of MotB , 1998, Journal of bacteriology.

[157]  K. Beyenbach,et al.  The V-type H+ ATPase: molecular structure and function, physiological roles and regulation , 2006, Journal of Experimental Biology.

[158]  A. Jagendorf,et al.  ATP formation caused by acid-base transition of spinach chloroplasts. , 1966, Proceedings of the National Academy of Sciences of the United States of America.

[159]  J. S. Parkinson,et al.  Bacterial motility: membrane topology of the Escherichia coli MotB protein. , 1988, Science.

[160]  Patrick Polzer,et al.  Structure of the Rotor Ring of F-Type Na+-ATPase from Ilyobacter tartaricus , 2005, Science.

[161]  M. Futai,et al.  Rotation of a complex of the gamma subunit and c ring of Escherichia coli ATP synthase. The rotor and stator are interchangeable. , 2001, The Journal of biological chemistry.

[162]  Michio Homma,et al.  Direct observation of steps in rotation of the bacterial flagellar motor , 2005, Nature.

[163]  H. Berg,et al.  Visualization of bacterial flagella by video-enhanced light microscopy , 1991, Journal of bacteriology.

[164]  R M Macnab,et al.  Examination of bacterial flagellation by dark-field microscopy , 1976, Journal of clinical microbiology.

[165]  T. Reese,et al.  FliN is a major structural protein of the C-ring in the Salmonella typhimurium flagellar basal body. , 1996, Journal of molecular biology.

[166]  Jan Pieter Abrahams,et al.  Structure at 2.8 Â resolution of F1-ATPase from bovine heart mitochondria , 1994, Nature.

[167]  Yoshiyuki Sowa,et al.  Bacterial flagellar motor , 2004, Quarterly Reviews of Biophysics.

[168]  Shin-Ichi Aizawa,et al.  Abrupt changes in flagellar rotation observed by laser dark-field microscopy , 1990, Nature.

[169]  I. Kawagishi,et al.  Very fast flagellar rotation , 1994, Nature.

[170]  Masasuke Yoshida,et al.  The rotor tip inside a bearing of a thermophilic F1-ATPase is dispensable for torque generation. , 2006, Biophysical journal.

[171]  M. Homma,et al.  The systematic substitutions around the conserved charged residues of the cytoplasmic loop of Na+-driven flagellar motor component PomA. , 2002, Journal of molecular biology.

[172]  J. Adler,et al.  Complementation of nonchemotactic mutants of Escherichia coli. , 1969, Genetics.

[173]  R. Macnab,et al.  Deletion Analysis of the Flagellar Switch Protein FliG of Salmonella , 2000, Journal of bacteriology.

[174]  M. Surette,et al.  Signal transduction in bacterial chemotaxis , 1992, The Journal of biological chemistry.

[175]  M. Futai,et al.  Rotational Catalysis of Escherichia coli ATP Synthase F1 Sector , 2007, Journal of Biological Chemistry.

[176]  D. Blair,et al.  Features of MotA proton channel structure revealed by tryptophan-scanning mutagenesis. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[177]  S. Kojima,et al.  Conformational change in the stator of the bacterial flagellar motor. , 2001, Biochemistry.

[178]  Kiwamu Saito,et al.  The γ-subunit rotation and torque generation in F1-ATPase from wild-type or uncoupled mutant Escherichia coli , 1999 .

[179]  S. Chervitz,et al.  The two-component signaling pathway of bacterial chemotaxis: a molecular view of signal transduction by receptors, kinases, and adaptation enzymes. , 1997, Annual review of cell and developmental biology.

[180]  A. Roujeinikova,et al.  Cloning, purification and crystallization of MotB, a stator component of the proton-driven bacterial flagellar motor , 2008, Acta crystallographica. Section F, Structural biology and crystallization communications.

[181]  K. Oosawa,et al.  M ring, S ring and proximal rod of the flagellar basal body of Salmonella typhimurium are composed of subunits of a single protein, FliF. , 1992, Journal of molecular biology.

[182]  K. Saito,et al.  ATP synthase F(1) sector rotation. Defective torque generation in the beta subunit Ser-174 to Phe mutant and its suppression by second mutations. , 2001, The Journal of biological chemistry.

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

[184]  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.

[185]  Daniel J. Muller,et al.  The Oligomeric State of c Rings from Cyanobacterial F-ATP Synthases Varies from 13 to 15 , 2007, Journal of bacteriology.