The Structure of ATPsynthases in Photosynthesis and Respiration

  • Bettina BöttcherEmail author
  • Peter Gräber
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 39)


A large number of biochemical reactions in cells are coupled with the hydrolysis of ATP, e.g. biosynthesis, ion translocation, muscle contraction. The largest amount of ATP is generated by F-type H+-ATPases, which are membrane integrated enzymes occurring in the cytoplasma membranes of bacteria, inner mitochondrial membranes and thylakoid membranes. Together with A-type and V-type ATPases they form a specific protein family, which couples proton (Na+) translocation across the membrane with the synthesis or hydrolysis of ATP. ATPases of this family are found in all taxonomic kingdoms and comprise F-ATPases, A-ATPases in Archaea and some bacteria and V-ATPases in the inner membranes of eukaryotes. A- and F-ATPases can function in ATP hydrolysis and ATP synthesis, although their main physiological role is ATP synthesis in most organisms. In contrast, V-ATPases are dedicated proton pumps, which work only in the direction of ATP hydrolysis. The predecessor of these ATPases was already present in the last universal common ancestor and probably might have evolved from RNA transporting translocases, which were located in the primordial membranes. Due to this evolutionary relationship, A-, V- and F-ATPases have a common architecture, which comprises a membrane-embedded part (F0, A0 or V0) and an extrinsic part (F1, A1 or V1) separated by a connecting region. This architecture supports a rotary mechanism, in which the rotation of the membrane- embedded part is concomitant with the transport of H+ (or Na+) across the membrane. The rotation of the membrane-embedded rotor is conveyed via a central stalk in the connecting region to the extrinsic part, where it is coupled to conformational changes in the catalytic nucleotide binding sites that support ATP synthesis/hydrolysis. An additional peripheral connection between the extrinsic part and the membrane bound part prevents the co-rotation of the extrinsic part and thus supports efficient coupling. Although, atomic structures of the holoenzymes are still missing, atomic models of sub-complexes and subunits give detailed insights into how the rotary mechanism couples ion-translocation with ATP synthesis/hydrolysis in this protein family.


Nucleotide Binding Site Proton Translocation Central Shaft Peripheral Stator Rotational Coupling 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



– Amino acid;


– Archaeal ATPase/ATPsynthase;


– Adenosine diphosphate;


– Adenosine triphosphate;


– Electron microscopy;


– F-type ATPase/ATPsynthase;


– Fluorescence resonance energy transfer;


– Last universal common ancestor;


– Inorganic phosphate;


– Vacuolar-type H+-ATPase



The authors thank the Deutsche Forschungsgemeinschaft for continued support. BB acknowledges support from the Darwin Trust of Edinburgh and the EU NoE 3D-Repertoire.


  1. Abrahams JP, Leslie AG, Lutter R, Walker JE (1994) Structure at 2.8 A resolution of F1-ATPase from bovine heart mitochondria. Nature 370:621–628PubMedCrossRefGoogle Scholar
  2. Arnold I, Pfeiffer K, Neupert W, Stuart RA, Schägger H (1998) Yeast mitochondrial F1F0-ATP synthase exists as a dimer: identification of three dimer-specific subunits. EMBO J 17:7170–7178PubMedCentralPubMedCrossRefGoogle Scholar
  3. Bernal RA, Stock D (2004) Three-dimensional structure of the intact Thermus thermophilus H+-ATPase/synthase by electron microscopy. Structure (Camb) 12:1789–1798CrossRefGoogle Scholar
  4. Bienert R, Rombach-Riegraf V, Diez M, Gräber P (2009) Subunit movements in single membrane-bound H+-ATP synthases from chloroplasts during ATP synthesis. J Biol Chem 284:36240–36247PubMedCentralPubMedCrossRefGoogle Scholar
  5. Bienert R, Zimmermann B, Rombach-Riegraf V, Gräber P (2011) Time-dependent FRET with single enzymes: domain motions and catalysis in H(+) -ATP Synthases. Chemphyschem 12:507–510Google Scholar
  6. Böttcher B, Schwarz L, Gräber P (1998) Direct indication for the existence of a double stalk in CF0F1. J Mol Biol 281:757–762PubMedCrossRefGoogle Scholar
  7. Böttcher B, Bertsche I, Reuter R, Gräber P (2000) Direct visualisation of conformational changes in EF0F1 by electron microscopy. J Mol Biol 296:449–457PubMedCrossRefGoogle Scholar
  8. Boyer PD (1993) The binding change mechanism for ATP synthase–some probabilities and possibilities. Biochim Biophys Acta 1140:215–250PubMedCrossRefGoogle Scholar
  9. Bultema JB, Braun HP, Boekema EJ, Kouril R (2009) Megacomplex organization of the oxidative phosphorylation system by structural analysis of respiratory supercomplexes from potato. Biochim Biophys Acta 1787:60–67PubMedCrossRefGoogle Scholar
  10. Cingolani G, Duncan TM (2011) Structure of the ATP synthase catalytic complex (F(1)) from Escherichia coli in an autoinhibited conformation. Nat Struct Mol Biol 18:701–707PubMedCentralPubMedCrossRefGoogle Scholar
  11. Claggett SB, O’Neil Plancher M, Dunn SD, Cain BD (2009) The b subunits in the peripheral stalk of F1F0 ATP synthase preferentially adopt an offset relationship. J Biol Chem 284:16531–16540PubMedCentralPubMedCrossRefGoogle Scholar
  12. Collinson IR, Runswick MJ, Buchanan SK, Fearnley IM, Skehel JM, van Raaij MJ, Griffiths DE, Walker JE (1994) Fo membrane domain of ATP synthase from bovine heart mitochondria: purification, subunit composition, and reconstitution with F1-ATPase. Biochemistry 33:7971–7978PubMedCrossRefGoogle Scholar
  13. Daum B, Nicastro D, Austin J 2nd, McIntosh JR, Kühlbrandt W (2010) Arrangement of photosystem II and ATP synthase in chloroplast membranes of spinach and pea. Plant Cell 22:1299–1312PubMedCentralPubMedCrossRefGoogle Scholar
  14. Dautant A, Velours J, Giraud MF (2010) Crystal structure of the Mg.ADP-inhibited state of the yeast F1c10-ATP synthase. J Biol Chem 285:29502–29510PubMedCentralPubMedCrossRefGoogle Scholar
  15. Del Rizzo PA, Bi Y, Dunn SD, Shilton BH (2002) The “second stalk” of Escherichia coli ATP synthase: structure of the isolated dimerization domain. Biochemistry 41:6875–6884PubMedCrossRefGoogle Scholar
  16. Dickson VK, Silvester JA, Fearnley IM, Leslie AG, Walker JE (2006) On the structure of the stator of the mitochondrial ATP synthase. EMBO J 25:2911–2918PubMedCentralPubMedCrossRefGoogle Scholar
  17. Diepholz M, Börsch M, Böttcher B (2008a) Structural organization of the V-ATPase and its implications for regulatory assembly and disassembly. Biochem Soc Trans 36:1027–1031PubMedCrossRefGoogle Scholar
  18. Diepholz M, Venzke D, Prinz S, Batisse C, Flörchinger B, Rössle M, Svergun DI, Böttcher B, Fethiere J (2008b) A different conformation for EGC stator subcomplex in solution and in the assembled yeast V-ATPase: possible implications for regulatory disassembly. Structure 16:1789–1798PubMedCrossRefGoogle Scholar
  19. Diez M, Zimmermann B, Börsch M, König M, Schweinberger E, Steigmiller S, Reuter R, Felekyan S, Kudryavtsev V, Seidel CA, Gräber P (2004) Proton-powered subunit rotation in single membrane-bound F0F1-ATP synthase. Nat Struct Mol Biol 11:135–141PubMedCrossRefGoogle Scholar
  20. Dmitriev O, Jones PC, Jiang W, Fillingame RH (1999) Structure of the membrane domain of subunit b of the Escherichia coli F0F1 ATP synthase. J Biol Chem 274:15598–15604PubMedCrossRefGoogle Scholar
  21. Drory O, Frolow F, Nelson N (2004) Crystal structure of yeast V-ATPase subunit C reveals its stator function. EMBO Rep 5:1148–1152PubMedCentralPubMedCrossRefGoogle Scholar
  22. Dudkina NV, Eubel H, Keegstra W, Boekema EJ, Braun HP (2005a) Structure of a mitochondrial supercomplex formed by respiratory-chain complexes I and III. Proc Natl Acad Sci U S A 102:3225–3229PubMedCentralPubMedCrossRefGoogle Scholar
  23. Dudkina NV, Heinemeyer J, Keegstra W, Boekema EJ, Braun HP (2005b) Structure of dimeric ATP synthase from mitochondria: an angular association of monomers induces the strong curvature of the inner membrane. FEBS Lett 579:5769–5772PubMedCrossRefGoogle Scholar
  24. Dudkina NV, Kudryashev M, Stahlberg H, Boekema EJ (2011) Interaction of complexes I, III, and IV within the bovine respirasome by single particle cryoelectron tomography. Proc Natl Acad Sci U S A 108:15196–15200PubMedCentralPubMedCrossRefGoogle Scholar
  25. Esteban O, Bernal RA, Donohoe M, Videler H, Sharon M, Robinson CV, Stock D (2008) Stoichiometry and localization of the stator subunits E and G in Thermus thermophilus H+-ATPase/synthase. J Biol Chem 283:2595–2603PubMedCrossRefGoogle Scholar
  26. Förster K, Turina P, Drepper F, Haehnel W, Fischer S, Gräber P, Petersen J (2010) Proton transport coupled ATP synthesis by the purified yeast H+-ATP synthase in proteoliposomes. Biochim Biophys Acta 1797:1828–1837PubMedCrossRefGoogle Scholar
  27. Furuike S, Hossain MD, Maki Y, Adachi K, Suzuki T, Kohori A, Itoh H, Yoshida M, Kinosita K Jr (2008) Axle-less F1-ATPase rotates in the correct direction. Science 319:955–958PubMedCrossRefGoogle Scholar
  28. Gibbons C, Montgomery MG, Leslie AG, Walker JE (2000) The structure of the central stalk in bovine F1-ATPase at 2.4 Å resolution. Nat Struct Biol 7:1055–1061PubMedCrossRefGoogle Scholar
  29. Giraud MF, Paumard P, Soubannier V, Vaillier J, Arselin G, Salin B, Schaeffer J, Brethes D, di Rago JP, Velours J (2002) Is there a relationship between the supramolecular organization of the mitochondrial ATP synthase and the formation of cristae? Biochim Biophys Acta 1555:174–180PubMedCrossRefGoogle Scholar
  30. Gogarten JP, Starke T, Kibak H, Fishman J, Taiz L (1992) Evolution and isoforms of V-ATPase subunits. J Exp Biol 172:137–147PubMedGoogle Scholar
  31. Gomis-Ruth FX, Moncalian G, Perez-Luque R, Gonzalez A, Cabezon E, de la Cruz F, Coll M (2001) The bacterial conjugation protein TrwB resembles ring helicases and F1- ATPase. Nature 409:637–641PubMedCrossRefGoogle Scholar
  32. Hausrath AC, Capaldi RA, Matthews BW (2001) The conformation of the epsilon- and gamma-subunits within the Escherichia coli F1 ATPase. J Biol Chem 276:47227–47232PubMedCrossRefGoogle Scholar
  33. Iwata M, Imamura H, Stambouli E, Ikeda C, Tamakoshi M, Nagata K, Makyio H, Hankamer B, Barber J, Yoshida M, Yokoyama K, Iwata S (2004) Crystal structure of a central stalk subunit C and reversible association/dissociation of vacuole-type ATPase. Proc Natl Acad Sci U S A 101:59–64PubMedCentralPubMedCrossRefGoogle Scholar
  34. Jefferies KC, Forgac M (2008) Subunit H of the vacuolar (H+) ATPase inhibits ATP hydrolysis by the free V1 domain by interaction with the rotary subunit F. J Biol Chem 283:4512–4519PubMedCentralPubMedCrossRefGoogle Scholar
  35. Junge W, Lill H, Engelbrecht S (1997) ATP synthase: an electrochemical transducer with rotatory mechanics. Trends Biochem Sci 22:420–423PubMedCrossRefGoogle Scholar
  36. Kabaleeswaran V, Shen H, Symersky J, Walker JE, Leslie AG, Mueller DM (2009) Asymmetric structure of the yeast F1 ATPase in the absence of bound nucleotides. J Biol Chem 284:10546–10551PubMedCentralPubMedCrossRefGoogle Scholar
  37. Kane PM (1995) Disassembly and reassembly of the yeast vacuolar H+-ATPase in vivo. J Biol Chem 270:17025–17032PubMedGoogle Scholar
  38. Karrasch S, Walker JE (1999) Novel features in the structure of bovine ATP synthase. J Mol Biol 290:379–384PubMedCrossRefGoogle Scholar
  39. Kibak H, Taiz L, Starke T, Bernasconi P, Gogarten JP (1992) Evolution of structure and function of V-ATPases. J Bioenerg Biomembr 24:415–424PubMedCrossRefGoogle Scholar
  40. Kitagawa N, Mazon H, Heck AJ, Wilkens S (2008) Stoichiometry of the peripheral stalk subunits E and G of yeast V1-ATPase determined by mass spectrometry. J Biol Chem 283:3329–3337PubMedCrossRefGoogle Scholar
  41. Lapierre P, Shial R, Gogarten JP (2006) Distribution of F- and A/V-type ATPases in Thermus scotoductus and other closely related species. Syst Appl Microbiol 29:15–23PubMedCrossRefGoogle Scholar
  42. Lau WC, Rubinstein JL (2010) Structure of intact Thermus thermophilus V-ATPase by cryo-EM reveals organization of the membrane-bound VO motor. Proc Natl Acad Sci U S A 107:1367–1372PubMedCentralPubMedCrossRefGoogle Scholar
  43. Lau WC, Baker LA, Rubinstein JL (2008) Cryo-EM structure of the yeast ATP synthase. J Mol Biol 382:1256–1264PubMedCrossRefGoogle Scholar
  44. Lee LK, Stewart AG, Donohoe M, Bernal RA, Stock D (2010) The structure of the peripheral stalk of Thermus thermophilus H+-ATPase/synthase. Nat Struct Mol Biol 17:373–378PubMedCentralPubMedCrossRefGoogle Scholar
  45. Maher MJ, Akimoto S, Iwata M, Nagata K, Hori Y, Yoshida M, Yokoyama S, Iwata S, Yokoyama K (2009) Crystal structure of A3B3 complex of V-ATPase from Thermus thermophilus. EMBO J 28:3771–3779PubMedCentralPubMedCrossRefGoogle Scholar
  46. Meier T, Matthey U, Henzen F, Dimroth P, Müller DJ (2001) The central plug in the reconstituted undecameric c cylinder of a bacterial ATP synthase consists of phospholipids. FEBS Lett 505:353–356PubMedCrossRefGoogle Scholar
  47. Meier T, Polzer P, Diederichs K, Welte W, Dimroth P (2005) Structure of the rotor ring of F-Type Na+-ATPase from Ilyobacter tartaricus. Science 308:659–662PubMedCrossRefGoogle Scholar
  48. Meier T, Krah A, Bond PJ, Pogoryelov D, Diederichs K, Faraldo-Gomez JD (2009) Complete ion-coordination structure in the rotor ring of Na+-dependent F-ATP synthases. J Mol Biol 391:498–507PubMedCrossRefGoogle Scholar
  49. Mellwig C, Böttcher B (2003) A unique resting position of the ATP-synthase from chloroplasts. J Biol Chem 278:18544–18549PubMedCrossRefGoogle Scholar
  50. Meyer B, Wittig I, Trifilieff E, Karas M, Schägger H (2007) Identification of two proteins associated with mammalian ATP synthase. Mol Cell Proteomics 6:1690–1699PubMedCrossRefGoogle Scholar
  51. Minauro-Sanmiguel F, Wilkens S, Garcia JJ (2005) Structure of dimeric mitochondrial ATP synthase: novel F0 bridging features and the structural basis of mitochondrial cristae biogenesis. Proc Natl Acad Sci U S A 102:12356–12358PubMedCentralPubMedCrossRefGoogle Scholar
  52. Mitchell (1961) Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 191:144–148PubMedCrossRefGoogle Scholar
  53. Mnatsakanyan N, Hook JA, Quisenberry L, Weber J (2009) ATP synthase with its gamma subunit reduced to the N-terminal helix can still catalyze ATP synthesis. J Biol Chem 284:26519–26525PubMedCentralPubMedCrossRefGoogle Scholar
  54. Muench SP, Huss M, Song CF, Phillips C, Wieczorek H, Trinick J, Harrison MA (2009) Cryo-electron microscopy of the vacuolar ATPase motor reveals its mechanical and regulatory complexity. J Mol Biol 386:989–999PubMedCrossRefGoogle Scholar
  55. Mulkidjanian AY, Makarova KS, Galperin MY, Koonin EV (2007) Inventing the dynamo machine: the evolution of the F-type and V-type ATPases. Nat Rev Microbiol 5:892–899PubMedCrossRefGoogle Scholar
  56. Murata T, Arechaga I, Fearnley IM, Kakinuma Y, Yamato I, Walker JE (2003) The membrane domain of the Na+-motive V-ATPase from Enterococcus hirae contains a heptameric rotor. J Biol Chem 278:21162–21167PubMedCrossRefGoogle Scholar
  57. Murata T, Yamato I, Kakinuma Y, Leslie AG, Walker JE (2005) Structure of the rotor of the V-Type Na+-ATPase from Enterococcus hirae. Science 308:654–659PubMedCrossRefGoogle Scholar
  58. Nelson N, Nelson H, Racker E (1972) Partial resolution of the enzymes catalyzing photophosphorylation. XII. Purification and properties of an inhibitor isolated from chloroplast coupling factor 1. J Biol Chem 247:7657–7662PubMedGoogle Scholar
  59. Noji H (1998) The rotary enzyme of the cell: the rotation of F1-ATPase. Science 282:1844–1845PubMedCrossRefGoogle Scholar
  60. Numoto N, Hasegawa Y, Takeda K, Miki K (2009) Inter-subunit interaction and quaternary rearrangement defined by the central stalk of prokaryotic V1-ATPase. EMBO Rep 10:1228–1234PubMedCentralPubMedCrossRefGoogle Scholar
  61. Olendzenski L, Liu L, Zhaxybayeva O, Murphey R, Shin DG, Gogarten JP (2000) Horizontal transfer of archaeal genes into the deinococcaceae: detection by molecular and computer-based approaches. J Mol Evol 51:587–599PubMedCrossRefGoogle Scholar
  62. 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 15:935–941PubMedCentralPubMedCrossRefGoogle Scholar
  63. Parra KJ, Keenan KL, Kane PM (2000) The H subunit (Vma13p) of the yeast V-ATPase inhibits the ATPase activity of cytosolic V1 complexes. J Biol Chem 275:21761–21767PubMedCrossRefGoogle Scholar
  64. Pogoryelov D, Yu J, Meier T, Vonck J, Dimroth P, Müller DJ (2005) The c15 ring of the Spirulina platensis F-ATP synthase: F1/F0 symmetry mismatch is not obligatory. EMBO Rep 6:1040–1044PubMedCentralPubMedCrossRefGoogle Scholar
  65. Pogoryelov D, Yildiz O, Faraldo-Gomez JD, Meier T (2009) High-resolution structure of the rotor ring of a proton-dependent ATP synthase. Nat Struct Mol Biol 16:1068–1073PubMedCrossRefGoogle Scholar
  66. Preiss L, Yildiz O, Hicks DB, Krulwich TA, Meier T (2010) A new type of proton coordination in an F(1)F(o)-ATP synthase rotor ring. PLoS Biol 8:e1000443PubMedCentralPubMedCrossRefGoogle Scholar
  67. Priya R, Tadwal VS, Roessle MW, Gayen S, Hunke C, Peng WC, Torres J, Gruber G (2008) Low resolution structure of subunit b (b (22-156)) of Escherichia coli F(1)F(O) ATP synthase in solution and the b-delta assembly. J Bioenerg Biomembr 40:245–255PubMedCrossRefGoogle Scholar
  68. Rees DM, Leslie AG, Walker JE (2009) The structure of the membrane extrinsic region of bovine ATP synthase. Proc Natl Acad Sci U S A 21:21597Google Scholar
  69. Rodgers AJW, Wilce MC (2000) Structure of the gamma-epsilon complex of ATP synthase. Nat Struct Biol 7:1051–1054PubMedCrossRefGoogle Scholar
  70. Rubinstein JL, Walker JE, Henderson R (2003) Structure of the mitochondrial ATP synthase by electron cryomicroscopy. EMBO J 22:6182–6192PubMedCentralPubMedCrossRefGoogle Scholar
  71. Rubinstein JL, Dickson VK, Runswick MJ, Walker JE (2005) ATP synthase from Saccharomyces cerevisiae: location of subunit h in the peripheral stalk region. J Mol Biol 345:513–520PubMedCrossRefGoogle Scholar
  72. Sagermann M, Stevens TH, Matthews BW (2001) Crystal structure of the regulatory subunit H of the V-type ATPase of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 98:7134–7139PubMedCentralPubMedCrossRefGoogle Scholar
  73. Schäfer E, Dencher NA, Vonck J, Parcej DN (2007) Three-dimensional structure of the respiratory chain supercomplex I1III2IV1 from bovine heart mitochondria. Biochemistry 46:12579–12585PubMedCrossRefGoogle Scholar
  74. Schägger H, Pfeiffer K (2000) Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J 19:1777–1783PubMedCentralPubMedCrossRefGoogle Scholar
  75. Seelert H, Dencher NA, Müller DJ (2003) Fourteen protomers compose the oligomer III of the proton-rotor in spinach chloroplast ATP synthase. J Mol Biol 333:337–344PubMedCrossRefGoogle Scholar
  76. Shao E, Nishi T, Kawasaki-Nishi S, Forgac M (2003) Mutational analysis of the non-homologous region of subunit A of the yeast V-ATPase. J Biol Chem 278:12985–12991PubMedCrossRefGoogle Scholar
  77. Shirakihara Y, Leslie AG, Abrahams JP, Walker JE, Ueda T, Sekimoto Y, Kambara M, Saika K, Kagawa Y, Yoshida M (1997) The crystal structure of the nucleotide-free alpha 3 beta 3 subcomplex of F1-ATPase from the thermophilic Bacillus PS3 is a symmetric trimer. Structure 5:825–836PubMedCrossRefGoogle Scholar
  78. Sielaff H, Rennekamp H, Wächter A, Xie H, Hilbers F, Feldbauer K, Dunn SD, Engelbrecht S, Junge W (2008) Domain compliance and elastic power transmission in rotary F(O)F(1)-ATPase. Proc Natl Acad Sci U S A 105:17760–17765PubMedCentralPubMedCrossRefGoogle Scholar
  79. Smith JB, Sternweis PC (1977) Purification of membrane attachment and inhibitory subunits of the proton translocating adenosine triphosphatase from Escherichia coli. Biochemistry 16:306–311PubMedCrossRefGoogle Scholar
  80. Srinivasan S, Vyas NK, Baker ML, Quiocho FA (2011) Crystal structure of the cytoplasmic N-terminal domain of subunit I, a homolog of subunit a, of V-ATPase. J Mol Biol 412:14–21PubMedCentralPubMedCrossRefGoogle Scholar
  81. Steigmiller S, Börsch M, Gräber P, Huber M (2005) Distances between the b-subunits in the tether domain of F(0)F(1)-ATP synthase from E. coli. Biochim Biophys Acta 1708:143–153PubMedCrossRefGoogle Scholar
  82. Stock D, Leslie AG, Walker JE (1999) Molecular architecture of the rotary motor in ATP synthase. Science 286:1700–1705PubMedCrossRefGoogle Scholar
  83. Strauss M, Hofhaus G, Schröder RR, Kühlbrandt W (2008) Dimer ribbons of ATP synthase shape the inner mitochondrial membrane. EMBO J 27:1154–1160PubMedCentralPubMedCrossRefGoogle Scholar
  84. Sumner JP, Dow JA, Earley FG, Klein U, Jäger D, Wieczorek H (1995) Regulation of plasma membrane V-ATPase activity by dissociation of peripheral subunits. J Biol Chem 270:5649–5653PubMedCrossRefGoogle Scholar
  85. Tsunoda SP, Rodgers AJ, Aggeler R, Wilce MC, Yoshida M, Capaldi RA (2001) Large conformational changes of the epsilon subunit in the bacterial F1F0 ATP synthase provide a ratchet action to regulate this rotary motor enzyme. Proc Natl Acad Sci U S A 98:6560–6564PubMedCentralPubMedCrossRefGoogle Scholar
  86. Tuller T, Birin H, Gophna U, Kupiec M, Ruppin E (2010) Reconstructing ancestral gene content by coevolution. Genome Res 20:122–132PubMedCentralPubMedCrossRefGoogle Scholar
  87. Uchihashi T, Iino R, Ando T, Noji H (2011) High-speed atomic force microscopy reveals rotary catalysis of rotorless F-ATPase. Science 333:755–758PubMedCrossRefGoogle Scholar
  88. Venzke D, Domgall I, Köcher T, Fethiere J, Fischer S, Böttcher B (2005) Elucidation of the stator organization in the V-ATPase of Neurospora crassa. J Mol Biol 349:659–669PubMedCrossRefGoogle Scholar
  89. Vollmar M, Schlieper D, Winn M, Büchner C, Groth G (2009) Structure of the c14 rotor ring of the proton translocating chloroplast ATP synthase. J Biol Chem 284:18228–18235PubMedCentralPubMedCrossRefGoogle Scholar
  90. Vonck J, Pisa KY, Morgner N, Brutschy B, Müller V (2009) Three-dimensional structure of A1A0 ATP synthase from the hyperthermophilic archaeon Pyrococcus furiosus by electron microscopy. J Biol Chem 284:10110–10119PubMedCentralPubMedCrossRefGoogle Scholar
  91. Watt IN, Montgomery MG, Runswick MJ, Leslie AG, Walker JE (2010) Bioenergetic cost of making an adenosine triphosphate molecule in animal mitochondria. Proc Natl Acad Sci U S A 107:16823–16827PubMedCentralPubMedCrossRefGoogle Scholar
  92. Wilkens S, Capaldi RA (1998) Electron microscopic evidence of two stalks linking the F1 and F0 parts of the Escherichia coli ATP synthase. Biochim Biophys Acta 1365:93–97PubMedCrossRefGoogle Scholar
  93. Wilkens S, Inoue T, Forgac M (2004) Three-dimensional structure of the vacuolar ATPase. Localization of subunit H by difference imaging and chemical cross-linking. J Biol Chem 279:41942–41949PubMedCrossRefGoogle Scholar
  94. Wilkens S, Zhang Z, Zheng Y (2005) A structural model of the vacuolar ATPase from transmission electron microscopy. Micron 36:109–126PubMedCrossRefGoogle Scholar
  95. Zarivach R, Vuckovic M, Deng W, Finlay BB, Strynadka NC (2007) Structural analysis of a prototypical ATPase from the type III secretion system. Nat Struct Mol Biol 14:131–137PubMedCrossRefGoogle Scholar
  96. Zhang Z, Zheng Y, Mazon H, Milgrom E, Kitagawa N, Kish-Trier E, Heck AJ, Kane PM, Wilkens S (2008) Structure of the yeast vacuolar ATPase. J Biol Chem 283:35983–35995PubMedCentralPubMedCrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2014

Authors and Affiliations

  1. 1.School of Biological SciencesUniversity of EdinburghEdinburghUK
  2. 2.Institut für Physikalische ChemieAlbert-Ludwigs-Universität FreiburgFreiburgGermany

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