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The Purple Phototrophic Bacteria pp 475–493Cite as

Proton Translocation and ATP Synthesis by the FoF1-ATPase of Purple Bacteria

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Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 28))

Summary

In purple bacteria both the light driven and respiratory electron transfers serve the sole purpose of generating a proton-motive force across their inner membrane. The backflow of protons is monopolized by the enzyme FoF1-ATP synthase producing ATP from ADP and Pi. Almost all the useful work derived from absorbed sunlight is delivered to the cell in form of the ATP/ADP-couple in purple bacteria, whereas this accounts for only about 20% of the total in green plants and cyanobacteria. FoF1 is composed of two rotary motors; Fo uses a transmembrane proton motive force to generate torque and F1 uses the torque to synthesize ATP. When operating in reverse the enzyme generates proton motive force at the expense of ATP hydrolysis. Both portions are mechanically coupled by a central rotary shaft and held together by a peripheral stalk. Elasticity of mechanical power transmission is a prerequisite for high kinetic efficiency of the two motor/generators. Although being elastically coupled, they do not slip against each other, and under physiological conditions there is no proton leak without concomitant ATP synthesis. If the membrane is de-energized, the enzyme is inactivated. Re-activation requires a protonmotive force, and it is presumably achieved via proton driven rotation of Fo transmitted to F1. Therefore, proton translocation by the FoF1 has the dual functions of driving and regulating ATP synthesis. The subunit compositions and construction principles of FoF1ATP synthases of various prokaryotic and eukaryotic organisms are very similar. The enzymes from photosynthetic organisms have proven to be particularly useful for elucidating the electrochemical aspects, as emphasized in this article.

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Abbreviations

AFM:

atomic force microscopy

E. :

Escherichia

FoF1 :

F-type ion translocating ATP synthase

NMR:

nuclear magnetic resonance

Pi :

inorganic phosphate

Rba. :

Rhodobacter

TMH:

transmembrane helix

Δμ̃ +H :

transmembrane electrochemical potential difference of proton

References

  • Altendorf K and Zitzmann W (1975) Identification of the DCCD-reactive protein of the energy transducing adenosinetriphosphatase complex from Escherichia coli. FEBS Lett 59: 268–272

    PubMed  CAS  Google Scholar 

  • Althoff G, Lill H and Junge W (1989) Proton channel of the chloroplast ATP synthase, CFo: Its time-averaged single-channel conductance as function of pH, temperature, isotopic and ionic medium composition. J Membr Biol 108: 263–271

    CAS  Google Scholar 

  • Angevine CM and Fillingame RH (2003) Aqueous access channels in subunit a of rotary ATP synthase. J Biol Chem 278: 6066–6074

    PubMed  CAS  Google Scholar 

  • Angevine CM, Herold KA and Fillingame RH (2003) Aqueous access pathways in subunit a of rotary ATP synthase extend to both sides of the membrane. Proc Natl Acad Sci USA 100: 13179–13183

    PubMed  CAS  Google Scholar 

  • Baccarini-Melandri A, Gest H and Pietro AS (1970) A coupling factor in bacterial photophosphorylation. J Biol Chem 245: 1224–1226

    PubMed  CAS  Google Scholar 

  • Bakker-Grunwald T and Van Dam K (1973) The energy level associated with the light-triggered Mg2+-dependent ATPase in spinach chloroplasts. Biochim Biophys Acta 292: 808–814

    PubMed  CAS  Google Scholar 

  • Baltscheffsky M and Lundin A (1979) Flash-induced increase of ATPase activity in Rhodospirillum rubrum chromatophores. In: Mukohata Y, Packer L (eds) Cation Flux Across Biomembranes, pp 209–218. Academic Press, New York

    Google Scholar 

  • Birkenhager R, Hoppert M, Deckers-Hebestreit G, Mayer F and Altendorf K (1995) The F0 complex of the Escherichia coli ATP synthase. Investigation by electron spectroscopic imaging and immunoelectron microscopy. Eur J Biochem 230: 58–67

    PubMed  CAS  Google Scholar 

  • Cain BD and Simoni RD (1988) Interaction between Glu-219 and His-245 within the a-subunit of FOF1-ATPase in Escherichia coli. J Biol Chem 263: 6606–6612

    PubMed  CAS  Google Scholar 

  • Cappellini P, Turina P, Fregni V and Melandri BA (1997) Sulfite stimulates the ATP hydrolysis activity of but not proton translocation by the ATP synthase of Rhodobacter capsulatus and interferes with its activation by Δ̃ +H . Eur J Biochem 248: 496–506

    PubMed  CAS  Google Scholar 

  • Carmeli C and Lifshitz Y (1972) Effects of P 1 and ADP on ATPase activity in chloroplasts. Biochim Biophys Acta 267: 86–95

    PubMed  CAS  Google Scholar 

  • Casadio R and Melandri BA (1996) CaATP inhibition of the MgATP-dependent proton pump (H+-ATPase) in bacterial photosynthetic membranes with a mechanism of alternate substrate inhibition. J Bioinorg Chem 1: 284–291

    CAS  Google Scholar 

  • Cherepanov DA and Junge W (2001) Viscoelastic dynamics of actin filaments coupled to rotary F-ATPase: Curvature as an indicator of the torque. Biophys J 81: 1234–1244

    PubMed  CAS  Google Scholar 

  • Cherepanov DA, Mulkidjanian AY and Junge W (1999) Transient accumulation of elastic energy in proton translocating ATP synthase. FEBS Lett 449: 1–6

    PubMed  CAS  Google Scholar 

  • Collinson IR, Runswick MJ, Buchanan SK, Fearnley IM, Skehel JM, van Raaij MJ, Griffiths DE and Walker JE (1994) Fo membrane domain of ATP synthase from bovine heart mitochondria: Purification, subunit composition, and reconstitution with F1-ATPase. Biochemistry 33: 7971–7978

    PubMed  CAS  Google Scholar 

  • Crofts AR and Wraight CA (1983) The electrochemical domain of photosynthesis. Biochim Biophys Acta 726: 149–185

    CAS  Google Scholar 

  • Cukierman S (2000) Proton mobilities in water and in different stereoisomers of covalently linked gramicidin A channels. Biophys J 78: 1825–1834

    PubMed  CAS  Google Scholar 

  • Del Rizzo PA, Bi Y and Dunn SD (2006) ATP synthase b subunit dimerization domain: A right-handed coiled coil with offset helices. J Mol Biol 364: 735–746

    PubMed  Google Scholar 

  • DeLeon-Rangel J, Zhang D and Vik SB (2003) The role of transmembrane span 2 in the structure and function of subunit a of the ATP synthase from Escherichia coli. Arch Biochem Biophys 418: 55–62

    PubMed  CAS  Google Scholar 

  • Dickson VK, Silvester JA, Fearnley IM, Leslie AG and Walker JE (2006) On the structure of the stator of the mitochondrial ATP synthase. EMBO J 25: 2911–2918

    PubMed  CAS  Google Scholar 

  • Diez M, Zimmermann B, Borsch M, Konig M, Schweinberger E, Steigmiller S, Reuter R, Felekyan S, Kudryavtsev V, Seidel CA and Graber P (2004) Proton-powered subunit rotation in single membrane-bound FOF1-ATP synthase. Nat Struct Mol Biol 11: 135–141

    PubMed  CAS  Google Scholar 

  • Dimroth P (1994) Bacterial sodium ion-coupled energetics. Antonie Van Leeuwenhoek 65: 381–395

    PubMed  CAS  Google Scholar 

  • Dimroth P, Wang H, Grabe M and Oster G (1999) Energy transduction in the sodium F-ATPase of Propionigenium modestum. Proc Natl Acad Sci USA 96: 4924–4929

    PubMed  CAS  Google Scholar 

  • Dimroth P, Matthey U, and Kaim G (2000) Critical evaluation of the one-versus the two-channel model for the operation of the ATP synthase’s F(o) motor. Biochim Biophys Acta 1459: 506–513

    PubMed  CAS  Google Scholar 

  • Dmitriev OY and Fillingame RH (2001) Structure of Ala(20) → Pro/Pro(64) → Ala substituted subunit c of Escherichia coli ATP synthase in which the essential proline is switched between transmembrane helices. J Biol Chem 276: 27449–27454

    PubMed  CAS  Google Scholar 

  • Drobinskaya IY, Kozlov IA, Murataliev MB and Vulfson EN (1985) Tightly bound adenosine diphosphate, which inhibits the activity of mitochondrial F1-ATPase, is located at the catalytic site of the enzyme. FEBS Lett 182: 419–424

    PubMed  CAS  Google Scholar 

  • Duncan TM, Bulygin W, Zhou Y, Hutcheon ML and Cross RL (1995) Rotation of subunits during catalysis by Escherichia coli F1-ATPase. Proc Natl Acad Sci USA 92: 10964–10968

    PubMed  CAS  Google Scholar 

  • Dunham KR and Selman BR (1981) Interactions of inorganic phosphate with spinach coupling factor 1. Effects on ATPase and ADP binding activities. J Biol Chem 256: 10044–10049

    PubMed  CAS  Google Scholar 

  • Dunn SD, McLachlin DT and Revington M (2000a) The second stalk of Escherichia coli ATP synthase. Biochim Biophys Acta 1458: 356–363

    PubMed  CAS  Google Scholar 

  • Dunn SD, Revington M, Cipriano DJ and Shilton BH (2000b) The b subunit of Escherichia coli ATP synthase. J Bioenerg Biomembr 32: 347–355

    PubMed  CAS  Google Scholar 

  • Elston T, Wang H, and Oster G (1998) Energy transduction in ATP synthase. Nature 391: 510–513

    PubMed  CAS  Google Scholar 

  • Emrich HM, Junge W and Witt HT (1969) Further evidence for an optical response of chloroplast bulk pigments to a light induced electrical field in photosynthesis. Z Naturforsch B 24: 1144–1146

    PubMed  CAS  Google Scholar 

  • Feng Y and McCarty RE (1990) Purification and reconstitution of active chloroplast F0. J Biol Chem 265: 5104–5109

    PubMed  CAS  Google Scholar 

  • Feniouk BA and Junge W (2005) Regulation of the F0F1-ATP synthase: The conformation of subunit s might be determined by directionality of subunit γ rotation. FEBS Lett 579: 5114–5118

    PubMed  CAS  Google Scholar 

  • Feniouk BA, Cherepanov DA, Junge W and Mulkidjanian AY (2001) Coupling of proton flow to ATP synthesis in Rhodobacter capsulatus: FOF1-ATP synthase is absent from about half of chromatophores. Biochim Biophys Acta 1506: 189–203

    PubMed  CAS  Google Scholar 

  • Feniouk BA, Cherepanov DA, Voskoboynikova NE, Mulkidjanian AY and Junge W (2002) Chromatophore vesicles of Rhodobacter capsulatus contain on average one FOF1-ATP synthase each. Biophys J 82: 1115–1122

    PubMed  CAS  Google Scholar 

  • Feniouk BA, Kozlova MA, Knorre DA, Cherepanov DA, Mulkidjanian AY and Junge W (2004) The proton driven rotor of ATP synthase: Ohmic conductance (10 fS), and absence of voltage gating. Biophys J 86: 4094–4109

    PubMed  CAS  Google Scholar 

  • Feniouk BA, Mulkidjanian AY and Junge W (2005) Proton slip in the ATP synthase of Rhodobacter capsulatus: induction, proton conduction, and nucleotide dependence. Biochim Biophys Acta 1706: 184–194

    PubMed  CAS  Google Scholar 

  • Feniouk BA, Suzuki T and Yoshida M (2006) The role of subunit epsilon in the catalysis and regulation of F0F1-ATP synthase. Biochim Biophys Acta 1757: 326–338

    PubMed  CAS  Google Scholar 

  • Feniouk BA, Suzuki T and Yoshida M (2007) Regulatory Interplay between proton motive force, ADP, phosphate, and subunit-epsilon in bacterial ATP synthase. J Biol Chem 282: 764–772

    PubMed  CAS  Google Scholar 

  • Fillingame RH (1975) Identification of the dicyclohexylcarbodiimide-reactive protein component of the adenosine 5′-triphosphate energy-transducing system of Escherichia coli. J Bacteriol 124: 870–883

    PubMed  CAS  Google Scholar 

  • Fillingame RH and Dmitriev OY (2002) Structural model of the transmembrane Fo rotary sector of H+-transporting ATP synthase derived by solution NMR and intersubunit cross-linking in situ. Biochim Biophys Acta 1565: 232–245

    PubMed  CAS  Google Scholar 

  • Fillingame RH, Jiang W and Dmitriev OY (2000a) Coupling H(+) transport to rotary catalysis in F-type ATP synthases: Structure and organization of the transmembrane rotary motor. J Exp Biol 203: 9–17

    PubMed  CAS  Google Scholar 

  • Fillingame RH, Jiang W, Dmitriev OY and Jones PC (2000b) Structural interpretations of FO rotary function in the Escherichia coli FOF1 ATP synthase. Biochim Biophys Acta 1458: 387–403

    PubMed  CAS  Google Scholar 

  • Fischer S and Graber P (1999) Comparison of ΔpH- and Δϕ-driven ATP synthesis catalyzed by the H+-ATPases from Escherichia coli or chloroplasts reconstituted into liposomes. FEBS Letters 457: 327–332

    PubMed  CAS  Google Scholar 

  • Fischer S, Graber P and Turina P (2000) The activity of the ATP synthase from Escherichia coli is regulated by the transmembrane proton motive force. J Biol Chem 275: 30157–30162

    PubMed  CAS  Google Scholar 

  • Galkin MA and Vinogradov AD (1999) Energy-dependent transformation of the catalytic activities of the mitochondrial FOF1-ATP synthase. FEBS Lett 448: 123–126

    PubMed  CAS  Google Scholar 

  • Gao YQ, Yang W and Karplus M (2005) A structure-based model for the synthesis and hydrolysis of ATP by F1-ATPase. Cell 123: 195–205

    PubMed  CAS  Google Scholar 

  • Gibbons C, Montgomery MG, Leslie AG, and Walker JE (2000) The structure of the central stalk in bovine F1-ATPase at 2.4 Å resolution. Nat Struct Biol 7: 1055–1061

    PubMed  CAS  Google Scholar 

  • Girvin ME and Fillingame RH (1994) Hairpin folding of subunit c of F1Fo ATP synthase: 1H distance measurements to nitroxide-derivatized aspartyl-61. Biochemistry 33: 665–674

    PubMed  CAS  Google Scholar 

  • Graber P, Schlodder E and Witt HT (1977) Conformational change of the chloroplast ATPase induced by a transmembrane electric field and its correlation to phosphorylation. Biochim Biophys Acta 461: 426–440

    PubMed  CAS  Google Scholar 

  • Groth G and Junge W (1993) Proton slip of chloroplast ATPase: Its nucleotide dependence, energetic threshold and relation to an alternating site mechanism of catalysis. Biochemistry 32: 8103–8111

    PubMed  CAS  Google Scholar 

  • Gumbiowski K, Panke O, Junge W and Engelbrecht S (2002) Rotation of the c subunit oligomer in EF0EF1 mutant cD61N. J Biol Chem 277: 31287–31290

    PubMed  CAS  Google Scholar 

  • Hangarter RP, Grandoni P and Ort DR (1987) The effects of chloroplast coupling factor reduction on the energetics of activation and on the energetics and efficiency of ATP formation. J Biol Chem 262: 13513–13519

    PubMed  CAS  Google Scholar 

  • Häsler K, Engelbrecht S and Junge W (1998) Three-stepped rotation of subunits gamma and epsilon in single molecules of F-ATPase as revealed by polarized, confocal fluorometry. FEBS Lett 426: 301–304

    PubMed  Google Scholar 

  • Häsler K, Pänke O and Junge W (1999) On the stator of rotary ATP synthase: the binding strength of subunit δ to (αβ)3 as determined by fluorescence correlation spectroscopy. Biochemistry 38: 13759–13765

    PubMed  Google Scholar 

  • Hatch LP, Cox GB and Howitt SM (1995) The essential arginine residue at position 210 in the a subunit of the Escherichia coli ATP synthase can be transferred to position 252 with partial retention of activity. J Biol Chem 270: 29407–29412

    PubMed  CAS  Google Scholar 

  • Hatch LP, Cox GB and Howitt SM (1998) Glutamate residues at positions 219 and 252 in the a-subunit of the Escherichia coli ATP synthase are not functionally equivalent. Biochim Biophys Acta 1363: 217–223

    PubMed  CAS  Google Scholar 

  • Hirono-Hara Y, Ishuzuka K, Kinosita K, Yoshida M and Noji H (2005) Activation of pausing F-1 motor by external force. Proc Natl Acad Sci USA 102: 4288–4293

    PubMed  CAS  Google Scholar 

  • Hisabori T, Kondoh A and Yoshida M (1999) The gamma subunit in chloroplast F1-ATPase can rotate in a unidirectional and counter-clockwise manner. FEBS Lett 463: 35–38

    PubMed  CAS  Google Scholar 

  • Hoppe J and Sebald W (1984) The proton conducting F0-part of bacterial ATP synthases. Biochim Biophys Acta 768: 1–27

    PubMed  CAS  Google Scholar 

  • Howitt SM and Cox GB (1992) Second-site revertants of an arginine-210 to lysine mutation in the a subunit of the FOF1-ATPase from Escherichia coli: Implications for structure. Proc Natl Acad Sci USA 89: 9799–9803

    PubMed  CAS  Google Scholar 

  • Hutcheon ML, Duncan TM, Ngai H and Cross RL (2001) Energy-driven subunit rotation at the interface between subunit a and the c oligomer in the F0 sector of Escherichia coli ATP synthase. Proc Natl Acad Sci USA 98: 8519–8524

    PubMed  CAS  Google Scholar 

  • Hyndman DJ, Milgrom YM, Bramhall EA and Cross RL (1994) Nucleotide-binding sites on Escherichia coli F1-ATPase. Specificity of noncatalytic sites and inhibition at catalytic sites by MgADP. J Biol Chem 269: 28871–28877

    PubMed  CAS  Google Scholar 

  • Itoh H, Takahashi A, Adachi K, Noji H, Yasuda R, Yoshida M and Kinosita K, Jr. (2004) Mechanically driven ATP synthesis by F1-ATPase. Nature 427: 465–468

    PubMed  CAS  Google Scholar 

  • Jackson JB (1988) Bacterial photosynthesis. In: Anthony C (ed) Bacterial Energy Transduction, pp 317–376. Academic Press, London

    Google Scholar 

  • Jackson JB and Crofts AR (1971) The kinetics of light induced carotenoid changes in Rhodopseudomonas sphaeroides and their relation to electrical field generation across the chromatophore membrane. Eur J Biochem 18: 120–130

    PubMed  CAS  Google Scholar 

  • Jans DA, Fimmel AL, Hatch L, Gibson F and Cox GB (1984) An additional acidic residue in the membrane portion of the b-subunit of the energy-transducing adenosine triphosphatase of Escherichia coli affects both assembly and function. Biochem J 221: 43–51

    PubMed  CAS  Google Scholar 

  • Jault JM and Allison WS (1993) Slow binding of ATP to non-catalytic nucleotide binding sites which accelerates catalysis is responsible for apparent negative cooperativity exhibited by the bovine mitochondrial F1-ATPase. J Biol Chem 268: 1558–1566

    PubMed  CAS  Google Scholar 

  • Jault JM, Matsui T, Jault FM, Kaibara C, Muneyuki E, Yoshida M, Kagawa Y and Allison WS (1995) The α3β3γ complex of the F1-ATPase from thermophilic Bacillus PS3 containing the αD261N substitution fails to dissociate inhibitory MgADP from a catalytic site when ATP binds to noncatalytic sites. Biochemistry 34: 16412–16418

    PubMed  CAS  Google Scholar 

  • Jiang W, Hermolin J and Fillingame RH (2001) The preferred stoichiometry of c subunits in the rotary motor sector of Escherichia coli ATP synthase is 10. Proc Natl Acad Sci USA 98: 4966–4971

    PubMed  CAS  Google Scholar 

  • Jones PC, Hermolin J, Jiang W, and Fillingame RH (2000) Insights into the rotary catalytic mechanism of FOF1 ATP synthase from the cross-linking of subunits b and c in the Escherichia coli enzyme. J Biol Chem 275: 31340–31346

    PubMed  CAS  Google Scholar 

  • Junge W (1970) Critical electric potential difference for photophosphorylation. Its relation to the chemiosomotic hypothesis and to the triggering requirements of the ATPase system. Eur J Biochem 14: 582–592

    PubMed  CAS  Google Scholar 

  • Junge W (1987) Complete tracking of transient proton flow through active chloroplast ATP synthase. Proc Natl Acad Sci USA 84: 7084–7088

    PubMed  CAS  Google Scholar 

  • Junge W (2004) Protons, proteins and ATP. Photosynth Res 80: 197–221

    PubMed  CAS  Google Scholar 

  • Junge W and Nelson N (2005) Structural biology. Nature’s rotary electromotors. Science 308: 642–644

    PubMed  CAS  Google Scholar 

  • Junge W and Witt HT (1968) On the ion transport system of photosynthesis-investigations on a molecular level. Z Naturforsch 23: 244–254

    CAS  Google Scholar 

  • Junge W, Rumberg B and Schroder H (1970) The necessity of an electric potential difference and its use for photophosphorylation in short flash groups. Eur J Biochem 14: 575–581

    PubMed  CAS  Google Scholar 

  • Junge W, Lill H and Engelbrecht S (1997) ATP synthase: An electrochemical transducer with rotatory mechanics. Trends Biochem Sci 22: 420–423

    PubMed  CAS  Google Scholar 

  • Kaim G and Dimroth P (1998a) ATP synthesis by the F1F0 ATP synthase of Escherichia coli is obligatorily dependent on the electric potential. FEBS Lett 434: 57–60

    PubMed  CAS  Google Scholar 

  • Kaim G and Dimroth P (1998b) Voltage-generated torque drives the motor of the ATP synthase. EMBO J 17: 5887–5895

    PubMed  CAS  Google Scholar 

  • Kaim G and Dimroth P (1999) ATP synthesis by F-type ATP synthase is obligatorily dependent on the transmembrane voltage. EMBO J 18: 4118–4127

    PubMed  CAS  Google Scholar 

  • Kaim G, Prummer M, Sick B, Zumofen G, Renn A, Wild UP, and Dimroth P (2002) Coupled rotation within single F0Fj enzyme complexes during ATP synthesis or hydrolysis. FEBS Lett 525: 156–163

    PubMed  CAS  Google Scholar 

  • Kato-Yamada Y, Noji H, Yasuda R, Kinosita K, Jr. and Yoshida M (1998) Direct observation of the rotation of epsilon subunit in FrATPase. J Biol Chem 273: 19375–19377

    PubMed  CAS  Google Scholar 

  • Kayalar C, Rosing J and Boyer PD (1977) An alternating site sequence for oxidative phosphorylation suggested by measurement of substrate binding patterns and exchange reaction inhibitions. J Biol Chem 252: 2486–2491

    PubMed  CAS  Google Scholar 

  • Kinosita K, Jr., Adachi K and Itoh H (2004) Rotation of FrATPase: How an ATP-driven molecular machine may work. Annu Rev Biophys Biomol Struct 33: 245–268

    PubMed  CAS  Google Scholar 

  • Kumamoto CA and Simoni RD (1986) Genetic evidence for interaction between the a. and b subunits of the Fo portion of the Escherichia coli proton translocating ATPase. J Biol Chem 261: 10037–10042

    PubMed  CAS  Google Scholar 

  • Larreta-Garde V and Thomas D (1985) Influence of light on long-term ADP phosphorylation. J Biol Chem 260: 6060–6062

    PubMed  CAS  Google Scholar 

  • Lightowlers RN, Howitt SM, Hatch L, Gibson F and Cox GB (1987) The proton pore in the Escherichia coli FOF1-ATPase: A requirement for arginine at position 210 of the a-subunit. Biochim Biophys Acta 894: 399–406

    PubMed  CAS  Google Scholar 

  • Lightowlers RN, Howitt SM, Hatch L, Gibson F and Cox G (1988) The proton pore in the Escherichia coli FOF1-ATPase: Substitution of glutamate by glutamine at position 219 of the alpha-subunit prevents FO-mediated proton permeability. Biochim Biophys Acta 933: 241–248

    PubMed  CAS  Google Scholar 

  • Long JC, Wang S and Vik SB (1998) Membrane topology of subunit a of the FOF1 ATP synthase as determined by labeling of unique cysteine residues. J Biol Chem 273: 16235–16240

    PubMed  CAS  Google Scholar 

  • Long JC, DeLeon-Rangel J and Vik SB (2002) Characterization of the first cytoplasmic loop of subunit a of the Escherichia coli ATP synthase by surface labeling, cross-linking, and mutagenesis. J Biol Chem 277: 27288–27293

    PubMed  CAS  Google Scholar 

  • Matsui T, Muneyuki E, Honda M, Allison WS, Dou C and Yoshida M (1997) Catalytic activity of the alpha3beta3gamma complex of F1-ATPase without noncatalytic nucleotide binding site. J Biol Chem 272: 8215–8221

    PubMed  CAS  Google Scholar 

  • Matthey U, Kaim G, Braun D, Wuthrich K and Dimroth P (1999) NMR studies of subunit c of the ATP synthase from Propionigenium modestum in dodecylsulphate micelles. Eur J Biochem 261: 459–467

    PubMed  CAS  Google Scholar 

  • Meier T, Matthey U, Henzen F, Dimroth P and Müller DJ (2002) The central plug in the reconstituted undecameric c cylinder of a bacterial ATP synthase consists of phospholipids. FEBS Lett 505: 353–356

    Google Scholar 

  • Meier T, Matthey U, von Ballmoos C, Vonck J, Krug VN, Kühlbrandt W and Dimroth P (2003) Evidence for structural integrity in the undecameric c-rings isolated from sodium ATP synthases. J Mol Biol 325: 389–397

    PubMed  CAS  Google Scholar 

  • Meier T, Polzer P, Diederichs K, Weite W and Dimroth P (2005a) Structure of the rotor ring of F-Type Na+-ATPase from Ilyobacter tartaricus. Science 308: 659–662

    PubMed  CAS  Google Scholar 

  • Meier T, Yu J, Raschle T, Henzen F, Dimroth P and Müller DJ (2005b) Structural evidence for a constant c11 ring stoichiometry in the sodium F-ATP synthase. FEBS J 272: 5474–5483

    PubMed  CAS  Google Scholar 

  • Melandri AB, Fabbri E, and Melandri BA (1975) Energy transduction in photosynthetic bacteria. VIII. Activation of the energy-transducing ATPase by inorganic phosphate. Biochim Biophys Acta 376: 82–88

    PubMed  CAS  Google Scholar 

  • Melandri BA, Baccarini-Melandri A, San Pietro A and Gest H (1971) Interchangeability of phosphorylation coupling factors in photosynthetic and respiratory energy conversion. Science 174: 514–516

    PubMed  CAS  Google Scholar 

  • Milgrom YM and Boyer PD (1990) The ADP that binds tightly to nucleotide-depleted mitochondrial F1-ATPase and inhibits catalysis is bound at a catalytic site. Biochim Biophys Acta 1020: 43–48

    PubMed  CAS  Google Scholar 

  • Milgrom YM, Ehler LL and Boyer PD (1990) ATP binding at noncatalytic sites of soluble chloroplast F1-ATPase is required for expression of the enzyme activity. J Biol Chem 265: 18725–18728

    PubMed  CAS  Google Scholar 

  • Milgrom YM, Ehler LL and Boyer PD (1991) The characteristics and effect on catalysis of nucleotide binding to noncatalytic sites of chloroplast F1-ATPase. J Biol Chem 266: 11551–11558

    PubMed  CAS  Google Scholar 

  • Miller MJ, Oldenburg M and Fillingame RH (1990) The essential carboxyl group in subunit c of the F1F0 ATP synthase can be moved and H+-translocating function retained. Proc Natl Acad Sci USA 87: 4900–4904

    PubMed  CAS  Google Scholar 

  • Mitome N, Ono S, Suzuki T, Shimabukuro K, Muneyuki E and Yoshida M (2002) The presence of phosphate at a catalytic site suppresses the formation of the MgADP-inhibited form of F1-ATPase. Eur J Biochem 269: 53–60

    PubMed  CAS  Google Scholar 

  • Mitome N, Suzuki T, Hayashi S and Yoshida M (2004) Thermophilic ATP synthase has a decamer c-ring: indication of noninteger 10:3 H+/ATP ratio and permissive elastic coupling. Proc Natl Acad Sci USA 101: 12159–12164

    PubMed  CAS  Google Scholar 

  • Moyle J and Mitchell P (1975) Active/inactive state transitions of mitochondrial ATPase molecules influenced by Mg2+, anions and aurovertin. FEBS Lett 56: 55–61

    PubMed  CAS  Google Scholar 

  • Noji H, Yasuda R, Yoshida M and Kinosita K, Jr. (1997) Directobservation of the rotation of F1-ATPase. Nature 386: 299–302

    PubMed  CAS  Google Scholar 

  • Noji H, Häsler K, Junge W, Kinosita K, Jr., Yoshida M and Engelbrecht S (1999) Rotation of Escherichia coli F1-ATPase. Biochem Biophys Res Commun 260: 597–599

    PubMed  CAS  Google Scholar 

  • Oberfeld B, Brunner J and Dimroth P (2006) Phospholipids occupy the internal lumen of the c ring of the ATP synthase of Escherichia coli. Biochemistry 45: 1841–1851

    PubMed  CAS  Google Scholar 

  • Omote H, Sambonmatsu N, Saito K, Sambongi Y, Iwamoto-Kihara A, Yanagida T, Wada Y and Futai M (1999) The γ-subunit rotation and torque generation in F1-ATPase from wild-type or uncoupled mutant Escherichia coli. Proc Natl Acad Sci USA 96: 7780–7784

    PubMed  CAS  Google Scholar 

  • Packham NK, Berriman JA and Jackson JB (1978) The charging capacitance of the chromatophore membrane. FEBS Lett 89: 205–210

    PubMed  CAS  Google Scholar 

  • Pänke O and Rumberg B (1999) Kinetic modeling of rotary CF0F1-ATP synthase: storage of elastic energy during energy transduction. Biochim Biophys Acta 1412: 118–128

    PubMed  Google Scholar 

  • Pänke O, Gumbiowski K, Junge W and Engelbrecht S (2000) F-ATPase: Specific observation of the rotating c subunit oligomer of EF0EF1. FEBS Lett 472: 34–38

    PubMed  Google Scholar 

  • Pänke O, Cherepanov DA, Gumbiowski K, Engelbrecht S and Junge W (2001) Viscoelastic dynamics of actin filaments coupled to rotary F-ATPase: Angular torque profile of the enzyme. Biophys J 81: 1220–1233

    Article  PubMed  Google Scholar 

  • Pati S, Brusilow WS, Deckers-Hebestreit G and Altendorf K (1991) Assembly of the F0 proton channel of the Escherichia coli F1F0 ATPase: Low proton conductance of reconstituted F0 sectors synthesized and assembled in the absence of F1. Biochemistry 30: 4710–4714

    PubMed  CAS  Google Scholar 

  • Patterson AR, Wada T and Vik SB (1999) His(15) of subunit a of the Escherichia coli ATP synthase is important for the structure or assembly of the membrane sector FO. Arch Biochem Biophys 368: 193–197

    PubMed  CAS  Google Scholar 

  • Pick U and Weiss M (1988) A light-dependent dicyclohexylcarbodiimide-sensitive Ca-ATPase activity in chloroplasts which is not coupled to proton translocation. Eur J Biochem 173: 623–628

    PubMed  CAS  Google Scholar 

  • Pogoryelov D, Yu J, Meier T, Vonck J, Dimroth P and Muller DJ (2005) The c 15 ring of the Spirulina platensis F-ATP synthase: F1/F0 symmetry mismatch is not obligatory. EMBO Rep 6: 1040–1044

    PubMed  CAS  Google Scholar 

  • Ponomarenko S, Volfson I and Strotmann H (1999) Proton gradient-induced changes of the interaction between CFO and CF1 related to activation of the chloroplast ATP synthase. FEBS Lett 443: 136–138

    PubMed  CAS  Google Scholar 

  • Porter AC, Kumamoto C, Aldape K and Simoni RD (1985) Role of the b subunit of the Escherichia coli proton-translocating ATPase. A mutagenic analysis. J Biol Chem 260: 8182–8187

    PubMed  CAS  Google Scholar 

  • Rastogi VK and Girvin ME (1999) Structural changes linked to proton translocation by subunit c of the ATP synthase. Nature 402: 263–268

    PubMed  CAS  Google Scholar 

  • Rondelez Y, Tresset G, Nakashima T, Kato-Yamada Y, Fujita H, Takeuchi S and Noji H (2005) Highly coupled ATP synthesis by F1-ATPase single molecules. Nature 433: 773–777

    PubMed  CAS  Google Scholar 

  • Sabbert D, Engelbrecht S and Junge W (1996) Intersubunit rotation in active F-ATPase. Nature 381: 623–625

    PubMed  CAS  Google Scholar 

  • Sabbert D, Engelbrecht S and Junge W (1997) Functional and idling rotatory motion within F1-ATPase. Proc Natl Acad Sci USA 94: 4401–4405

    PubMed  CAS  Google Scholar 

  • Sambongi Y, Iko Y, Tanabe M, Omote H, Iwamoto-Kihara A, Ueda I, Yanagida T, Wada Y and Futai M (1999) Mechanical rotation of the c subunit oligomer in ATP synthase (F0F1): direct observation. Science 286: 1722–1724

    PubMed  CAS  Google Scholar 

  • Saphon S, Jackson JB, Lerbs V and Witt HT (1975a) The functional unit of electrical events and phosphorylation in chromatophores from Rhodopseudomonas sphaeroides. Biochim Biophys Acta 408: 58–66

    PubMed  CAS  Google Scholar 

  • Saphon S, Jackson JB and Witt HT (1975b) Electrical potential changes, H+ translocation and phosphorylation induced by short flash excitation in Rhodopseudomonas sphaeroides chromatophores. Biochim Biophys Acta 408: 67–82

    PubMed  CAS  Google Scholar 

  • Schneider E and Altendorf K (1985) All three subunits are required for the reconstitution of an active proton channel (F0) of Escherichia coli ATP synthase (F1F0). EMBO J 4: 515–518

    PubMed  CAS  Google Scholar 

  • Schönknecht G, Junge W, Lill H and Engelbrecht S (1986) Complete tracking of proton flow in thylakoids-the unit conductance of CF0 is greater than 10 fS. FEBS Lett 203: 289–294

    Google Scholar 

  • Schulenberg B, Wellmer F, Lill H, Junge W and Engelbrecht S (1997) Cross-linking of chloroplast F0F1-ATPase subunit e to γ without effect on activity. ε and γ are parts of the rotor. Eur J Biochem 249: 134–141

    PubMed  CAS  Google Scholar 

  • Seelert H, Poetsch A, Dencher NA, Engel A, Stahlberg H and Muller DJ (2000) Structural biology. Proton-powered turbine of a plant motor. Nature 405: 418–419

    PubMed  CAS  Google Scholar 

  • Senior AE, Nadanaciva S and Weber J (2002) The molecular mechanism of ATP synthesis by F1F0-ATP synthase. Biochim Biophys Acta 1553: 188–211

    PubMed  CAS  Google Scholar 

  • Shirakihara Y, Leslie AG, Abrahams JP, Walker JE, Ueda T, Sekimoto Y, Kambara M, Saika K, Kagawa Y and Yoshida M (1997) The crystal structure of the nucleotide-free α3β3 subcomplex of F1-ATPase from the thermophilic Bacillus PS3 is a symmetric trimer. Structure 5: 825–836

    PubMed  CAS  Google Scholar 

  • Singh S, Turina P, Bustamante CJ, Keller DJ and Capaldi RA (1996) Topographical structure of membrane-bound Escherichia coli F1F0 ATP synthase in aqueous buffer. FEBS Lett 397: 30–34

    PubMed  CAS  Google Scholar 

  • Smith LT, Rosen G and Boyer PD (1983) Properties of ATP tightly bound to catalytic sites of chloroplast ATP synthase. J Biol Chem 258: 10887–10894

    PubMed  CAS  Google Scholar 

  • Sone N, Yoshida M, Hirata H and Kagawa Y (1979) Carbodiimide-binding protein of H+-translocating ATPase and inhibition of H+ conduction by dicyclohexylcarbodiimide. J Biochem (Tokyo) 85: 503–509

    CAS  Google Scholar 

  • Sorgen PL, Caviston TL, Perry RC and Cain BD (1998) Deletions in the second stalk of F1F0-ATP synthase in Escherichia coli. J Biol Chem 273: 27873–27878

    PubMed  CAS  Google Scholar 

  • Sorgen PL, Bubb MR and Cain BD (1999) Lengthening the second stalk of F1F0 ATP synthase in Escherichia coli. J Biol Chem 274: 36261–36266

    PubMed  CAS  Google Scholar 

  • Stahlberg H, Muller DJ, Suda K, Fotiadis D, Engel A, Meier T, Matthey U and Dimroth P (2001) Bacterial Na(+)-ATP synthase has an undecameric rotor. EMBO Rep 2: 229–233

    PubMed  CAS  Google Scholar 

  • Stalz WD, Greie JC, Deckers-Hebestreit G and Altendorf K (2003) Direct interaction of subunits a and b of the F0 complex of Escherichia coli ATP synthase by forming an ab 2 subcomplex. J Biol Chem 278: 27068–27071

    PubMed  CAS  Google Scholar 

  • Steffens K, Hoppe J and Altendorf K (1988) F0 part of the ATP synthase fromEscherichia coli. Influence of subunits a, and b, on the structure of subunit c. Eur J Biochem 170: 627–630

    PubMed  CAS  Google Scholar 

  • Stock D, Leslie AG and Walker JE (1999) Molecular architecture of the rotary motor in ATP synthase. Science 286: 1700–1705

    PubMed  CAS  Google Scholar 

  • Suzuki T, Ueno H, Mitome N, Suzuki J and Yoshida M (2002) F0 of ATP synthase is a rotary proton channel: Obligatory coupling of proton translocation with rotation of c-subunit ring. J Biol Chem 277: 13281–13285

    PubMed  CAS  Google Scholar 

  • Suzuki T, Murakami T, Iino R, Suzuki J, Ono S, Shirakihara Y and Yoshida M (2003) F0F1-ATPase/synthase is geared to the synthesis mode by conformational rearrangement of epsilon subunit in response to proton motive force and ADP/ATP balance. J Biol Chem 278: 46840–46846

    PubMed  CAS  Google Scholar 

  • Takeyasu K, Omote H, Nettikadan S, Tokumasu F, Iwamoto-Kihara A and Futai M (1996) Molecular imaging of Escherichia coli F0F1-ATPase in reconstituted membranes using atomic force microscopy. FEBS Lett 392: 110–113

    PubMed  CAS  Google Scholar 

  • Tanabe M, Nishio K, Iko Y, Sambongi Y, Iwamoto-Kihara A, Wada Y and Futai M (2001) Rotation of a complex of the γ subunit and c ring of Escherichia coli ATP synthase. The rotor and stator are interchangeable. J Biol Chem 276: 15269–15274

    PubMed  CAS  Google Scholar 

  • Tsunoda SP, Aggeler R, Yoshida M and Capaldi RA (2001a) Rotation of the c subunit oligomer in fully functional F1F0 ATP synthase. Proc Natl Acad Sci USA 98: 898–902

    PubMed  CAS  Google Scholar 

  • Tsunoda SP, Rodgers AJ, Aggeler R, Wilce MC, Yoshida M and Capaldi RA (2001b) Large conformational changes of the ε subunit in the bacterial F1F0 ATP synthase provide a ratchet action to regulate this rotary motor enzyme. Proc Natl Acad Sci USA 98: 6560–6564

    PubMed  CAS  Google Scholar 

  • Turina P, Giovannini D, Gubellini F and Melandri BA (2004) Physiological ligands ADP and Pi modulate the degree of intrinsic coupling in the ATP synthase of the photosynthetic bacterium Rhodobacter capsulatus. Biochemistry 43: 11126–11134

    PubMed  CAS  Google Scholar 

  • Turina P and Melandri BA (2002) A point mutation in the ATP synthase of Rhodobacter capsulatus results in differential contributions of ΔpH and Δϕ in driving the ATP synthesis reaction. Eur J Biochem 269: 1984–1992

    PubMed  CAS  Google Scholar 

  • Turina P, Rumberg B, Melandri BA and Graber P (1992) Activation of the H+-ATP synthase in the photosynthetic bacterium Rhodobacter capsulatus. J Biol Chem 267: 11057–11063

    PubMed  CAS  Google Scholar 

  • Turina P, Samoray D, and Graber P (2003) H+/ATP ratio of proton transport-coupled ATP synthesis and hydrolysis catalysed by CF0F1-liposomes. EMBO J 22: 418–426

    PubMed  CAS  Google Scholar 

  • Turina P, Venturoli G, and Melandri BA (1990) Evaluation of the buffer capacity and permeability constant for protons in chromatophores from Rhodobacter capsulatus. Eur J Biochem 192: 39–47

    PubMed  CAS  Google Scholar 

  • Ueno H, Suzuki T, Kinosita K, Jr. and Yoshida M (2005) ATP-driven stepwise rotation of F0F1-ATP synthase. Proc Natl Acad Sci USA 102: 1333–1338

    PubMed  CAS  Google Scholar 

  • Valiyaveetil FI and Filiingame RH (1997) On the role of Arg-210 and Glu-219 of subunit a in proton translocation by the Escherichia coli F0F1-ATP synthase. J Biol Chem 272: 32635–32641

    PubMed  CAS  Google Scholar 

  • Valiyaveetil FI and Fillingame RH (1998) Transmembrane topography of subunit a in the Escherichia coli F1F0 ATP synthase. J Biol Chem 273: 16241–16247

    PubMed  CAS  Google Scholar 

  • van Walraven HS, Strotmann H, Schwarz O, and Rumberg B (1996) The H+/ATP coupling ratio of the ATP synthase from thiol-modulated chloroplasts and two cyanobacterial strains is four. FEBS Lett 379: 309–313

    PubMed  Google Scholar 

  • Velours J, Paumard P, Soubannier V, Spannagel C, Vaillier J, Arselin G and Graves PV (2000) Organisation of the yeast ATP synthase F0: A study based on cysteine mutants, thiol modification and cross-linking reagents. Biochim Biophys Acta 1458: 443–456

    PubMed  CAS  Google Scholar 

  • Vik SB and Antonio BJ(1994)A mechanism of proton translocation by F1F0 ATP synthases suggested by double mutants of the a subunit. J Biol Chem 269: 30364–30369

    PubMed  CAS  Google Scholar 

  • Vik SB, Cain BD, Chun KT and Simoni RD (1988) Mutagenesis of the a subunit of the F1F0-ATPase from Escherichia coli. Mutations at Glu-196, Pro-190, and Ser-199. J Biol Chem 263: 6599–6605

    PubMed  CAS  Google Scholar 

  • Vik SB, Long JC, Wada T, and Zhang D (2000) A model for the structure of subunit a of the Escherichia coli ATP synthase and its role in proton translocation. Biochim Biophys Acta 1458: 457–466

    PubMed  CAS  Google Scholar 

  • Wada T, Long JC, Zhang D and Vik SB (1999) A novel labeling approach supports the five-transmembrane model of subunit a of the Escherichia coli ATP synthase. J Biol Chem 274: 17353–17357

    PubMed  CAS  Google Scholar 

  • Wang Z, Hicks DB, Guffanti AA, Baldwin K and Krulwich TA (2004) Replacement of amino acid sequence features of a- and c-subunits of ATP synthases of alkaliphilic Bacillus with the Bacillus consensus sequence results in defective oxidative phosphorylation and non-fermentative growth at pH 10.5. J Biol Chem 279: 26546–26554

    PubMed  CAS  Google Scholar 

  • Watts SD and Capaldi RA (1997) Interactions between the F1 and F0 parts in the Escherichia coli ATP synthase. Associations involving the loop region of c subunits. J Biol Chem 272: 15065–15068

    PubMed  CAS  Google Scholar 

  • Watts SD, Tang C and Capaldi RA (1996) The stalk region of the Escherichia coli ATP synthase. Tyrosine 205 of the subunit is in the interface between the F1 and F0 parts and can interact with both the ε and c oligomer. J Biol Chem 271: 28341–28347

    PubMed  CAS  Google Scholar 

  • Weber H, Junge W, Hoppe J and Sebald W (1986) Laser-activated carbene labels the same residues in the proteolipid subunit of the ATP synthase in energized and nonenergized chloroplasts and mitochondria. FEBS Lett 202: 23–26

    CAS  Google Scholar 

  • Weber J (2006) ATP synthase : Subunit-subunit interactions in the stator stalk. Biochim Biophys Acta 1757: 1162–1170

    PubMed  CAS  Google Scholar 

  • Weber J, Bowman C, Wilke-Mounts S and Senior AE (1995) α-Aspartate 261 is a key residue in noncatalytic sites of Escherichia coli F1-ATPase. J Biol Chem 270: 21045–21049

    PubMed  CAS  Google Scholar 

  • Weber J and Senior AE (2003) ATP synthesis driven by proton transport in F1F0-ATP synthase. FEBS Lett 545: 61–70

    PubMed  CAS  Google Scholar 

  • Weber J, Wilke-Mounts S, Grell E and Senior AE (1994) Tryptophan fluorescence provides a direct probe of nucleotide binding in the noncatalytic sites of Escherichia coli F1-ATPase. J Biol Chem 269: 11261–11268

    PubMed  CAS  Google Scholar 

  • Weber J, Wilke-Mounts S and Senior AE (2002) Quantitative determination of binding affinity of δ-subunit in Escherichia coli F1-ATPase: effects of mutation, Mg2+, and pH on K d . J Biol Chem 277: 18390–18396

    PubMed  CAS  Google Scholar 

  • Weber J, Wilke-Mounts S, Nadanaciva S and Senior AE (2004) Quantitative determination of direct binding of b subunit to F1 in Escherichia coli F1F0-ATP synthase. J Biol Chem 279: 11253–11258.

    PubMed  CAS  Google Scholar 

  • Yasuda R, Noji H, Kinosita K and Yoshida M (1998) F1-ATPase is a highly efficient molecular motor that rotates with discrete 120° steps. Cell 93: 1117–1124

    PubMed  CAS  Google Scholar 

  • Yoshida M, Muneyuki E and Hisabori T (2001) ATP synthase — a marvellous rotary engine of the cell. Nat Rev Mol Cell Biol 2: 669–677

    PubMed  CAS  Google Scholar 

  • Zhang D and Vik SB (2003) Helix packing in subunit a of the Escherichia coli ATP synthase as determined by chemical labeling and proteolysis of the cysteine-substituted protein. Biochemistry 42: 331–337

    PubMed  CAS  Google Scholar 

  • Zhang Y and Filiingame RH (1995) Subunits coupling H+ transport and ATP synthesis in the Escherichia coli ATP synthase. Cys-Cys cross-linking of F1 subunit epsilon to the polar loop of F1 subunit c. J Biol Chem 270: 24609–24614

    PubMed  CAS  Google Scholar 

  • Zharova TV and Vinogradov AD (2004) Energy-dependent transformation of F0F1-ATPase in Paracoccus denitrificans plasma membranes. J Biol Chem 279: 12319–12324

    PubMed  CAS  Google Scholar 

  • Zharova TV and Vinogradov AD (2006) Energy-linked binding of Pi is required for continuous steady-state proton-translocating ATP hydrolysis catalyzed by FOF1 ATP synthase. Biochemistry 45: 14552–14558

    PubMed  CAS  Google Scholar 

  • Zimmermann B, Diez M, Zarrabi N, Graber P and Borsch M (2005) Movements of the e-subunit during catalysis and activation in single membrane-bound H+-ATP synthase. EMBO J 24: 2053–2063

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Chemical Resources Laboratory, Tokyo Institute of Technology, Nagatsuta 4259, Midori-ku, Yokohama, 226-8503, Japan

    Boris A. Feniouk

  2. Department of Biophysics, University of Osnabrück, DE-49069, Osnabrück, Germany

    Wolfgang Junge

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  1. Boris A. Feniouk
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Correspondence to Wolfgang Junge .

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  1. University of Sheffield, UK

    C. Neil Hunter

  2. University of Pennsylvania, USA

    Fevzi Daldal

  3. Argonne National Laboratory, USA

    Marion C. Thurnauer

  4. University of British Columbia, Canada

    J. Thomas Beatty

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Feniouk, B.A., Junge, W. (2009). Proton Translocation and ATP Synthesis by the FoF1-ATPase of Purple Bacteria. In: Hunter, C.N., Daldal, F., Thurnauer, M.C., Beatty, J.T. (eds) The Purple Phototrophic Bacteria. Advances in Photosynthesis and Respiration, vol 28. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-8815-5_24

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