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Energy transduction in ATP synthase

Nature volume 391, pages 510–513 (1998)Cite this article

Abstract

Mitochondria, bacteria and chloroplasts use the free energy stored in transmembrane ion gradients to manufacture ATP by the action of ATP synthase. This enzyme consists of two principal domains. The asymmetric membrane-spanning Fo portion contains the proton channel, and the soluble F1 portion contains three catalytic sites which cooperate in the synthetic reactions1. The flow of protons through Fo is thought to generate a torque which is transmitted to F1 by an asymmetric shaft, the coiled-coil γ-subunit. This acts as a rotating ‘cam’ within F1, sequentially releasing ATPs from the three active sites1,2,3,4,5. The free-energy difference across the inner membrane of mitochondria and bacteria is sufficient to produce three ATPs per twelve protons passing through the motor. It has been suggested that this protonmotive force biases the rotor's diffusion so that Fo constitutes a rotary motor turning the γ shaft6. Here we show that biased diffusion, augmented by electrostatic forces, does indeed generate sufficient torque to account for ATP production. Moreover, the motor's reversibility — supplying torque from ATP hydrolysis in F1 converts the motor into an efficient proton pump7 — can also be explained by our model.

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Figure 1: Structure of FoF1 ATP synthase5,6.
Figure 2: Charge geometry and movement of protons in ATP synthase.
Figure 3: Properties of the ATP synthase rotor.
Figure 4: Solid lines show the rotation rate of the motor as a function of the p K a of the rotor Asp 61 sites with and without the presence of the stator Arg 210 charge when the load torque is fixed at 41 pN nm.

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References

  1. Boyer, P. The binding change mechanism for ATP synthase — some probabilities and possibilities. Biochim. Biophys. Acta 1140, 215–250 (1993).

    Article  ADS  CAS  PubMed  Google Scholar 

  2. Abrahams, J., Leslie, A., Lutter, R. & Walker, J. Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria. Nature 370, 621–628 (1994).

    Article  ADS  CAS  PubMed  Google Scholar 

  3. Fillingame, R. H. Coupling H+ transport and ATP synthesis in F1Fo-ATP synthases: glimpses of interacting parts in a dynamic molecular machine. J. Exp. Biol. 200, 217–224 (1997).

    CAS  PubMed  Google Scholar 

  4. Cross, R. & Duncan, T. Subunit rotation in FoF1-ATP synthases as a means of coupling proton transport through Foto the binding changes in F1. J. Bioenerg. Biomem. 28, 403–408 (1996).

    Article  CAS  Google Scholar 

  5. Engelbrecht, S. & Junge, W. ATP synthase: a tentative structural model. FEBS Lett. 414, 485–491 (1997).

    Article  CAS  PubMed  Google Scholar 

  6. Junge, W., Lill, H. & Engelbrecht, S. ATP synthase: An electro-chemical transducer with rotatory mechanics. Trends Biochem. Sci. 22, 420–423 (1997).

    Article  CAS  PubMed  Google Scholar 

  7. Yasuda, R., Noji, H., Kinosita, K., Motojima, F. & Yoshida, M. Rotation of the γ subunit in F1-ATPase; Evidence that ATP synthase is a rotary motor enzyme. J. Bioenerg. Biomem. 29, 207–209 (1997).

    Article  CAS  Google Scholar 

  8. Groth, G. & Walker, J. Model of the C-subunit oligomer in the membrane domain of F-ATPases. FEBS Lett. 410, 117–123 (1997).

    Article  CAS  PubMed  Google Scholar 

  9. Dmitriev, O. Y., Altendorf, K. & Fillingame, R. H. Reconstitution of the Focomplex of Escherichia coli ATP synthase from isolated subunits: Varying the number of essential carboxylates by co-incorporation of wild-type and mutant subunit c after purification in organic solvent. Eur. J. Biochem. 233, 478–483 (1995).

    Article  CAS  PubMed  Google Scholar 

  10. Valiyaveetil, F. & Fillingame, R. On the role of Arg 210 and Glu 219 of subunit a in proton translocation by the Escherichia coli FoF1ATP synthase. J. Biol. Chem. (in the press).

  11. Fillingame, R. H., Girvin, M. E. & Zhang, Y. Correlations of structure and function in subunit c of Escherichia coli FoF1ATP synthase. Biochem. Soc. Trans. 23, 760–766 (1995).

    Article  CAS  PubMed  Google Scholar 

  12. Howitt, S., Rodgers, A., Hatch, L., Gibson, F. & Cox, G. The coupling of the relative movement of the a and c subunits of the Foto the conformational changes in the F1-ATPase. J. Bioenerg. Biomem. 28, 415–420 (1996).

    Article  CAS  Google Scholar 

  13. Vik, S. B. & Antonio, B. J. Amechanism of proton translocation by F1FoATP synthases suggested by double mutants of the a subunit. J. Biol. Chem. 269, 30364–30369 (1994).

    CAS  PubMed  Google Scholar 

  14. Khan, S. & Berg, H. Isotope and thermal effects in chemiosmotic coupling to the flagellar motor of Streptococcus. Cell 32, 913–919 (1983).

    Article  CAS  PubMed  Google Scholar 

  15. Meister, M., Caplan, S. R. & Berg, H. C. Dynamics of a tightly coupled mechanism for flagellar rotation: Bacterial motility, chemiosmotic coupling, protonmotive force. Biophys. J. 55, 905–914 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Berg, H. & Khan, S. in Mobility and Recognition in Cell Biology (eds Sund, H. & Veeger, C.) 485–497 (de Gruyter, Berlin, 1983).

    Google Scholar 

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

    Article  ADS  CAS  PubMed  Google Scholar 

  18. Fillingame, R. in The Bacteria: A Treatise On Structure And Function (ed. Krulwich, T.) 345–392 (Academic, London, 1990).

    Google Scholar 

  19. Harrison, M., Finbow, M. & Findlay, J. Postulate for the molecular mechanism of the vacuolar H+-ATPase (hypothesis). J. Membr. Biol. 14, 1–3 (1997).

    Article  CAS  Google Scholar 

  20. Elston, T. & Oster, G. Protein turbines I: The bacterial flagellar motor. Biophys. J. 73, 703–721 (1997).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  21. Risken, H. The Fokker-Planck Equation (Springer, New York, 1989).

    Book  Google Scholar 

  22. Assadi-Porter, F. & Fillingame, R. Proton-translocating carboxyl of subunit c of F1FoH+-ATP synthase: The unique environment suggested by the pKa determined by 1H NMR. Biochem. 34, 16186–16193 (1995).

    Article  CAS  Google Scholar 

  23. Noji, H., Yasuda, R., Yoshida, M. & Kinosita, K. Direct observation of the rotation of F1-ATPase. Nature 386, 299–302 (1997).

    Article  ADS  CAS  PubMed  Google Scholar 

  24. Finbow, M. & Harrison, M. The vacuolar H+-ATPase: A universal proton pump of eukaryotes. Biochem. J. 324, 697–712 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Dimroth, P. Primary sodium ion translocating enzymes. Biochim. Biophys. Acta 1318, 11–51 (1997).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank C. Peskin, R. Fillingame, W. Junge, H.-P. Moore, J. Walker, R. Cross, and S.Khan for valuable comments. T.E. was suppported by postdoctoral support from Los Alamos National Laboratory, H.W. by a postdoctoral fellowship from National Energy Research Scientific Computing Center, and G.O. by a grant from the NSF.

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  1. Department of Molecular and Cellular Biology, University of California, Berkeley, 94720-3112, California, USA

    Timothy Elston, Hongyun Wang & George Oster

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Correspondence to George Oster.

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Elston, T., Wang, H. & Oster, G. Energy transduction in ATP synthase. Nature 391, 510–513 (1998). https://doi.org/10.1038/35185

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