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Nature of biological electron transfer

Abstract

Powerful first-order analysis of intraprotein electron transfer is developed from electron-transfer measurements both in biological and in chemical systems. A variation of 20 Å in the distance between donors and acceptors in protein changes the electron-transfer rate by 1012-fold. Protein presents a uniform electronic barrier to electron tunnelling and a uniform nuclear characteristic frequency, properties similar to an organic glass. Selection of distance, free energy and reorganization energy are sufficient to define rate and directional specificity of biological electron transfer, meeting physiological requirements in diverse systems.

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References

  1. Chance, B. & Nishimura, M. Proc. natn. Acad. Sci. U.S.A. 46, 19–24 (1960).

    Article  ADS  CAS  Google Scholar 

  2. Devault, D. & Chance, B. Biophys. J. 6, 825–847 (1966).

    Article  ADS  CAS  Google Scholar 

  3. Mitchell, P. Nature 191, 144–148 (1961).

    Article  ADS  CAS  Google Scholar 

  4. Devault, D. Q. Rev. Biophys. 13, 387–564 (1980).

    Article  CAS  Google Scholar 

  5. Marcus, R. A. J. chem. Phys. 24, 966–978 (1956).

    Article  ADS  CAS  Google Scholar 

  6. Marcus, R. A. & Sutin, N. Biochim. biophys. Acta 811, 265–322 (1985).

    Article  CAS  Google Scholar 

  7. Levich, V. G., & Dogonadze, R. R. Dokl. Akad. Nauk USSR 124, 123–126 (1959).

    CAS  Google Scholar 

  8. Jortner, J. J. chem. Phys. 64, 4860–4867 (1976).

    Article  ADS  CAS  Google Scholar 

  9. Hopfield, J. J. Proc. natn. Acad. Sci. U.S.A. 71, 3640–3644 (1974).

    Article  ADS  CAS  Google Scholar 

  10. Michel, H., Deisenhofer, J. & Epp, O. EMBO J. 5, 2445–2451 (1986).

    Article  CAS  Google Scholar 

  11. Allen, J. P., Feher, G., Yeates, T. O., Komiya, H. & Rees, D. C. Proc. natn Acad. Sci. U.S.A. 84, 5730–5734 (1987).

    Article  ADS  CAS  Google Scholar 

  12. Chang, C. H. et al. FEBS Lett. 205, 82–86 (1986).

    Article  CAS  Google Scholar 

  13. Gunner, M. R. & Dutton, P. L. J. Am. chem. Soc. 111, 3400–3412 (1989).

    Article  CAS  Google Scholar 

  14. Therien, M. J. et al. in Electron Transfer in Inorganic, Organic and Biological Systems (eds Bolton, J., McLendon, G. L.&Mataga, N.) 191–199 (American Chemical Society, Washington DC 1991).

    Book  Google Scholar 

  15. Cowan, J. A., Upmacis, R. K., Beratan, D. N., Onuchic, J. N. & Gray, H. B. Ann. N. Y. Acad. Sci. 550, 68–84 (1988).

    Article  ADS  CAS  Google Scholar 

  16. Closs, G. L. & Miller, J. R. Science 240, 440–447 (1988).

    Article  ADS  CAS  Google Scholar 

  17. Fox, L. S., Kozik, M., Winkler, J. R. & Gray, H. B. Science 247, 1069–1071 (1990).

    Article  ADS  CAS  Google Scholar 

  18. Wasielewski, M. R., Niemczyk, M. P., Svec, W. A. & Pewitt, E. B. J. Am. chem. Soc. 107, 1080–1082 (1985).

    Article  CAS  Google Scholar 

  19. Joran, A. D. et al. Nature 327, 508–511 (1987).

    Article  ADS  CAS  Google Scholar 

  20. Franzen, S., Goldstein, R. F. & Boxer, S. G. J. phys. Chem. 94, 5135–5149 (1990).

    Article  CAS  Google Scholar 

  21. Gaines, G. L., O'Neil, M. P., Svec, W. A., Niemczyk, M. P. & Wasielewski, M. R. J. Am. chem. Soc. 113, 719–721 (1991).

    Article  CAS  Google Scholar 

  22. Wilier, J. R., Beitz, J. V. & Huddleston, R. K. J. Am. chem. Soc. 106, 5057–5068 (1984).

    Article  Google Scholar 

  23. Meade, T. J., Gray, H. B. & Winkler, J. R. J. Am. chem. Soc. 111, 4353–4356 (1989).

    Article  CAS  Google Scholar 

  24. Knapp, S. et al. J. Am. chem. Soc. 113, 4010–4013 (1991).

    Article  CAS  Google Scholar 

  25. Parson, W. W., Clayton, R. K. & Codgell, R. J. Biochim. biophys. Acta 387, 265–277 (1975).

    Article  CAS  Google Scholar 

  26. Schenck, C. C., Blankenship, R. E. & Parson, W. W. Biochim. biophys. Acta 680, 44–59 (1982).

    Article  CAS  Google Scholar 

  27. Chidsey, C. E. D., Kirmaier, C., Holten, D. & Boxer, S. G. Biochim. biophys. Acta 766, 424–437 (1985).

    Article  Google Scholar 

  28. Holten, D., Windsor, M. W., Parson, W. W. & Thornber, J. P. Biochim. biophys. Acta 501, 112–126 (1978).

    Article  CAS  Google Scholar 

  29. Shopes, R. J. & Wraight, C. A. Biochim. biophys. Acta 806, 348–356 (1985).

    Article  CAS  Google Scholar 

  30. Shuvalov, V. A. & Klevanik, A. V. FEBS Lett. 160, 51–55 (1983).

    Article  CAS  Google Scholar 

  31. Holzapfel, W. et al. Proc. natn. Acad. Sci. U.S.A. 87, 5168–5172 (1990).

    Article  ADS  CAS  Google Scholar 

  32. Michel-Beyerle, M. E. et al. Biochim. biophys. Acta 932, 52–70 (1988).

    Article  CAS  Google Scholar 

  33. Parson, W. W., Chu, Z. T. & Warshel, A. Biochim biophys Acta 1017, 251–272 (1990).

    Article  CAS  Google Scholar 

  34. Lockhart, D. J., Kirmaier, C., Holten, D. & Boxer, S. G. J. phys. Chem. 94, 6987–6995 (1990).

    Article  CAS  Google Scholar 

  35. Holzapfel, W. et al. Chem. Phys. Lett. 160, 1–7 (1989).

    Article  ADS  CAS  Google Scholar 

  36. Giangiacomo, K. M. & Dutton, P. L. Proc. natn. Acad. Sci. U.S.A. 86, 2658–2662 (1989).

    Article  ADS  CAS  Google Scholar 

  37. Takahashi, E. & Wraight, C. A. FEBS Lett. 283, 140–144 (1991).

    Article  CAS  Google Scholar 

  38. Shopes, R. J., Holten, D., Levine, L. & Wraight, C. A. Photosyn. Res. 12, 165–180 (1987).

    Article  CAS  Google Scholar 

  39. Gamow, G. Z. Phys. 51, 204–212 (1928).

    Article  ADS  CAS  Google Scholar 

  40. Beratan, D. N., Betts, J. N. & Onuchic, J. N. Science 252, 1285–1288 (1991).

    Article  ADS  CAS  Google Scholar 

  41. McLendon, G. Accts chem. Res. 21, 160–167 (1988).

    Article  CAS  Google Scholar 

  42. Tiede, D. M. et al. in The Photosynthetic Bacterial Reaction Center, Structure and Dynamics (eds Breton, J. & Vermeglio, A.) 13–20 (Plenum, New York, 1988).

    Book  Google Scholar 

  43. Dracheva, S. M. et al. Eur J. Biochem. 171, 253–264 (1988).

    Article  CAS  Google Scholar 

  44. Carithers, R. P. & Parson, W. W. Biochim. biophys. Acta 387, 194–211 (1975).

    Article  CAS  Google Scholar 

  45. Shopes, R. J. & Wraight, C. A. Biochim. biophys. Acta 893, 409–425 (1987).

    Article  CAS  Google Scholar 

  46. Wasielewski, M. R. & Niemczyk, M. P. in Porphyrins: Excited States and Dynamics (eds Gouterman, M., Rentzepis, P. M. & Straub, K. D.) 154–165 (Am. Chem. Soc., Little Rock, Arkansas, 1985).

    Google Scholar 

  47. Wasielewski, M. R., Niemczyck, M. P., Johnson, D. G., Svec, W. A. & Minsek, D. W. Tetrahedron 45, 4785–4806 (1989).

    Article  CAS  Google Scholar 

  48. MacQueen, D. B. & Schanze, K. S. J. Am. chem. Soc. 113, 7470–7479 (1991).

    Article  CAS  Google Scholar 

  49. Antolovich, M. et al. J. phys. Chem. 95, 1933–1941 (1991).

    Article  CAS  Google Scholar 

  50. Perkins, T. A., Hauser, B. T., Eyler, J. R. & Schanze, K. S. J. phys. Chem. 94, 8745–8748 (1990).

    Article  CAS  Google Scholar 

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Moser, C., Keske, J., Warncke, K. et al. Nature of biological electron transfer. Nature 355, 796–802 (1992). https://doi.org/10.1038/355796a0

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