Advertisement

Photosynthesis Research

, Volume 22, Issue 3, pp 173–186 | Cite as

Electron tunneling pathways in proteins: influences on the transfer rate

  • David N. Beratan
  • José Nelson Onuchic
Theory Regular Paper

Abstract

A strategy for calculating the tunneling matrix element dependence on the medium intervening between donor and acceptor in specific proteins is described. The scheme is based on prior studies of small molecules and is general enough to allow inclusion of through bond and through space contributions to the electronic tunneling interaction. This strategy should allow the prediction of relative electron transfer rates in a number of proteins. It will therefore serve as a design tool and will be explicitly testable, in contrast with calculations on single molecules. As an example, the method is applied to ruthenated myoglobin and the tunneling matrix elements are estimated. Quantitative improvements of the model are described and effects due to motion of the bridging protein are discussed. The method should be of use for designing target proteins having tailored electron transfer rates for production with site directed mutagenesis. The relevance of the technique to understanding certain photosynthetic reaction center electron transfer rates is discussed.

Key words

electronic coupling electron transfer pathways electron transfer theory electron tunneling nuclear tunneling protein mediated electronic coupling tunneling matrix element 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Allen JP, Feher G, Yeates TO, Komiya H and Rees DC (1988) Structure of the reaction center from Rhodobacter sphaeroides R-26: Protein-cofactor (quinones and Fe2+) interactions. Proc Natl Acad Sci (USA) 85: 8487–8491Google Scholar
  2. Axup AW, Albin MA, Mayo SL, Crutchley RJ and Gray HB (1988) Distance dependence of photoinduced long-range electron transfer in zinc-ruthenium-modified myoglobins. J Am Chem Sco 110: 435–439Google Scholar
  3. Beratan DN and Hopfield JJ (1984) Calculation of electron tunneling matrix elements in rigid systems: mixed-valence dithiaspirocyclobutane. J Am Chem Soc 106: 1584–1594Google Scholar
  4. Beratan DN, Onuchic JN and Hopfield JJ (1985) Limiting forms of the tunneling matrix element in the long distance bridge mediated electron transfer problem. J Chem Phys 83: 5325–5329Google Scholar
  5. Beratan DN, Onuchic HN and Hopfield JJ (1987) Electron transfer through covalent and noncovalent pathways in proteins. J Chem Phys 86: 4488–4498Google Scholar
  6. Betts J, Beratan DN, Bowler BE, Onuchic JN and Gray HB, Work in progressGoogle Scholar
  7. Bixon M and Jortner J (1986) Coupling of protein modes to electron transfer in bacterial photosynthesis. J Phys Chem 90: 3795–3800Google Scholar
  8. Bowler B, Meade TJ, Mayo SL, Richards and GrayHB (1989) Long range electron transfer in structurally engineered [pentaammineruthenium(histidine-62)]-cytochrome c. PreprintGoogle Scholar
  9. Chance B et al. (eds) (1979) Tunneling in Biological Systems. New York: Academic PressGoogle Scholar
  10. Cowan JA, Upmacis RK, Beratan DN, Onuchic JN and Gray HB (1988) Long range electron transfer in myoglobin. Ann NY Acad Sci 550: 68–84Google Scholar
  11. DeVault D (1984) Quantum Mechanical Tunneling in Biological Systems, 2nd edition. New York: Cambridge PressGoogle Scholar
  12. DeVault D and Chance B (1966) Studies of photosynthesis using a pulsed laser I. Temperature dependence of cytochrome oxidation rate in chromatium. Evidence for tunneling. Biophys J 6: 825–847Google Scholar
  13. Feher G Personal communication. Site directed mutagenesis studies are now being performed on these systemsGoogle Scholar
  14. Fischer SF and Scherer POJ (1987) On the initial charge separation in bacterial reaction centers: long range electron transfer via an exciton-charge transfer (ECT) coupling mechanism. Chem Phys Lett 141: 179–185Google Scholar
  15. Frauenfelder H and Wolynes PG (1985) Rate theories and puzzles of hemoprotein kinetics. Science 229: 337–345Google Scholar
  16. Govindjee (ed) (1982) Photosynthesis. New York: Academic PressGoogle Scholar
  17. Grigorov LN and Chernavskii DS (1972) Quantum mechanical model of electron transfer from cytochrome to chlorophyll in photosynthesis. Biofizika 17: 202–209 (English translation)Google Scholar
  18. Halpern J and Orgel L (1960) The theory of electron transfer between metal ions in bridged systems. Discuss Faraday Soc 29: 32–41Google Scholar
  19. Hopfield JJ (1974) Electron transfer between biological molecules by thermally activated tunneling. Proc Natl Acad Sci (USA) 71: 3640–3644Google Scholar
  20. Jackman MP, McGinnis J, Powls R, Salmon GA and Sykes AG (1988) Preparation and characterization of two His-59 ruthenium-modified algal plastocyanins and an unusually small rate constant for ruthenium (II) → copper (II) intramolecular electron transfer over ∼ 12 Å. J Am Chem Soc 110: 5880–5887Google Scholar
  21. Jortner J (1976) Temperature dependent activation energy for electron transfer between biological molecules. J Chem Phys 64: 4860–4867Google Scholar
  22. Kuki A (1989) Personal communicationGoogle Scholar
  23. Kuki A and Wolynes PG (1987) Electron tunneling paths in proteins. Science 236: 1647–1652Google Scholar
  24. Larsson S (1981) Electron transfer in chemical and biological systems. Orbital rules for nonadiabatic transfer. J Am Chem Soc 103: 4034–4040Google Scholar
  25. Liang N, Pielak GJ, Mauk AG, Smith M and Hoffman BM (1987) Yeast cytochrome c with phenylalanine or tyrosine at position 87 transfers electrons to (zinc cytochrome c peroxidase)+ at a rate ten thousand times that of the serine-87 or glycine-87 variants. Proc Natl Acad Sci (USA) 84: 1249–1252Google Scholar
  26. Michel-Beyerle ME, Plato M, Deisenhofer J, Michel H, Bixon M and Jortner J (1988) Unidirectionality of charge separation in reaction centers of photosynthetic bacteria. Biochim Biophys Acta 932: 52–70Google Scholar
  27. McConnell H (1961) Intramolecular charge transfer in aromatic free radicals. J Chem Phys 35: 508–515Google Scholar
  28. Newton MD (1988) Electronic structure analysis of electron transfer matrix elements for transition metal redox pairs. J Phys Chem 92: 3049–3056Google Scholar
  29. Onuchic JN and Beratan DN (1987) Molecular bridge effects on distant charge tunneling. J Am Chem Soc 109: 6771–6778Google Scholar
  30. Onuchic JN and Beratan DN (1989) Submitted for publicationGoogle Scholar
  31. Onuchic JN, Beratan DN and Hopfield JJ (1986) Some aspects of electron transfer reaction dynamics. J Phys Chem 90: 3707–3721Google Scholar
  32. Onuchic JN and Wolynes PG (1988) Classical and quantum pictures of reaction dynamics in condensed matter: resonances, dephasing, and all that. J Phys Chem 92: 6495–6503Google Scholar
  33. Peterson-Kennedy SE, McGourty JL, Kalweit JA and Hoffman B (1986) Temperature dependence of and ligation effects on long range electron transfer in complementary [Zn, FeIII] hemoglobin hybrids. J Am Chem Soc 108: 1739–1746Google Scholar
  34. Plato M, Mobius K, Michel-Beyerle ME, Bixon M and Jortner J (1988) Intramolecular electronic interactions in the primary charge separation in bacterial photosynthesis. J Am Chem Soc 110: 7279–7285Google Scholar
  35. Sneddon SF, Morgan RS and Brooks CL (1988) A new classification of the amino acid side chains based on doublet acceptor energy levels. Biophys J 53: 83–89Google Scholar
  36. Warshal A and Parson W (1987) Spectroscopic properties of photosynthetic reaction centers. 1. Theory. J Am Chem Soc 109: 6143–6152Google Scholar
  37. Yates K (1971) Hückel Molecular Orbital Theory. New York: Academic PressGoogle Scholar
  38. Yeates TO, Komiya H, Chirino A, Rees DC, Allen JP and Feher G (1988) Structure of the reaction center from Rhodobacter sphaeroides R-26 and 2.4.1: Protein-cofactor (bacteriochlorophyll, bacteriopheophytin, and carotenoid) interactions. Proc Natl Acad Sci (USA) 85: 7993–7997Google Scholar

Copyright information

© Kluwer Academic Publishers 1989

Authors and Affiliations

  • David N. Beratan
    • 1
  • José Nelson Onuchic
    • 2
  1. 1.Jet Propulsion LaboratoryCalifornia Institute of TechnologyPasadenaUSA
  2. 2.Instituto de Fisica e Quimica de São CarlosUniversidade de São PauloSão Carlos, SPBrazil

Personalised recommendations