Photosynthesis Research

, Volume 55, Issue 2–3, pp 147–152 | Cite as

Oscillations of the energy gap for the initial electron-transfer step in bacterial reaction centers

  • William W. Parson
  • Zhen Tao Chu
  • Arieh Warshel
Article

Abstract

Oscillations in the electrostatic energy gap [ΔVelec(t)] for electron transfer from the primary electron donor (P) to the adjacent bacteriochlorophyll (B) in photosynthetic bacterial reaction centers are examined by molecular-dynamics simulations. Autocorrelation functions of ΔVelec in the reactant state (PB) include prominent oscillations with an energy of 17 cm−1. This feature is much weaker if the trajectory is propagated in the product state P+B. The autocorrelation functions also include oscillations in the regions of 5, 80 and 390 cm−1 in both states, and near 25 and 48 cm−1 in P+B. The strong 17-cm−1 oscillation could involve motions that modulate the distance between P and B, because a similar oscillation occurs in the direct electrostatic interactions between the electron carriers.

computer simulations electron transfer energy gap molecular dynamics oscillations reaction centers (bacterial) 

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References

  1. Alden RG, Parson WW, Chu ZT and Warshel A (1995) Calculations of electrostatic energies in photosynthetic reaction centers. J Am Chem Soc 117: 12284–12298Google Scholar
  2. Alden RG, Parson WW, Chu ZT and Warshel A (1996) Orientation of the OH Dipole of Tyrosine (M)210 and its effect on electrostatic energies in photosynthetic bacterial reaction centers. J Phys Chem 100: 16761–16770Google Scholar
  3. Boxer SG, Lockhart DJ and Middendorf TR (1986) Photochemical hole burning in photosynthetic reaction centers. Chem Phys Lett 123: 476–482Google Scholar
  4. Cherepy NJ, Shreve AP, Moore LJ, Franzen S, Boxer SG and Mathies RA (1994) Near-infrared resonance Raman spectroscopy of the special pair and the accessory bacteriochlorophylls in photosynthetic reaction centers. J Phys Chem 98: 6023–6029Google Scholar
  5. Cherepy NJ, Holzwarth AA and Mathies RA (1995) Near-infrared resonance Raman spectra of Chloroflexus aurantiacus photosynthetic reaction centers. Biochemistry 34: 5288–5293Google Scholar
  6. Cherepy NJ, Shreve AP, Moore LJ, Boxer SG and Mathies RA (1997) Electronic and nuclear dynamics of the accessory bacteriochlorophylls in bacterial photosynthetic reaction centers from resonance Raman intensities. J Phys Chem 101: 3250–3260Google Scholar
  7. Czarnecki K, Chynwat V, Erickson JP, Frank HA and Bocian DF (1997a) Characterization of the strongly coupled, low-frequency vibrational modes of the special pair of photosynthetic reaction centers via isotopic labeling of the cofactors. J Am Chem Soc 119: 415–426Google Scholar
  8. Czarnecki K, Chynwat V, Erickson JP, Frank HA and Bocian DF (1997b) Identification of the magnesium-histidine stretching vibration of the bacteriochlorophyll cofactors in photosynthetic reaction centers via N-15-labeling of the histidines. J Am Chem Soc 119: 2594–2595Google Scholar
  9. Deisenhofer J, Epp O, Sinning I and Michel H (1995) Crystallographic refinement at 2.3 Å resolution and refined model of the photosynthetic reaction center from Rhodopseudomonas viridis. J Mol Biol 246: 429–457Google Scholar
  10. Gehlen JN, Marchi M and Chandler M (1994) Dynamics affecting the primary charge transfer in photosynthesis. Science 263: 499–502Google Scholar
  11. Hayes JM and Small GJ (1986) Photochemical hole burning and strong electron-phonon coupling: Primary donor states of reaction centers of photosynthetic bacteria. J Phys Chem 90: 4928–4931Google Scholar
  12. Hwang J-K and Warshel A (1987) Microscopic examination of free energy relationships for electron transfer in polar solvents. J Am Chem Soc 109: 715–720Google Scholar
  13. Jankowiak R, Hayes JM and Small GJ (1993) Spectral hole-burning spectroscopy in amorphous molecular solids and proteins. Chem Rev 93: 1471–1502Google Scholar
  14. Johnson SG, Tang D, Jankowiak R, Hayes JM, Small GJ and Tiede DM(1993) Photochemical hole-burned spectra of protonated and deuterated reaction centers of Rhodobacter sphaeroides. J Phys Chem 97: 6924–6933Google Scholar
  15. Klevanik AV, Ganago AO, Shkuropatov AY and Shuvalov VA (1988) Electron-phonon and vibronic structure of absorption spectra of the primary electron donor in reaction centers of Rhodopseudomonas viridis, Rhodobacter sphaeroides and Chloroflexus aurantiacus at 1.7–70 K. FEBS Lett 237: 61–64Google Scholar
  16. Lee FS and Warshel A (1992) A local reaction field method for fast evaluation of long-range electrostatic interactions in molecular simulations. J Chem Phys 97: 3100–3107Google Scholar
  17. Lee FS, Chu ZT and Warshel A (1993) Microscopic and semimicroscopic calculations of electrostatic energies in proteins by the POLARIS and ENZYMIX programs. J Comp Chem 14: 161–185Google Scholar
  18. Luzhkov V and Warshel A (1992) Microscopic models for quantum mechanical calculations of chemical processes in solutions: LD/AMPAC and SCAAS/AMPAC calculations of solvation energies. J Comp Chem 13: 199–213Google Scholar
  19. Middendorf TR, Mazzola LT, Gaul DF, Schenck CC and Boxer SG (1991) Photochemical hole-burning spectroscopy of a photosynthetic reaction center mutant with altered charge separation kinetics: Properties and decay of the initially excited state. J Phys Chem 95-10142–10151Google Scholar
  20. Palaniappan V, Schenck CC and Bocian DF (1995) Low-frequency near-infrared-excitation resonance Raman spectra of (M)H202L mutant reaction centers from Rhodobacter sphaeroides. Implications for the structural, vibronic, and electronic properties of the bacteriochlorin cofactors. J Phys Chem 99: 17049–17058Google Scholar
  21. Parson WW and Warshel A (1987) Spectroscopic properties of photosynthetic reaction centers. 2. Application of the theory to Rhodopseudomonas viridis. J Am Chem Soc 109: 6152–6163Google Scholar
  22. Parson WW and Warshel A (1995) Theoretical analyses of electrontransfer reactions. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 559–575. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  23. Parson WW, Chu ZT and Warshel A (1990) Electrostatic control of charge separation in bacterial photosynthesis. Biochim Biophys Acta 1017: 251–272Google Scholar
  24. Parson WW, Chu ZT and Warshel A (1998) Reorganization energy of the initial electron-transfer step in photosynthetic bacterial reaction centers. Biophys J (in press)Google Scholar
  25. Schulten K and Tesch M (1991) Coupling of protein motion to electron transfer: Molecular dynamics and stochastic quantum mechanics study of photosynthetic reaction centers. Chem Phys 158: 421–446Google Scholar
  26. Shreve AP, Cherepy NJ, Franzen S, Boxer SG and Mathies RA (1991) Rapid-flow resonance Raman spectroscopy of bacterial photosynthetic reaction centers. Proc Natl Acad Sci USA 88: 11207–11211Google Scholar
  27. Souaille M and Marchi M (1997) Nuclear dynamics and electronic transition in a photosynthetic reaction center. J Am Chem Soc 119: 3948–3958Google Scholar
  28. Stanley RJ and Boxer SG (1995) Oscillations in spontaneous fluorescence from photosynthetic reaction centers. J Phys Chem 99: 859–863Google Scholar
  29. Streltsov AM, Vulto SI, Hoff AJ, Aartsma TJ and Shuvalov VA (1997) Oscillations within the BL absorption band Rhodobacter sphaeroides reaction centers upon 30-fs excitation at 865 nm. Abstr Proc Cadarache III ConfGoogle Scholar
  30. Vos MH, Rappaport F, Lambry J-H, Breton J and Martin J-L (1993) Visualization of coherent nuclear motion in a membrane protein by femtosecond spectroscopy. Nature 363: 320–325Google Scholar
  31. Vos MH, Jones MR, Hunter CN, Breton J, Lambry J-C and Martin J-L (1994a) Coherent dynamics during the primary electron-transfer reaction in membrane-bound reaction centers of Rhodobacter sphaeroides. Biochemistry 33: 6750–6757Google Scholar
  32. Vos MH, Jones MR, Hunter CN, Breton J and Martin J-L (1994b) Coherent nuclear dynamics at room temperature in bacterial reaction centers. Proc Natl Acad Sci USA 91: 12701–12705Google Scholar
  33. Warshel A and Parson WW (1991) Computer simulations of electron-transfer reactions in solution and in photosynthetic reaction centers. Ann Rev Phys Chem 42: 279–309Google Scholar
  34. Warshel A, Sussman F and King G (1986) The free energies of charges in solvated proteins. Microscopic calculations using a reversible charging process. Biochemistry 25: 8368–8372Google Scholar
  35. Warshel A, Chu Z-T and Parson WW (1989) Dispersed polaron simulations of electron transfer in photosynthetic reaction centers. Science 246: 112–116Google Scholar
  36. Warshel A, Chu ZT and Hwang J-K (1991) The dynamics of the primary event in rhodopsins revisited. Chem Phys 158: 303–314Google Scholar
  37. Warshel A, Chu ZT and Parson WW (1994) On the energetics of the primary electron-transfer process in bacterial reaction centers. Photochem Photobiol A Chem 82: 123–128Google Scholar
  38. Woodbury NW, Peloquin JM, Alden RG, Lin X, Taguchi AKW, Williams JC and Allen JP (1994) Relationship between thermodynamics and mechanim during photoinduced charge separation in reaction centers from Rhodobacter sphaeroides. Biochemistry 33: 8101–8112Google Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • William W. Parson
    • 1
  • Zhen Tao Chu
    • 2
  • Arieh Warshel
    • 2
  1. 1.Department of BiochemistryUniversity of WashingtonSeattleUSA
  2. 2.Department of ChemistryUniversity of Southern CaliforniaLos AngelesUSA

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