Photosystem I pp 583-594 | Cite as

Application of Marcus Theory to Photosystem I Electron Transfer

  • Christopher C. Moser
  • P. Leslie Dutton
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 24)


To understand the engineering of light induced electron transfer and energy conversion, photosystem I (PS I) has been extensively reshaped by isolation, removal of protein subunits, and redox cofactors and in some cases reconstitution of exotic redox centers. Such manipulations together with Marcus theory and its biologically focused empirical derivations show that electron tunneling dominated electron transfer kinetics are established principally by the natural selection of distance between redox centers; the driving force and reorganization energy of each electron transfer step falls within a range that assures robust function, despite the repeated impact of mutation and change during evolution. Relatively simple empirical expressions for determining electron tunneling rates are more than adequate to understand the operation of PS I, especially since kinetic and preparative heterogeneity is common. Unlike other photosystems, the typical twofold symmetry of redox centers translates into a functionally relevant, near-symmetric two-branch pattern of electron transfer that culminates in the ability of the quinone on either branch to reduce the first redox center in the terminal iron–sulfur chain. Relatively small differences apparent in the kinetics of the two branches may reflect the tolerance of evolutionary drift in the thermodynamic properties of individual redox centers. Calculation suggests that productive charge separation, while slightly favoring the B chain chlorins, initially reduces both quinones roughly equally; long-term redox equilibration and short-circuiting charge recombination, however, tend to favor electron return through the A-branch.


Electron Transfer Slow Phase Electron Tunneling Charge Recombination Reorganization Energy 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Agalarov R and Brettel K (2003) Temperature dependence of biphasic forward electron transfer from the phylloquinone(s) A1 in photosystem I: only the slower phase is activated. Biochim Biophys Acta 1604: 7–12PubMedCrossRefGoogle Scholar
  2. Ashnagar A, Bruce JM, Dutton PL and Prince RC (1984) One- and two-electron reduction of hydroxy-1,4-naphthoquinones and hydroxy-9,10-anthraquinones. The role of internal hydrogen bonding and its bearing on the redox chemistry of the anthracycline antitumour quinones. Biochim Biophys Acta 801: 351–359PubMedGoogle Scholar
  3. Braun BS, Benbow U, Lloyd-Williams P, Bruce JM and Dutton PL (1986) Determination of partition coefficients of quinones by high-performance liquid chromatography. Methods Enzymol 125: 119–129PubMedCrossRefGoogle Scholar
  4. Brettel K (1997) Electron transfer and arrangement of the redox cofactors in photosystem I. Biochim Biophys Acta 1318: 322–373CrossRefGoogle Scholar
  5. Chamorovsky SK and Cammack R (1982) Direct determination of the midpoint potential of the acceptor-X in chloroplast photosystem-I by electrochemical reduction and electron-spin-resonance spectroscopy. Photobiochem Photobiophys 4: 195–200Google Scholar
  6. Evans MCW and Heathcote P (1980) Effects of glycerol on the redox properties of the electron-acceptor complex in spinach photosystem-I particles. Biochim Biophys Acta 590: 89–96PubMedCrossRefGoogle Scholar
  7. Evans MCW, Reeves SG and Cammack R (1974) Determination of oxidation-reduction potential of bound iron-sulfur proteins of primary electron-acceptor complex of photosystem-I in spinach-chloroplasts. FEBS Lett 49: 111–114PubMedCrossRefGoogle Scholar
  8. Fairclough WV, Forsyth A, Evans MCW, Rigby SEJ, Purton S and Heathcote P (2003) Bidirectional electron transfer in photosystem I: electron transfer on the psaA side is not essential for phototrophic growth in Chlamydomonas. Biochim Biophys Acta 1606: 43–55PubMedCrossRefGoogle Scholar
  9. Golbeck JH (1993) The structure of photosystem-I. Curr Opin Struct Biol 3: 508–514CrossRefGoogle Scholar
  10. Guergova-Kuras M, Boudreaux B, Joliot A, Joliot P and Redding K (2001) Evidence for two active branches for electron transfer in photosystem I. Proc Natl Acad Sci USA 98: 4437–4442PubMedCrossRefGoogle Scholar
  11. Gunner MR and Dutton PL (1989) Temperature and -delta-g-degrees dependence of the electron-transfer from BPh to Qa in reaction center protein from Rhodobacter-sphaeroides with different quinones as Qa. JACS 111: 3400–3412CrossRefGoogle Scholar
  12. Heathcote P, Hanley JA and Evans MCW (1993) Double-reduction of A1 abolishes the EPR signal attributed to A1: evidence for C2 symmetry in the photosystem I reaction centre. Biochim Biophys Acta 1144: 54–61CrossRefGoogle Scholar
  13. Hopfield JJ (1974) Electron transfer between biological molecules by thermally activated tunneling. Proc Natl Acad Sci USA 71: 3640–3664PubMedCrossRefGoogle Scholar
  14. Itoh S, Iwaki M and Ikegami I (2001) Modification of photosystem I reaction center by the extraction and exchange of chlorophylls and quinones. Biochim Biophys Acta 1507: 115–138PubMedCrossRefGoogle Scholar
  15. Ivashin N and Larsson S (2003) Electron transfer pathways in photosystem I reaction centers. Chem Phys Lett 375: 383–387CrossRefGoogle Scholar
  16. Iwaki M and Itoh S (1989) Electron transfer in spinach photosystem I reaction center containing benzo-, naphtho- and anthraquinones in place of phylloquinone. FEBS Lett 256: 11–16CrossRefGoogle Scholar
  17. Joliot P and Joliot A (1999) In vivo analysis of the electron transfer within photosystem I: are the two phylloquinones involved? Biochemistry 38: 11130–11136PubMedCrossRefGoogle Scholar
  18. Jordan R, Nessau U and Schlodder E (1998) Charge recombination between reduced iron–sulfur clusters and P700+. In: Garab G (ed) Photosynthesis: Mechanisms and Effects. Pp 663–666 Kluwer Academic Publishers, DordrechtGoogle Scholar
  19. Kleinherenbrink FAM, Hastings G, Wittmershaus BP and Blankenship RE (1994) Delayed fluorescence from Fe-S type photosynthetic reaction centers at low redox potential. Biochemistry 33: 3096–3105PubMedCrossRefGoogle Scholar
  20. Klukas O, Schubert WD, Jordan P, Krauß N, Fromme P, Witt HT and Saenger W (1999) Localization of two phylloquinones, QK and QK′, in an improved electron density map of photosystem I at 4-Ångstrom resolution. J Biol Chem 274: 7361–7367PubMedCrossRefGoogle Scholar
  21. Krabben L, Schlodder E, Jordan R, Carbonera D, Giacometti G, Lee H, Webber AN and Lubitz W (2000) Influence of the axial ligands on the spectral properties of P700 of photosystem I: a study of site-directed mutants. Biochemistry 39: 13012–13025PubMedCrossRefGoogle Scholar
  22. Kumazaki S, Iwaki M, Ikegami I, Kandori H, Yoshihara K and Itoh S (1994) Rates of primary electron-transfer reactions in the photosystem-I reaction-center reconstituted with different quinones as the secondary acceptor. J Phys Chem 98: 11220–11225CrossRefGoogle Scholar
  23. Levich VG and Dogonadze RR (1959) Teiriya bezizluchatelnikh electronnikh perekhodov mezhdu ionami v rastvorakh. Dokl Akad Nauk SSSR 124: 123–126Google Scholar
  24. Lin X, Williams JC, Allen JP and Mathis P (1994) Relationship between rate and free-energy difference for electron-transfer from cytochrome c (2) to the reaction-center in Rhodobacter sphaeroides. Biochemistry 33: 13517–13523PubMedCrossRefGoogle Scholar
  25. Marcus RA (1956) On the theory of oxidation-reduction reactions involving electron transfer: I. J Chem Phys 24: 966–978CrossRefGoogle Scholar
  26. Marcus RA and Sutin N (1985) Electron transfers in chemistry and biology. Biochim Biophys Acta 811: 265–322Google Scholar
  27. Moser CC and Dutton PL (1992) Engineering protein structure for electron transfer function in photosynthetic reaction centers. Biochim Biophys Acta 1101: 171–176PubMedGoogle Scholar
  28. Moser CC, Keske JM, Warncke K, Farid RS and Dutton PL (1992) Nature of biological electron transfer. Nature 355: 796–802PubMedCrossRefGoogle Scholar
  29. Moser CC, Page CC and Dutton PL (2001). Photosynthesis: bacterial reaction center. In: Balzani V (ed) Electron Transfer in Chemistry, pp 24–38. Wiley-VCH, New YorkGoogle Scholar
  30. Page CC, Moser CC, Chen X and Dutton PL (1999) Natural engineering principles of electron tunneling in biological oxidation-reduction. Nature 402: 47–52PubMedCrossRefGoogle Scholar
  31. Parrett KG, Mehari T, Warren PG and Golbeck JH (1989) Purification and properties of the intact P-700 and FX-containing photosystem-I core protein. Biochim Biophys Acta 973: 324–332PubMedGoogle Scholar
  32. Ramesh VM, Guergova-Kuras M, Joliot P and Webber AN (2002) Electron transfer from plastocyanin to the photosystem I reaction center in mutants with increased potential of the primary donor in Chlamydomonas reinhardtii. Biochemistry 41: 14652–14658PubMedCrossRefGoogle Scholar
  33. Sakuragi Y, Zybailov B, Shen GZ, Jones AD, Chitnis PR, van der Est A, Bittl R, Zech S, Stehlik D, Golbeck JH and Bry-ant DA (2002) Insertional inactivation of the menG gene, encoding 2-phytyl-1,4-naphthoquinone methyltransferase of Synechocystis sp. PCC 6803, results in the incorporation of 2-phytyl-1, 4-naphthoquinone into the A1 site and alteration of the equilibrium constant between A1 and FX in photosystem I. Biochemistry 41: 394–405.PubMedCrossRefGoogle Scholar
  34. Savikhin S, Xu W, Martinsson P, Chitnis PR and Struve WS (2001) Kinetics of charge separation and A0 → A1 electron transfer in photosystem reaction centers. Biochemistry 40: 9282–9290PubMedCrossRefGoogle Scholar
  35. Schlodder E, Falkenberg K, Gergeleit M and Brettel K (1998) Temperature dependence of forward and reverse electron tranfer from A1 , the reduced secondary electron acceptor in photosystem I. Biochemistry 37: 9466–9476PubMedCrossRefGoogle Scholar
  36. Sétif P and Bottin H (1989) Identification of electron-transfer reactions involving the acceptor-A1 of photosystem-I at room-temperature. Biochemistry 28: 2689–2697CrossRefGoogle Scholar
  37. Sétif P and Brettel K (1993) Forward electron transfer from phylloquinone A1 to iron-sulfur centers in spinach photosystem I. Biochemistry 32: 7846–7854PubMedCrossRefGoogle Scholar
  38. Shinkarev VP, Zybailov B, Vassiliev IR and Golbeck JH (2002) Modeling of the P700+ charge recombination kinetics with phylloquinone and plastoquinone-9 in the A1 site of photosystem I. Biophys J 83: 2885–2897PubMedCrossRefGoogle Scholar
  39. Shuvalov VA (1976) The study of the primary photoprocesses in photosystem I of chloroplasts recombination luminescence, chlorophyll triplet state and triplet-triplet annihilation. Biochim Biophys Acta 430: 113–121PubMedCrossRefGoogle Scholar
  40. Vos MH and van Gorkom HJ (1988) Thermodynamics of electron transport in photosystem I studied by electric field-stimulated charge recombination. Biochim Biophys Acta 934: 293–302CrossRefGoogle Scholar
  41. Vos MH and Van Gorkom HJ (1990) Thermodynamical and structural information on photosynthetic systems obtained from electroluminescence kinetics. Biophys J 58: 1547–1555PubMedGoogle Scholar
  42. Warncke K and Dutton PL (1993) Influence of Qa site redox cofactor structure on equilibrium binding, in situ electrochemistry, and electron-transfer performance in the photosynthetic reaction center protein. Biochemistry 32: 4769–4779PubMedCrossRefGoogle Scholar
  43. Zech SG, van der Est AJ and Bittll R (1997) Measurement of cofactor distances between P700+ and A1 in native and quinone-substituted photosystem I using pulsed electron paramagnetic resonance spectroscopy. Biochemistry 36: 9774–9779PubMedCrossRefGoogle Scholar
  44. Zybailov B, van der Est A, Zech SG, Teutloff C, Johnson TW, Shen G, Bittl R, Stehlik D, Chitnis PR and Golbeck JH (2000) Recruitment of a foreign quinone into the A1 site of photosystem I-II. Structural and functional characterization of phylloquinone biosynthesis pathway mutants by electron paramagnetic resonance and electron-nuclear double resonance spectroscopy. J Biol Chem 275: 8531–8539PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • Christopher C. Moser
    • 1
  • P. Leslie Dutton
    • 1
  1. 1.Department of Biochemistry and BiophysicsUniversity of PennsylvaniaPhiladelphiaUSA

Personalised recommendations