Application of the Marcus theory for analysis of the temperature dependence of the reactions leading to photosynthetic water oxidation: results and implications

Abstract

The temperature dependence of donor side reactions was analysed within the framework of the Marcus theory of nonadiabatic electron transfer. The following results were obtained for PS II membrane fragments from spinach: (1) the reorganisation energy of P680+• reduction by YZ is of the order of 0.5 eV in samples with a functionally fully competent water oxidising complex (WOC); (2) destruction of the WOC by Tris-washing gives rise to a drastic increase of λ to values of the order of 1.6 eV; (3) the reorganisation energies of the oxidation steps in the WOC are dependent, on the redox states Si with values of about 0.6 eV for the reactions YZOXS0→YZS1 and YZOXS1→YZS2, 1.6 eV for the reaction YZOXS2→YZS3 and 1.1 eV (above a characteristic temperature uc of about 6 °C) for the reaction YZOXS3→→YZS0+O2. Using an empirical rate constant-distance relationship, the van der Waals distance between YZ and P680 was found to be about 10 A, independent of the presence or absence of the WOC, whereas the distance between YZ and the manganese cluster in the WOC was ≥15 A. Based on the calculated activation energies the environment of YZ is inferred to be almost "dry" and hydrophobic when the WOC is intact but becomes enriched with water molecules after WOC destruction. Furthermore, it is concluded that the transition S2→S3 is an electron transfer reaction gated by a conformational change, i.e. it comprises significant structural changes of functional relevance. Measurements of kinetic H/D isotope exchange effects support the idea that none of these reactions is gated by the break of a covalent O-H bond. The implications of these findings for the mechanism of water oxidation are discussed.