Photosynthetic oxygen evolution: H/D isotope effects and the coupling between electron and proton transfer during the redox reactions at the oxidizing side of Photosystem II

The oxygen evolving complex (OEC) of Photosystem II (PS TI) incorporates a Mn-cluster and probably a further redox cofactor, X. Four quanta of light drive the OEC through the increasingly oxidized states S-0 double right arrow S-1 double right arrow S-2 double right arrow S-3 double right arrow S-4 to yield O-2 during the transition S-4-->S-0. It has been speculated that the oxidation of water might be kinetically facilitated by the abstraction of hydrogen. This implied that the respective electron acceptor is deprotonated upon oxidation. Whether Y-Z and X fulfill this expectation is under debate. We have previously inferred a 'chemical' deprotonation of X based on the kinetics of proton release (Haumann M, Drerenstedt W, Hundelt M and Junge W (1996) Biochim Biophys Acta 1273: 237-250. Here, we investigated the rates of electron transfer and proton release as function of the D2O/H2O ratio, the pH, and the temperature both in thylakoids and PS II core particles. The largest kinetic isotope effect on the rate of electron transfer (factor of 2.1-2.4) and the largest pH-dependence (factor of about 2 between pH 5 and 8) was found on S-2 double right arrow S-3 where X is oxidized. During the other transitions both factors were much smaller (less than or equal to 1.4). Electron transfer is probably kinetically steered by proton transfer only during S-2 double right arrow S-3. These results corroborate the notion that X-. serves as a hydrogen acceptor for bound water during S-4-->S-0. We propose a consistent scheme for the final reaction with water to yield dioxygen: two two-electron (hydrogen) transfers in series with a peroxide intermediate.