Photosynthetic oxygen evolution: H/D isotope effects and the coupling between electron and proton transfer during transitions S-2 double right arrow S-3 and S-3 double right arrow S-4->S-0

Abstract

The oxygen evolving complex (OEC) of photosystem II (PS II) incorporates a tetra Mn-cluster, tyrosine (Y-Z) and probably one histidine residue (X) as redox cofactors. 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 S-4-->S-0. It has been speculated that some oxidized cofactor abstracts hydrogen from bound water. This implies that its oxidoreduction is electroneutral and linked to its deprotonation. To identify such steps we investigated the rates of electron transfer and proton release as function of the D2O/H2O ratio, the pH, and the temperature in thylakoids and PS II core particles. Upon oxidation of X on S-2 double right arrow S-3, a rise of the pH from 5 to 8 increased the rate of the electron transfer to Y-Z by a factor of 2,5 and substitution of D2O for H2O gave an isotopic ratio of 2.1. Contrastingly, during all other transitions, including the O-2-evolving step S-4-->S-0, the electron transfer rate was much less sensitive to these parameters (factors of less than or equal to 1.4). These results suggest a kinetical steering role of proton transfer only during S-2 double right arrow S-3. We propose that X(.) (His(.)?) serves as a hydrogen acceptor for bound water during S-4-->S-0.