Light induced oxidative water splitting in photosynthesis: Energetics, kinetics and mechanism

The essential steps of photosynthetic water splitting take place in Photosystem II (PS II) and comprise three different reaction sequences: (i) light induced formation of the radical pair P680+QA-, (ii) P680+ driven oxidative water splitting into O2 and four protons, and (iii) two step plastoquinone reduction to plastoquinol by QA-. This mini-review briefly summarizes our state of knowledge on energetics, kinetics and mechanism of oxidative water splitting. Essential features of the two types of reactions involved are described: (a) P680+ reduction by the redox active tyrosine Yz   and (b) sequence of oxidation steps induced by Yzox in the water-oxidizing complex (WOC).The rate of the former reaction is limited by the non-adiabatic electron transfer (NET) step and the multi-phase kinetics shown to originate from a sequence of relaxation processes. In marked contrast, the rate of the stepwise oxidation by Yzox of the WOC up to the redox level S3 is not limited by NET but by trigger reactions which probably comprise proton shifts and/or conformational changes. The overall rate of the final reaction sequence leading to formation and release of O2 is assumed to be limited by the electron transfer step from the S3 state of WOC to Yzox due to involvement of an endergonic redox equilibrium. Currently discussed controversial ideas on possible pathways are briefly outlined.Several crucial points of the mechanism of oxidative water splitting, like O–O bond formation, role of local proton shift(s), details of hydrogen bonding, are still not clarified and remain a challenging topic of future research.

Research highlights
► Energetics and mechanism of the multi-phase kinetics of P680+
• reduction by Yz.
► Energetics of Si state transitions, especially of YzoxS0→YZS1+noH+ and YzoxS3→→YZS0+O2+n3H+.
► Redox steps YzoxSi→YZSi+1+niH+ are rate limited by a triggered reaction for i = 0,1 and 2.
► The rate of reaction YzoxS3→→YZS0+O2+n3H+ is limited by an endergonic redox equilibrium.
► The dynamics of a local proton gradient are essential for O-O bond formation.