Oxidative photosynthetic water splitting: energetics, kinetics and mechanism

This minireview is an attempt to summarize our current knowledge on oxidative water splitting in photosynthesis. Based on the extended Kok model (Kok, Forbush, McGloin (1970) Photochem Photobiol 11:457-476) as a framework, the energetics and kinetics of two different types of reactions comprising the overall process are discussed: (i) P680+* reduction by the redox active tyrosine YZ of polypeptide D1 and (ii) Yz (ox) induced oxidation of the four step sequence in the water oxidizing complex (WOC) leading to the formation of molecular oxygen. The mode of coupling between electron transport (ET) and proton transfer (PT) is of key mechanistic relevance for the redox turnover of YZ and the reactions within the WOC. The peculiar energetics of the oxidation steps in the WOC assure that redox state S1 is thermodynamically most stable. This is a general feature in all oxygen evolving photosynthetic organisms and assumed to be of physiological relevance. The reaction coordinate of oxidative water splitting is discussed on the basis of the available information about the Gibbs energy differences between the individual redox states Si+1 and Si and the data reported for the activation energies of the individual oxidation steps in the WOC. Finally, an attempt is made to cast our current state of knowledge into a mechanism of oxidative water splitting with special emphasis on the formation of the essential O-O bond and on the active role of the protein in tuning the local proton activity that depends on time and redox state Si. The O-O linkage is assumed to take place at the level of a complexed peroxide.