Molecular basis for turnover inefficiencies (misses) during water oxidation in photosystem II

Photosynthesis stores solar light as chemical energy and efficiency of this process is highly important. The electrons required for CO₂ reduction are extracted from water in a reaction driven by light-induced charge separations in the Photosystem II reaction center and catalyzed by the CaMn₄O₅-cluster. This cyclic process involves five redox intermediates known as the S₀-S₄ states. In this study, we quantify the flash-induced turnover efficiency of each S state by electron paramagnetic resonance spectroscopy. Measurements were performed in photosystem II membrane preparations from spinach in the presence of an exogenous electron acceptor at selected temperatures between -10 °C and +20 °C and at flash frequencies of 1.25, 5 and 10 Hz. The results show that at optimal conditions the turnover efficiencies are limited by reactions occurring in the water oxidizing complex, allowing the extraction of their S state dependence and correlating low efficiencies to structural changes and chemical events during the reaction cycle. At temperatures 10 °C and below, the highest efficiency (i.e. lowest miss parameter) was found for the S₁ → S₂ transition, while the S₂ → S₃ transition was least efficient (highest miss parameter) over the whole temperature range. These electron paramagnetic resonance results were confirmed by measurements of flash-induced oxygen release patterns in thylakoid membranes and are explained on the basis of S state dependent structural changes at the CaMn₄O₅-cluster that were determined recently by femtosecond X-ray crystallography. Thereby, possible "molecular errors" connected to the e ^- transfer, H⁺ transfer, H₂O binding and O₂ release are identified.