Molecular basis for turnover inefficiencies (misses) during water oxidation in photosystem II.
Guangye HanPetko ChernevStenbjörn StyringJohannes MessingerFikret MamedovPublished in: Chemical science (2022)
Photosynthesis stores solar light as chemical energy and efficiency of this process is highly important. The electrons required for CO 2 reduction are extracted from water in a reaction driven by light-induced charge separations in the Photosystem II reaction center and catalyzed by the CaMn 4 O 5 -cluster. This cyclic process involves five redox intermediates known as the S 0 -S 4 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 S 1 → S 2 transition, while the S 2 → S 3 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 CaMn 4 O 5 -cluster that were determined recently by femtosecond X-ray crystallography. Thereby, possible "molecular errors" connected to the e - transfer, H + transfer, H 2 O binding and O 2 release are identified.