Unequal misses during the flash-induced advancement of photosystem II: effects of the S state and acceptor side cycles

Photosynthetic water oxidation is catalyzed by the oxygen-evolving complex (OEC) in photosystem II (PSII). This process is energetically driven by light-induced charge separation in the reaction center of PSII, which leads to a stepwise accumulation of oxidizing equivalents in the OEC (S(i) states, i = 0–4) resulting in O(2) evolution after each fourth flash, and to the reduction of plastoquinone to plastoquinol on the acceptor side of PSII. However, the S(i)-state advancement is not perfect, which according to the Kok model is described by miss-hits (misses). These may be caused by redox equilibria or kinetic limitations on the donor (OEC) or the acceptor side. In this study, we investigate the effects of individual S state transitions and of the quinone acceptor side on the miss parameter by analyzing the flash-induced oxygen evolution patterns and the S(2), S(3) and S(0) state lifetimes in thylakoid samples of the extremophilic red alga Cyanidioschyzon merolae. The data are analyzed employing a global fit analysis and the results are compared to the data obtained previously for spinach thylakoids. These two organisms were selected, because the redox potential of Q(A)/Q(A)(−) in PSII is significantly less negative in C. merolae (E(m) = − 104 mV) than in spinach (E(m) = − 163 mV). This significant difference in redox potential was expected to allow the disentanglement of acceptor and donor side effects on the miss parameter. Our data indicate that, at slightly acidic and neutral pH values, the E(m) of Q(A)(−)/Q(A) plays only a minor role for the miss parameter. By contrast, the increased energy gap for the backward electron transfer from Q(A)(−) to Pheo slows down the charge recombination reaction with the S(3) and S(2) states considerably. In addition, our data support the concept that the S(2) → S(3) transition is the least efficient step during the oxidation of water to molecular oxygen in the Kok cycle of PSII.