Estimation of the driving force for dioxygen formation in photosynthesis

Photosynthetic water oxidation to molecular oxygen is carried out by photosystem II (PSII) over a reaction cycle involving four photochemical steps that drive the oxygen-evolving complex through five redox states Si (i = 0,…, 4). For understanding the catalytic strategy of biological water oxidation it is important to elucidate the energetic landscape of PSII and in particular that of the final S4 → S0 transition. In this short-lived chemical step the four oxidizing equivalents accumulated in the preceding photochemical events are used up to form molecular oxygen, two protons are released and at least one substrate water molecule binds to the Mn4CaO5 cluster. In this study we probed the probability to form S4 from S0 and O2 by incubating YD-less PSII in the S0 state for 2–3 days in the presence of (18)O2 and H2(16)O. The absence of any measurable (16,18)O2 formation by water-exchange in the S4 state suggests that the S4 state is hardly ever populated. On the basis of a detailed analysis we determined that the equilibrium constant K of the S4 → S0 transition is larger than 1.0 × 10(7) so that this step is highly exergonic. We argue that this finding is consistent with current knowledge of the energetics of the S0 to S4 reactions, and that the high exergonicity is required for the kinetic efficiency of PSII.