The S2 State of the Oxygen-Evolving Complex of Photosystem II Explored by QM/MM Dynamics: Spin Surfaces and Metastable States Suggest a Reaction Path Towards the S3 State

摘要

One of the key steps in photosynthetic solar-energy conversion performed by plants, algae, and cyanobacteria is the splitting of water into molecular oxygen and hydrogen equivalents. To achieve this challenging task photosynthetic organisms use a protein complex that remained almost unchanged during the evolution in the last two and a half billion years: the photosystem II (PSII). The reaction proceeds by the accumulation of four oxidizing equivalents on the {Mn4CaO5} cluster through five (S0-S4) oxidation states that are sequentially attained during water splitting (Kok cycle). The deep understanding of the way nature has found to perform this difficult task efficiently has a great relevance not only for biology but also for inspiring the development of biomimetic artificial systems that can be used to store solar energy in an environmentally friendly way. Atomic details of the structure of the oxygen-evolving complex (OEC) of PSII have been revealed by extended X-ray absorption fine structure (EXAFS) experiments and by X-ray crystallography at increasing resolution levels.However, the accurate position of the {Mn4CaO5} cluster atoms and its ligands emerged only when a X-ray structure at 1.9 A resolution became accessible. However, the effect of a possible X-ray photo-reduction, in particular on the characterization of the Kok's state described by this structure and on the unrealistic bond lengths between the oxygen atom O5 and the two manganese ions Mnl and Mn4, is matter of debate. Additionally, important contributions to the structure refinement came from theoretical studies.