Structural models of the biological oxygen-evolving complex: achievements, insights, and challenges for biomimicry
The oxygen-evolving complex (OEC) in Photosystem II (PS-II) of oxygenic photosynthesis catalyzes the oxidation of water into dioxygen, protons and electrons, a reaction that underpins solar to chemical energy conversion in the biosphere. The inorganic core of the OEC is an oxo-bridged cluster that comprises four Mn and one Ca ions, Mn4CaO5. Deciphering the structure of this cluster and its immediate environment has been the aim of intense experimental efforts that span decades of research. The constantly improving structural definition of the OEC in the last fifteen years has offered opportunities to better understand its properties and function; it has also provided ever clearer and more well-defined targets for biomimetic synthetic chemistry. Here we present a critical overview of the most recent advances in molecular structural models of the OEC, focusing mostly on successful research efforts reported after the availability of atomically resolved crystallographic models of PS-II. We delineate the properties that have been targeted in biomimetic studies and analyze which structural aspects have by now been reproduced in synthetic systems. In combination with in-depth theoretical studies, the availability of novel synthetic structural analogues has led to considerable insight into structure–property correlations despite the lack of catalytic activity. Nevertheless, there are important features of the OEC that remain inaccessible to synthetic chemistry. Principal among them are the unique type of restricted structural flexibility and the highly structured and stable ligand sphere which enable the tightly controlled interplay of geometry, spin state and reactivity that is the hallmark of the OEC.