From manganese oxidation to water oxidation: assembly and evolution of the water-splitting complex in photosystem II

The manganese cluster of photosystem II has been the focus of intense research aiming to understand the mechanism of H₂O-oxidation. Great effort has also been applied to investigating its oxidative photoassembly process, termed photoactivation that involves the light-driven incorporation of metal ions into the active Mn₄CaO₅ cluster. The knowledge gained on these topics has fundamental scientific significance, but may also provide the blueprints for the development of biomimetic devices capable of splitting water for solar energy applications. Accordingly, synthetic chemical approaches inspired by the native Mn cluster are actively being explored, for which the native catalyst is a useful benchmark. For both the natural and artificial catalysts, the assembly process of incorporating Mn ions into catalytically active Mn oxide complexes is an oxidative process. In both cases this process appears to share certain chemical features, such as producing an optimal fraction of open coordination sites on the metals to facilitate the binding of substrate water, as well as the involvement of alkali metals (e.g., Ca²⁺) to facilitate assembly and activate water-splitting catalysis. This review discusses the structure and formation of the metal cluster of the PSII H₂O-oxidizing complex in the context of what is known about the formation and chemical properties of different Mn oxides. Additionally, the evolutionary origin of the Mn₄CaO₅ is considered in light of hypotheses that soluble Mn²⁺ was an ancient source of reductant for some early photosynthetic reaction centers ('photomanganotrophy'), and recent evidence that PSII can form Mn oxides with structural resemblance to the geologically abundant birnessite class of minerals. A new functional role for Ca²⁺ to facilitate sustained Mn²⁺ oxidation during photomanganotrophy is proposed, which may explain proposed physiological intermediates during the likely evolutionary transition from anoxygenic to oxygenic photosynthesis.