Electron, proton and hydrogen-atom transfers in photosynthetic water oxidation

When photosynthetic organisms developed so that they could use water as an electron source to reduce carbon dioxide, the stage was set for efficient proliferation. Algae and plants spread globally and provided the foundation for our atmosphere and for O₂-based chemistry in biological systems. Light-driven water oxidation is catalysed by photosystem II, the active site of which contains a redox-active tyrosine denoted Y_Z, a tetramanganese cluster, calcium and chloride. In 1995, Gerald Babcock and co-workers presented the hypothesis that photosynthetic water oxidation occurs as a metallo-radical catalysed process. In this model, the oxidized tyrosine radical is generated by coupled proton/electron transfer and re-reduced by abstracting hydrogen atoms from substrate water or hydroxide-ligated to the manganese cluster. The proposed function of Y_Z requires proton transfer from the tyrosine site upon oxidation. The oxidation mechanism of Y_Z in an inhibited and O₂-evolving photosystem II is discussed. Domino-deprotonation from Y_Z to the bulk solution is shown to be consistent with a variety of data obtained on metal-depleted samples. Experimental data that suggest that the oxidation of Y_Z in O₂-evolving samples is coupled to proton transfer in a hydrogen-bonding network are described. Finally, a dielectric-dependent model for the proton release that is associated with the catalytic cycle of photosystem II is discussed.