Bridge over troubled water: resolving the competing photosystem II crystal structures.

Density functional theory (DFT) calculations, at the Becke-Perdew/TZP level of theory, were used to investigate a set of CaMn(4)-containing clusters that model the active site of the water-oxidizing complex (WOC) of photosystem II (PSII). Metal-atom positions for three representative isomeric clusters of the formula [CaMn(4)C(9)N(2)O(16)H(10)](+)4 H(2)O are in good agreement with the disparate Mn(4) geometries of the three most recent X-ray crystal structures. Remarkably, interconversion between these three isomeric clusters is found to be facile, resulting from subtle changes in the coordination environment around the CaMn(4) centre. This result provides a clear rationalisation of the marked differences in reported crystal structures. Recent concerns have been raised regarding the opportunity for X-ray-damage-induced distortion of the metal-containing active centre during crystallographic analysis. Our calculations suggest that an even greater problem may be presented by the apparent fluxionality of the CaMn(4) skeleton within the active centre. Structural rearrangement may well precede crystallographic analysis, for example by the preferential "freezing-out" of one of several near-isoenergetic structures during the workup for crystallisation. This prospect, which our calculations cannot exclude, highlights the difficulties that will continue to be faced by experimentalists seeking unambiguous structural information on the WOC's active site.