S-state dependence of the calcium requirement and binding characteristics in the oxygen-evolving complex of photosystem II

The functional role of the Call ion in the oxygen-evolving complex of photosystem II is not yet clear. Current models explain why the redox cycle of the complex would be interrupted after the S-3 state without Call, but the literature shows that it is interrupted after the S-2 state. Reinterpretation of the literature on methods of Call depletion [Miqyass, M., van Gorkom, H. J., and Yocum, C. F. (2007) Photosynth. Res. 92, 275-287] led us to propose that all S-state transit I ions require Call. Here we confirm that interpretation by measurements of flash-induced S-state transitions in UV absorbance. The results are explained by a cation exchange at the Call binding site that, in the absence of the extrinsic PsbP and PsbQ polypeptides, can occur in minutes in low S-states and in seconds in high S-states, depending on the concentration of the substituting cation. In the S-2(K+) or S-2(Na+) state a slow conformational change occurs that prevents recovery of the slow-exchange situation on return to a lower S-state but does not inhibit the S-state cycle in the presence of Ca2+. The ratio of binding affinities for monovalent vs divalent cations increases dramatically in the higher S-states. With the possible exception of S-0 to S-1, all S-state transitions specifically require Call, suggesting that Ca2+-bound H2O plays an essential role in a H+ transfer network required for H+-coupled electron transfer from the Mn cluster to tyrosine Z.