Activating anions that replace Cl- in the O-2-evolving complex of photosystem II slow the kinetics of the terminal step in water oxidation and destabilize the S-2 and S-3 states

Photosystem II, the multisubunit protein complex that oxidizes water to O-2 , requires the inorganic cofactors Ca2+ and Cl- to exhibit optimal activity . Chloride can be replaced functionally by a small number of anionic cofact ors (Br-, NO3-, NO2-, I-), but among these anions, only Br- is capable of r estoring rates of oxygen evolution comparable to those observed with Cl-. U V absorption difference spectroscopy was utilized in the experiments descri bed here as a probe to monitor donor side reactions in photosystem II in th e presence of Cl- or surrogate anions. The rate of the final step of the wa ter oxidation cycle was found to depend on the activating anion bound at th e Cl- site, but the kinetics of this step did not limit the light-saturated rate of oxygen evolution. Instead, the lower oxygen evolution rates suppor ted by surrogate anions appeared to be correlated with an instability of th e higher oxidation states of the oxygen-evolving complex that was induced b y addition of these anions. Reduction of these states takes place not only with I- but also with NO2- and to a lesser extent even with NO3- and Br- an d is not related to the ability of these anions to bind at the Cl- binding site. Rather, it appears that these anions can attack higher oxidation stat es of the oxygen evolving complex from a second site that is not shielded b y the extrinsic 17 and 23 kDa polypeptides and cause a one-electron reducti on. The decrease of the oxygen evolution rate may result from accumulated d amage to the reaction center protein by the one-electron oxidation product of the anion.