Role of D1-His190 in the proton-coupled oxidation of tyrosine YZ in manganese-depleted photosystem II

TO further characterize the role of D1-His190 in the oxidation of tyrosine Y-Z in photosystem II, the pH dependence of P-680(.+) reduction was measured in H190A and Mn-depleted wild-type* PSII particles isolated from the cyanobacterium, Synechocystis sp. PCC 6803. Measurements were conducted in the presence and absence of imidazole and other small organic bases. In H190A PSII particles, rapid reduction of P-680(.+) attributed to electron transfer from Y-Z increased dramatically above pH 9, with an apparent pK(A) of similar to 10.3. In the presence of ethanolamine and imidazole, this dramatic increase occurred at lower pH values, with the efficiency of YZ oxidation correlating with the solution pK(A) value of the added base. We conclude that the pK(A) of Y-Z is similar to 10.3 in D1-H190A PSII particles. In Mn-depleted wild type* PSII particles, P-680(.+) reduction was accelerated by all exogenous bases examined (substituted imidazoles, histidine, Tris, and 1,4-diazabicyclo[2.2.2] octane). We conclude that Y-Z is solvent accessible in Mn-depleted wild-type* PSII particles and that its pK(A) is near that of tyrosine in solution. In Mn-depleted wild-type* PSII particles, over 80% of the kinetics of P680.+ reduction after a flash could be described by three kinetic components. The individual rate constants of these components varied slightly with pH, but their relative proportions varied dramatically with pH, showing apparent pK(A) values of 7.5 and 6.25 (6.9 and 5.8 in the presence of Ca2+ and Mg2+ ions). An additional pKA value (pK(A) < 4.5) may also be present. To describe these data, we propose (1) the pKA of His190 is 6.9-7.5, depending on buffer ions, (2) the deprotonation of Y-Z is facilitated by the transient formation of a either a hydrogen bond or a hydrogen-bonded water bridge between Y-Z and D1-His190, and (3) when protonated, D1-His190 interacts with nearby residues having pK(A) values near 6 and 4. Because Y-Z and D1-His190 are located near the Mn cluster, these residues may interact with the Mn cluster in the intact system.