Function of tyrosine Z in water oxidation by photosystem II: Electrostatical promotor instead of hydrogen abstractor

Abstract

Photosynthetic water oxidation by photosystem II is mediated by a Mn-4 cluster, a cofactor X still chemically ill-defined, and a tyrosine, Y-Z (D1-Tyr161). Before the final reaction with water proceeds to yield O-2 (transition S-4 --> S-0), two oxidizing equivalents are stored on Mn-4 (S-0 double right arrow S-1 double right arrow S-2), a third on X (S-2 double right arrow S-3), and a forth on Y-Z (S-3 double right arrow S-4). It has been proposed that Y-Z functions as a pure electron transmitter between Mn4X and P-680, or, more recently, that it acts as an abstractor of hydrogen from bound water. We scrutinized the coupling of electron and proton transfer during the oxidation of Y-Z in PSII core particles with intact or impaired oxygen-evolving capacity, The rates of electron transfer to P-680(+), of electrochromism, and of pH transients were determined as a function of the pH, the temperature, and the H/D ratio, In oxygen-evolving material, we found only evidence for electrostatically induced proton release from peripheral amino acid residues but not from Y-Z(ox) itself. The positive charge stayed near Y-Z(ox), and the rate of electron transfer was nearly independent of the pH. In core particles with an impaired Mn-4 cluster, on the other hand, the rate of the electron transfer became strictly dependent on the protonation state of a single base (pK approximate to 7). At pH <7, the rate of electron transfer revealed the same slow rate (t(1/2) approximate to 35 mu s) as that of proton release into the bulk. The deposition of a positive charge around Y-Z(ox) was no longer detected. A large H/D isotope effect (approximate to 2.5) on these rates was also indicative of a steering of electron abstraction by proton transfer. That Y-Z(ox) was deprotonated into the bulk in inactive but not in oxygen-evolving material argues against the proposed role of Y-Z(ox) as an acceptor of hydrogen from water. Instead, the positive charge in its vicinity may shift the equilibrium from bound water to bound peroxide upon S-3 double right arrow S-4 as a prerequisite for the formation of oxygen upon S-4 --> S-0.