Effects of Sr2+-substitution on the reduction rates of Yz* in PSII membranes--evidence for concerted hydrogen-atom transfer in oxygen evolution.

Several groups have recently investigated the kinetic effects of biochemical treatments, site-directed mutagenesis, or substitution of essential cofactors on the stepwise, water-oxidizing chemistry catalyzed by Photosystem II. Consistently, these studies show evidence for a slowing of the final, oxygen-releasing step, S(3) --> S(0), of the catalytic cycle. To a degree, some of this work also shows a slowing of the earlier S-state transitions. To study these processes in more detail, we have investigated the effect of replacing Ca(2+) with Sr(2+)on the rates of the S-state transitions by using time-resolved electron paramagnetic resonance. The results show a slowdown of the last transition in the cycle, consistent with a report from Boussac et al. [Boussac, A., Sétif, P., and Rutherford, A. W. (1992) Biochemistry 31, 1224-1234], and of the earlier S-state transitions as well, which suggests that a common molecular mechanism is at work and that Sr(2+) is less effective than Ca(2+) in supporting it. While the oxidation of Y(z) by P(680)(+) has been extensively studied and can be understood within the context of nonadiabatic electron tunneling combined with rapid, non-rate-limiting proton transfer in the holo-system [Tommos, C., and Babcock, G. T. (2000) Biochim. Biophys. Acta 1458, 199], the reduction of Y(z*) by the Mn cluster cannot be described effectively by a nonadiabatic electron-transfer formalism. This indicates that this reaction is rate limited by processes other than electron tunneling. We discuss our results for Y(z*) reduction and those of others for the activation parameters (E(a), A, KIE, and rates) associated with this process, in terms of both sequential and concerted proton-coupled, electron transfer. Our analysis indicates that concerted hydrogen-atom transfer processes best explain the observed characteristics of the S-state advances.