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 Ca2+ with Sr2+ 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., Setif, 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 Sr2+ is less effective than Ca2+ 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 hole-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.