Effects of Sr2+-substitution on the reduction rates of Y-z(center dot) in PSII membranes - Evidence for concerted hydrogen-atom transfer in oxygen evolution

Several groups have recently investigated the kinetic effects of biochemica l treatments, site-directed mutagenesis, or substitution of essential cofac tors on the stepwise, water-oxidizing chemistry catalyzed by Photosystem II . Consistently, these studies show evidence for a slowing of the final, oxy gen-releasing step, S-3 (-->) S-0, of the catalytic cycle. To a degree, som e 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 re placing Ca2+ with Sr2+ on the rates of the S-state transitions by using tim e-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 effectiv e than Ca2+ in supporting it. While the oxidation of Y-z by P-680(+) has be en extensively studied and can be understood within the context of nonadiab atic electron tunneling combined with rapid, non-rate-limiting proton trans fer in the hole-system [Tommos, C., and Babcock, G. T. (2000) Biochim. Biop hys. Acta 1458, 199], the reduction of Y-z(.) by the Mn cluster cannot be d escribed effectively by a nonadiabatic electron-transfer formalism. This in dicates 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 thi s process, in terms of both sequential and concerted proton-coupled, electr on transfer. Our analysis indicates that concerted hydrogen-atom transfer p rocesses best explain the observed characteristics of the S-state advances.