Spin-Lattice Relaxation of Coupled Metal-Radical Spin-Dimers in Proteins: Application to Fe 2+-Cofactor ( [formula omitted], [formula omitted], ϕ− ) Dimers in Reaction Centers from Photosynthetic Bacteria

Abstract

The spin-lattice relaxation times ( T 1) for the reduced quinone acceptors Q A − and Q B − , and the intermediate pheophytin acceptor ϕ − , were measured in native photosynthetic reaction centers (RC) containing a high spin Fe 2+ (S = 2) and in RCs in which Fe 2+ was replaced by diamagnetic Zn 2+. From these data, the contribution of the Fe 2+ to the spin-lattice relaxation of the cofactors was determined. To relate the spin-lattice relaxation rate to the spin-spin interaction between the Fe 2+ and the cofactors, we developed a spin-dimer model that takes into account the zero field splitting and the rhombicity of the Fe 2+ ion. The relaxation mechanism of the spin-dimer involves a two-phonon process that couples the fast relaxing Fe 2+ spin to the cofactor spin. The process is analogous to the one proposed by R. Orbach ( Proc. R. Soc. A. ( Lond.). 264:458–484) for rare earth ions. The spin-spin interactions are, in general, composed of exchange and dipolar contributions. For the spin dimers studied in this work the exchange interaction, J o, is predominant. The values of J o for Q A − Fe 2+, Q B − Fe 2+, and ϕ − Fe 2+ were determined to be (in kelvin) −0.58, −0.92, and −1.3 × 10 −3, respectively. The |J o| of the various cofactors (obtained in this work and those of others) could be fitted with the relation exp(− β J d), where d is the distance between cofactor spins and β J had a value of (0.66-0.86) Å −1. The relation between J o and the matrix element |V ij| 2 involved in electron transfer rates is discussed.