Spin-lattice relaxation of coupled metal-radical spin-dimers in proteins:: Application to Fe2+-cofactor (QA, QB, φ) dimers in reaction centers from photosynthetic bacteria

The spin-lattice relaxation times (T-1) for the reduced quinone acceptors Q(A)(radical anion) and Q(B)(radical anion) and the intermediate pheophytin acceptor phi(radical anion), were measured in native photosynthetic reaction centers (RC) containing a high spin Fe2+ (S = 2) and in RCs in which Fe2+ was replaced by diamagnetic Zn2+. From these data, the contribution of the Fe2+ to the spin-lattice relaxation of the cofactors was determined. To relate the spin-lattice relaxation rate to the spin-spin interaction between the Fe2+ and the cofactors, we developed a spin-dimer model that takes into account the zero field splitting and the rhombicity of the Fe2+ ion. The relaxation mechanism of the spin-dimer involves a two-phonon process that couples the fast relaxing Fe2+ spin to the cofactor spin. The process is analogous to the one proposed by R. Orbach (Proc. P. 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 dinners studied in this work the exchange interaction, J(o), is predominant. The values of J(o) for Q(A)(radical anion)Fe(2+), Q(B)(radical anion)Fe(2+), and phi(radical anion)Fe(2+) were determined to be (in kelvin) -0.58, -0.92, and -1.3 x 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(-beta(J)d), where d is the distance between cofactor spins and beta(J) had a value of (0.66-0.86) Angstrom(-1). The relation between J(o) and the matrix element \V-ij\(2) involved in electron transfer rates is discussed.