Long-range electron spin-spin interactions in the bacterial photosynthetic reaction center

The electron spin-lattice relaxation behavior of the oxidized bacteriochlorophyll a dimer in reaction centers from Rhodobacter sphaeroides has been examined by the method of saturation-recovery EPR over the temperature range 3.8 K ≤ T ≤ 22 K. Its spin-lattice relaxation is nonexponential due to an orientation-dependent dipolar interaction with the non-heme Fe(II) of the reaction center. The saturation-recovery EPR traces were fit by using an equation which models the recovery in terms of a sum of isotropic (scalar) and orientation-dependent (dipolar) rate constants. The center-to-center distance between the bacteriochlorophyll a dimer and the non-heme Fe(II) is 28 Å and it is found that the Heisenberg exchange interaction is too small to make a measurable contribution to the scalar relaxation rate of the oxidized bacteriochlorophyll a dimer. The scalar relaxation rates for the oxidized bacteriochlorophyll a dimer show a T¹ temperature dependence which differs significantly from that of model porphyrin radicals. It appears that the unusually rigid protein environment surrounding the bacteriochlorophyll a dimer produces a strong coupling between the spin transitions of the radical and the low-frequency vibrational modes of the lattice. The dipolar rate constants of the oxidized bacteriochlorophyll a dimer and those of the stable tyrosine radical, Y_D ^•, in Mn-depleted photosystem II show the same temperature dependence. This confirms the assignment of the non-heme Fe(II) as the source of relaxation enhancement for Y_D ^• in Mn-depleted photosystem II and shows that the spin relaxation properties of the non-heme Fe(II) species in the two proteins are very similar. Using the relative magnitudes of the dipolar rate constants in the two proteins and the distance between the bacteriochlorophyll a dimer and the non-heme Fe(II) in the bacterial reaction center, we calculate a Y_D ^•-Fe(II) distance of 37 ± 5 Å in photosystem II. This agrees well with the distance predicted from the structure of the bacterial reaction center.