Structure and Function of the Cytochrome c 2:Reaction Center Complex from Rhodobacter sphaeroides

Abstract

In purple non-sulfur photosynthetic bacteria, a c-type heme protein, cytochrome (Cyt) c2, serves as the electron donor to the reaction center (RC) which is the site of the initial photochemical electron transfer. The second order rate of electron transfer from Cyt c2 to the RC is diffusion limited and optimized to facilitate electron transfer through the photosynthetic apparatus. This review summarizes the X-ray crystal structure of the Cyt c2:RC complex from Rhodobacter (Rba.) sphaeroides and studies based on the structure that elucidate the molecular basis for the role of the complex in electron transfer. The structure of the complex shows the heme cofactor in van der Waals contact with the reaction center and in close proximity to the bacteriochlorophyll dimer, the primary electron donor. The binding interface region includes: a) a solvent-separated region with long-range electrostatic interactions between complementary charged residues on Cyt c2 and the RC which play a role in protein docking and binding, and b) a small central region with short-range interactions, including hydrophobic, hydrogen bonding, and a cation-$π$ interaction, which play a role in binding the Cyt in close contact to the RC surface to facilitate strong electronic coupling between cofactors for rapid inter-protein electron transfer. Both types of interactions contribute to the binding. However, the two types of interactions have markedly different effects on the electron transfer kinetics. The long-range electrostatic interactions change the second order rate constant by changing the association rate but not the electron transfer rate in the bound state. The short-range interactions do not affect the association rate but change the dissociation rate as well as the electron transfer rate in the bound state. The strength of the binding interactions is optimized to allow sufficiently fast dissociation of the oxidized Cyt c2 that does not limit the rate of cyclic electron transfer.