Traffic within the Cytochrome b6f Lipoprotein Complex: Gating of the Quinone Portal

The cytochrome bc complexes b(6)f and bc(1) catalyze proton-coupled quinol/quinone redox reactions to generate a transmembrane proton electrochemical gradient. Quinol oxidation on the electrochemically positive (p) interface of the complex occurs at the end of a narrow quinol/quinone entry/exit Q(p) portal, 11 angstrom long in bc complexes. Superoxide, which has multiple signaling functions, is a by-product of the p-side quinol oxidation. Although the transmembrane core and the chemistry of quinone redox reactions are conserved in bc complexes, the rate of superoxide generation is an order of magnitude greater in the b(6)f complex, implying that functionally significant differences in structure exist between the b(6)f and bc(1) complexes on the p-side. A unique structure feature of the b(6)f p-side quinol oxidation site is the presence of a single chlorophyll-a molecule whose function is unrelated to light harvesting. This study describes a cocrystal structure of the cytochrome b(6)f complex with the quinol analog stigmatellin, which partitions in the Q(p) portal of the bc(1) complex, but not effectively in b(6)f. It is inferred that the Q(p) portal is partially occluded in the b(6)f complex relative to bc(1). Based on a discrete molecular-dynamics analysis, occlusion of the Q(p) portal is attributed to the presence of the chlorophyll phytyl tail, which increases the quinone residence time within the Q(p) portal and is inferred to be a cause of enhanced superoxide production. This study attributes a novel (to our knowledge), structure-linked function to the otherwise enigmatic chlorophyll-a in the b(6)f complex, which may also be relevant to intracellular redox signaling.