Structure of the cytochrome b6f complex: new prosthetic groups, Q-space, and the ‘hors d’oeuvres hypothesis’ for assembly of the complex

William A. Cramer, Jiusheng Yan, Huamin Zhang, Genji Kurisu, Janet L. Smith

3-A crystal structures of the cytochrome b6f complex have provided a structural framework for the photosynthetic electron transport chain. The structures of the 220,000 molecular weight dimeric cytochrome b6f complex from the thermophilic cyanobacterium, Mastigocladis laminosus (Kurisu et al. 2003, Science 302: 1009-1014), and the green alga, Chlamydomonas reinhardtii (Stroebel et al. 2003, Nature 426: 413-418), are very similar. The latter is the first structure of a integral membrane photosynthetic electron transport complex from a eukaryotic source. The M. laminosus and C. reinhardtii structures have provided structural information and experimental insights to the properties and functions of three native and novel prosthetic groups, a chlorophyll a, a beta-carotene, and a unique heme x, one copy of which is found in each monomer of the cytochrome b6f complex, but not the cytochrome bc1 complex from the mitochondrial respiratory chain of animals and yeast. Several functional insights have emerged from the structures including the function of the dimer; the properties of heme x; the function of the inter-monomer quinone-exchange cavity; a quinone diffusion pathway through relatively narrow crevices or portals; a modified reaction scheme for n-side quinone redox reactions; a necessarily novel mechanism for quenching of the bound chlorophyll triplet state; a possible role for the bound chlorophyll a in activation of the LHC kinase; and a structural and assembly role for the four small PetG, L, M, and N subunits. An 'hors d'oeuvres hypothesis' for assembly of the complex is proposed for the small 'hydrophobic stick' or 'picket fence' polypeptides at the periphery of the complex, based on the cis-positive orientation of the small hydrophobic subunits and the 'toothpick' binding mode of the beta-carotene.