Conservation of Lipid Binding Sites in Cytochrome bc Complexes1

Abstract

Cytochrome bc complexes present in the energy transducing membranes of respiration and photosynthesis share structural and functional homology. By comparing the ten lipid, detergent and pigment positions in the crystal structures of the dimeric photosynthetic cytochrome b6f complex from 2 cyanobacteria2,3 and an alga4, obtained in the presence of synthetic and natural lipids, with the 13 natural lipid and detergent positions in the yeast cytochrome bc1 dimer5, an extensive conservation of lipid sites has been deduced. Seven lipid and detergent sites in the cyanobacterial b6f complex overlap three natural lipid sites in the algal complex, and four sites in the respiratory bc1 complex. The lipids occupying these sites differ between b6f and bc1: the crystal structures of b6f2-4 contain natural sulfolipid and monogalactosyldiacylglycerol, and synthetic phosphatidylcholine whereas the respiratory bc1 complex5 contains cardiolipin, phosphatidic acid and phosphatidyl-ethanolamine. Phosphatidyl-glycerol and digalactosyldiacylglycerol have been identified in the b6f complex by mass spectrometry. The lipid-like chlorophyll-a, β-carotene and eicosane are unique to b6f. Based on structural superposition of b6f and bc1, sequence conservation, analyses of inter-molecular distances, and amino acid and lipid B-factors, the following lipid functions are inferred in b6f: (i) substitution of bc1 trans-membrane helix (TMH) H by a lipid and chlorophyll chlorin ring in b6f; (ii) lipid and β-carotene mediated connection of trans-membrane peripheral and core domains; (iii) stabilization of the iron-sulfur protein TMH, perhaps relevant to catalytic domain motion; (iv) n-side charge and polarity compensation; (v) β-carotene-mediated super-complex with photosystem I reaction center complex. A physiological function for conserved Pet G and N6 subunits is proposed. 1Hasan et al., JMB (in press); 2Yamshita et al., JMB 2007; 3Baniulis et al., JBC 2009; 4Stroebel et al., Nature 2003; 5Solmaz and Hunte, JBC 2008; 6Schneider et al., Res. Microb. 2007; Funding:NIH-GM038323