Biological identity and diversity in photosynthesis and respiration: structure of the lumen-side domain of the chloroplast Rieske protein.

Abstract

The cytochrome b6f complex functions in oxygenic photosynthesis as an integral membrane protein complex that mediates coupled electron transfer and proton translocation. The Rieske [2Fe-2S] protein subunit of the complex functions at the electropositive (p) membrane interface as the electron acceptor for plastoquinol and donor for the cytochrome f subunit, and may have a dynamic role in catalyzing electron and proton transfer at the membrane interface. There are significant structure/function similarities to the cytochrome bc1 complex of the respiratory chain. The 1.83 A crystal structure of a 139-residue C-terminal fragment of the Rieske [2Fe-2S] protein, derived from the cytochrome b6f complex of spinach chloroplasts, has been solved by multiwavelength anomalous diffraction. The structure of the fragment comprises two domains: a small 'cluster-binding' subdomain and a large subdomain. The [2Fe-2S] cluster-binding subdomains of the chloroplast and mitochondrial Rieske proteins are virtually identical, whereas the large subdomains are strikingly different despite a common folding topology. A structure-based sequence alignment of the b6f and bc1 groups of Rieske soluble domains is presented. The segregation of structural conservation and divergence in the cluster-binding and large subdomains of the Rieske protein correlates with the overall relatedness of the cytochrome b6f and bc1 complexes, in which redox domains in the aqueous p phase are dissimilar and those within the membrane are similar. Distinct sequences and surface charge distributions among Rieske large subdomains may provide a signature for interaction with the p-side oxidant protein and for the pH of the intraorganelle compartment.