Emergence of cytochrome bc complexes in the context of photosynthesis

Abstract

The cytochrome bc (cyt bc) complexes are involved in Q-cycling; they oxidize membrane quinols by high-potential electron acceptors, such as cytochromes or plastocyanin, and generate transmembrane proton gradient. In several prokaryotic lineages, and also in plant chloroplasts, the catalytic core of the cyt bc complexes is built of a four-helical cytochrome bc (cyt b) that contains three hemes, a three-helical subunit IV, and an iron-sulfur Rieske protein (cytochrome b(6)f-type complexes). In other prokaryotic lineages, and also in mitochondria, the cyt b subunit is fused with subunit IV, yielding a sevenor eight-helical cyt b with only two hemes (cyt bc1-type complexes). Here we present an updated phylogenomic analysis of the cyt b subunits of cyt bc complexes. This analysis provides further support to our earlier suggestion that (1) the ancestral version of cyt bc complex contained a small four-helical cyt b with three hemes similar to the plant cytochrome b(6) and (2) independent fusion events led to the formation of large cyts b in several lineages. In the search for a primordial function for the ancestral cyt bc complex, we address the intimate connection between the cyt bc complexes and photosynthesis. Indeed, the Q-cycle turnover in the cyt bc complexes demands high-potential electron acceptors. Before the Great Oxygenation Event, the biosphere had been highly reduced, so high-potential electron acceptors could only be generated upon light-driven charge separation. It appears that an ancestral cyt bc complex capable of Q-cycling has emerged in conjunction with the (bacterio) chlorophyll-based photosynthetic systems that continuously generated electron vacancies at the oxidized (bacterio) chlorophyll molecules.