Evolution of cytochrome bc complexes: From membrane-anchored dehydrogenases of ancient bacteria to triggers of apoptosis in vertebrates

Abstract

This review traces the evolution of the cytochrome bc complexes from their early spread among prokaryotic lineages and up to the mitochondrial cytochrome bc1 complex (complex III) and its role in apoptosis. The results of phylogenomic analysis suggest that the bacterial cytochrome b6f-type complexes with short cytochromes b were the ancient form that preceded in evolution the cytochrome bc1-type complexes with long cytochromes b. The common ancestor of the b6f-type and the bc1-type complexes probably resembled the b6f-type complexes found in Heliobacteriaceae and in some Planctomycetes. Lateral transfers of cytochrome bc operons could account for the several instances of acquisition of different types of bacterial cytochrome bc complexes by archaea. The gradual oxygenation of the atmosphere could be the key evolutionary factor that has driven further divergence and spread of the cytochrome bc complexes. On one hand, oxygen could be used as a very efficient terminal electron acceptor. On the other hand, auto-oxidation of the components of the bc complex results in the generation of reactive oxygen species (ROS), which necessitated diverse adaptations of the b6f-type and bc1-type complexes, as well as other, functionally coupled proteins. A detailed scenario of the gradual involvement of the cardiolipin-containing mitochondrial cytochrome bc1 complex into the intrinsic apoptotic pathway is proposed, where the functioning of the complex as an apoptotic trigger is viewed as a way to accelerate the elimination of the cells with irreparably damaged, ROS-producing mitochondria.

Evolution of b-type cytochromes in prokaryotes

“…About 75% of the "A" group of sequences correspond to a split cytochrome b 6 (marked with a red asterisk at the corresponding nodes), where petD encodes the C-terminal subunit 4; in these cases petB and petD sequences were concatenated before the multiple alignment and phylogenetic analysis. There is, however, not significant bootstrap support for grouping all the split cytochromes together, and thus inferring an early origin of the split cytochrome b 6 from which the fused cytochrome-b of the bc complex evolved, as suggested previously (Dibrova et al, 2013). Our results are in agreement with studies which have suggested that the split between the N-and C-terminal regions of cytochrome b 6 occurred several times independently in different clades (Baymann et al, 2012, Kao andHunte, 2014).…”

“…However, other researchers have refuted this conclusion, again based on expanded phylogenies, suggesting an early origin for a b 6 f-type complex, and later fusions and HGT to form the present picture of distribution of these enzymes (Dibrova et al, 2013). Recent evidence from genomic data showing the presence of multiple Rieske/cytb proteins in many species further complicates the picture (Dibrova et al, 2013.…”

“…Previous analyses (Lebrun et al, 2006, Dibrova et al, 2013, Kao and Hunte, 2014 Table 1). The presence of these pfam domains indicates homology, so we included all sequences from the orthology groups previously analyzed, but also added the additional three orthology groups for completeness.…”

“…Previous analyses (Schutz et al, 2000, Lebrun et al, 2006, Nitschke et al, 2010, Dibrova et al, 2013 have attempted to derive a complete phylogeny of cytochrome-b from a diverse set of prokaryotes, but they mostly focus on the comparison of cytochrome b 6 of the b 6 f complex of photosynthesis and the cytochrome bc complex of respiration. Also, in those analyses only some cytochromeb domain containing proteins were included while some other were excluded; this might skew the results, and thus the conclusions.…”

“…Removal of the K00241 sequences (dataset cytb.R2 comprising 472 sequences total) improved the resolution, so that most orthology groups appeared tightly clustered, albeit not with significant bootstrap support ( Figure S1). Dataset cytABCD.R7 (section 3.2) was analyzed to better resolve questions raised by previous analyses (Lebrun et al, 2006, Dibrova et al, 2013 on the evolution of cytochrome b 6 . Dataset cytBHL.R9 was used to address the relationships of more distant cytochrome-b types (section 3.3); it includes the b-type cytochromes of the bc complex (K00412: CYTB and K00410: fbch), the formate dehydrogenase (K00127) and the Ni/Fe dehydrogenase (K03620).…”