Abstract
We propose a scheme for the origin of mitochondria based on phylogenetic reconstructions with more than 400 yeast nuclear genes that encode mitochondrial proteins. Half of the yeast mitochondrial proteins have no discernable bacterial homologues, while one-tenth are unequivocally of α-proteobacterial origin. These data suggest that the majority of genes encoding yeast mitochondrial proteins are descendants of two different genomic lineages that have evolved in different modes. First, the ancestral free-living α-proteobacterium evolved into an endosymbiont of an anaerobic host. Most of the ancestral bacterial genes were lost, but a small fraction of genes supporting bioenergetic and translational processes were retained and eventually transferred to what became the host nuclear genome. In a second, parallel mode, a larger number of novel mitochondrial genes were recruited from the nuclear genome to complement the remaining genes from the bacterial ancestor. These eukaryotic genes, which are primarily involved in transport and regulatory functions, transformed the endosymbiont into an ATP-exporting organelle.
Highlights
The endosymbiotic theory for the origin of mitochondria implies in its simplest form that the mitochondrial proteins are encoded by genes that have descended from an ancestral a-proteobacterium (Gray, 1992)
Phylogenetic reconstructions based on rRNA, ribosomal proteins, heat shock proteins, NADH dehydrogenase subunits, cytochrome oxidase and cytochrome b reveal a close evolutionary relationship between mitochondria and aerobic a-proteobacteria (Olsen et al, 1994; Viale and Arakaki, 1994; Andersson et al, 1998; Sicheritz-Ponten et al, 1998; Gray et al, 1999)
The most parsimonious interpretation of these results is that both Rickettsia and mitochondria arose from an ancestral a-proteobacterium that had the capacity for oxidative phosphorylation, in accordance with an important prediction of the endosymbiotic theory
Summary
The endosymbiotic theory for the origin of mitochondria implies in its simplest form that the mitochondrial proteins are encoded by genes that have descended from an ancestral a-proteobacterium (Gray, 1992). Almost all of the genes encoding the proteins of modern mitochondria are found in the nuclear genomes of their host cells (Gray et al, 1999). Our initial comparisons of coding sequences from the Rickettsia genome with nuclear homologues encoding mitochondrial proteins in Saccharomyces cerevisiae provided indications of a more complex evolutionary scenario (Andersson et al, 1998). We ®nd that more than half of the proteins of the yeast mitochondrial proteome have no counterparts in bacteria Phylogenetic reconstructions of these proteins produce coherent clusters of purely eukaryotic homologues. The phylogenetic trees are available underother resources' in the Comparative and Functional Genomics HomePage (a section of Yeast) at http://www.interscience.wiley.com
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