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Mol. Biol. Evol. 21(9):1643-1660. 2004
DOI: 10.1093/molbev/msh160
© 2004 by the Society for Molecular Biology and Evolution. ISSN: 0737-4038

A Genome Phylogeny for Mitochondria Among {alpha}-Proteobacteria and a Predominantly Eubacterial Ancestry of Yeast Nuclear Genes

Christian Esser*, Nahal Ahmadinejad*, Christian Wiegand*, Carmen Rotte*, Federico Sebastiani*, Gabriel Gelius-Dietrich*, Katrin Henze*, Ernst Kretschmann{dagger}, Erik Richly{ddagger}, Dario Leister{ddagger}, David Bryant§, Michael A. Steel||, Peter J. Lockhart, David Penny and William Martin*,1

* Institute of Botany III, University of Düsseldorf, Düsseldorf, Germany
{dagger} European Bioinformatics Institute, Hinxton, Cambridge, United Kingdom
{ddagger} Max-Planck Institut für Züchtungsforschung, Köln, Germany
§ McGill Centre for Bioinformatics, Montréal, Québec, Canada
||Department of Mathematics and Statistics, University of Canterbury, Christchurch, New Zealand
Allan Wilson Centre for Molecular Ecology and Evolution, Massey University, Palmerston North, New Zealand

1 E-mail: w.martin{at}uni-duesseldorf.de.

Analyses of 55 individual and 31 concatenated protein data sets encoded in Reclinomonas americana and Marchantia polymorpha mitochondrial genomes revealed that current methods for constructing phylogenetic trees are insufficiently sensitive (or artifact-insensitive) to ascertain the sister of mitochondria among the current sample of eight {alpha}-proteobacterial genomes using mitochondrially-encoded proteins. However, Rhodospirillum rubrum came as close to mitochondria as any {alpha}-proteobacterium investigated. This prompted a search for methods to directly compare eukaryotic genomes to their prokaryotic counterparts to investigate the origin of the mitochondrion and its host from the standpoint of nuclear genes. We examined pairwise amino acid sequence identity in comparisons of 6,214 nuclear protein-coding genes from Saccharomyces cerevisiae to 177,117 proteins encoded in sequenced genomes from 45 eubacteria and 15 archaebacteria. The results reveal that ~75% of yeast genes having homologues among the present prokaryotic sample share greater amino acid sequence identity to eubacterial than to archaebacterial homologues. At high stringency comparisons, only the eubacterial component of the yeast genome is detectable. Our findings indicate that at the levels of overall amino acid sequence identity and gene content, yeast shares a sister-group relationship with eubacteria, not with archaebacteria, in contrast to the current phylogenetic paradigm based on ribosomal RNA. Among eubacteria and archaebacteria, proteobacterial and methanogen genomes, respectively, shared more similarity with the yeast genome than other prokaryotic genomes surveyed.

Key Words: Endosymbiosis • Genome analysis • mitochondria • origin of eukaryotes • archaebacteria • eubacteria


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