From Endosymbiont to Host-Controlled Organelle: The Hijacking of Mitochondrial Protein Synthesis and Metabolism

Mitochondria are eukaryotic organelles that originated from the endosymbiosis of an alpha-proteobacterium. To gain insight into the evolution of the mitochondrial proteome as it proceeded through the transition from a free-living cell to a specialized organelle, we compared a reconstructed ancestral proteome of the mitochondrion with the proteomes of alpha-proteobacteria as well as with the mitochondrial proteomes in yeast and man. Overall, there has been a large turnover of the mitochondrial proteome during the evolution of mitochondria. Early in the evolution of the mitochondrion, proteins involved in cell envelope synthesis have virtually disappeared, whereas proteins involved in replication, transcription, cell division, transport, regulation, and signal transduction have been replaced by eukaryotic proteins. More than half of what remains from the mitochondrial ancestor in modern mitochondria corresponds to translation, including post-translational modifications, and to metabolic pathways that are directly, or indirectly, involved in energy conversion. Altogether, the results indicate that the eukaryotic host has hijacked the proto-mitochondrion, taking control of its protein synthesis and metabolism.

[1]  M S Waterman,et al.  Identification of common molecular subsequences. , 1981, Journal of molecular biology.

[2]  M. Denis-Duphil.  Pyrimidine biosynthesis in Saccharomyces cerevisiae: the ura2 cluster gene, its multifunctional enzyme product, and other structural or regulatory genes involved in de novo UMP synthesis. , 1989, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[3]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[4]  W. Miller.  Mitochondrial specificity of the early steps in steroidogenesis , 1995, The Journal of Steroid Biochemistry and Molecular Biology.

[5]  D. Sankoff,et al.  An ancestral mitochondrial DNA resembling a eubacterial genome in miniature , 1997, Nature.

[6]  P. Kiberstis.  Mitochondria Make A Comeback , 1999, Science.

[7]  Hiroyuki Ogata,et al.  KEGG: Kyoto Encyclopedia of Genes and Genomes , 1999, Nucleic Acids Res..

[8]  P. Bork,et al.  Variation and evolution of the citric-acid cycle: a genomic perspective. , 1999, Trends in microbiology.

[9]  Michael Y. Galperin,et al.  Comparative genomics of the Archaea (Euryarchaeota): evolution of conserved protein families, the stable core, and the variable shell. , 1999, Genome research.

[10]  B. Lang,et al.  Mitochondrial evolution. , 1999, Science.

[11]  Michael Y. Galperin,et al.  The COG database: a tool for genome-scale analysis of protein functions and evolution , 2000, Nucleic Acids Res..

[12]  S. Salzberg,et al.  Genome sequences of Chlamydia trachomatis MoPn and Chlamydia pneumoniae AR39. , 2000, Nucleic acids research.

[13]  C. Kurland,et al.  Origin and Evolution of the Mitochondrial Proteome , 2000, Microbiology and Molecular Biology Reviews.

[14]  C. Kurland,et al.  The Dual Origin of the Yeast Mitochondrial Proteome , 2000, Yeast.

[15]  B. Lang,et al.  The origin and early evolution of mitochondria , 2001, Genome Biology.

[16]  I. Scheffler,et al.  Mitochondria make a come back. , 2001, Advanced drug delivery reviews.

[17]  Michael Y. Galperin,et al.  The COG database: new developments in phylogenetic classification of proteins from complete genomes , 2001, Nucleic Acids Res..

[18]  W. Martin,et al.  Evolution of the enzymes of the citric acid cycle and the glyoxylate cycle of higher plants. A case study of endosymbiotic gene transfer. , 2002, European journal of biochemistry.

[19]  C. Kurland,et al.  The global phylogeny of glycolytic enzymes , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Ronald W. Davis,et al.  Systematic screen for human disease genes in yeast , 2002, Nature Genetics.

[21]  Bradford W. Gibson,et al.  Characterization of the human heart mitochondrial proteome , 2003, Nature Biotechnology.

[22]  T. Kuwana,et al.  Bcl-2-family proteins and the role of mitochondria in apoptosis. , 2003, Current opinion in cell biology.

[23]  L. Ijlst,et al.  Fatty acid metabolism in Saccharomyces cerevisiae , 2003, Cellular and Molecular Life Sciences CMLS.

[24]  Steven W. Taylor,et al.  Global organellar proteomics. , 2003, Trends in biotechnology.

[25]  J. Nunnari,et al.  The Division of Endosymbiotic Organelles , 2003, Science.

[26]  Albert Sickmann,et al.  The proteome of Saccharomyces cerevisiae mitochondria , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Marjan S. Bolouri,et al.  Integrated Analysis of Protein Composition, Tissue Diversity, and Gene Regulation in Mouse Mitochondria , 2003, Cell.

[28]  J. Herrmann.  Converting bacteria to organelles: evolution of mitochondrial protein sorting. , 2003, Trends in microbiology.

[29]  Darren A. Natale,et al.  The COG database: an updated version includes eukaryotes , 2003, BMC Bioinformatics.

[30]  Toni Gabaldón,et al.  Reconstruction of the Proto-Mitochondrial Metabolism , 2003, Science.

[31]  A. Millar,et al.  What makes a mitochondrion? , 2003, Genome Biology.

[32]  S. Berry.  Endosymbiosis and the design of eukaryotic electron transport. , 2003, Biochimica et biophysica acta.

[33]  O. Gascuel,et al.  A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. , 2003, Systematic biology.

[34]  C. Kurland,et al.  On the origin of mitochondria: a genomics perspective. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[35]  M. Fujita,et al.  Proteomics of the rice cell: systematic identification of the protein populations in subcellular compartments , 2004, Molecular Genetics and Genomics.

[36]  Eoin Fahy,et al.  MitoProteome: mitochondrial protein sequence database and annotation system , 2004, Nucleic Acids Res..

[37]  P. Beech,et al.  Diverse eukaryotes have retained mitochondrial homologues of the bacterial division protein FtsZ. , 2004, Protist.

[38]  Robert C. Edgar,et al.  MUSCLE: a multiple sequence alignment method with reduced time and space complexity , 2004, BMC Bioinformatics.

[39]  M. Huynen,et al.  Shaping the mitochondrial proteome. , 2004, Biochimica et biophysica acta.

[40]  Kara Dolinski,et al.  Saccharomyces Genome Database (SGD) provides tools to identify and analyze sequences from Saccharomyces cerevisiae and related sequences from other organisms , 2004, Nucleic Acids Res..

[41]  Eoin Fahy,et al.  Identification of protein associations in organelles, using mass spectrometry-based proteomics. , 2004, Mass spectrometry reviews.

[42]  N. Pfanner,et al.  The protein import machinery of mitochondria , 2007 .

[43]  R. Lill,et al.  Iron-sulfur-protein biogenesis in eukaryotes. , 2005, Trends in biochemical sciences.

[44]  M. Huynen,et al.  Tracing the evolution of a large protein complex in the eukaryotes, NADH:ubiquinone oxidoreductase (Complex I). , 2005, Journal of molecular biology.

[45]  T. Lithgow,et al.  Evolution of the Molecular Machines for Protein Import into Mitochondria , 2006, Science.

[46]  Joaquín Dopazo,et al.  BABELOMICS: a systems biology perspective in the functional annotation of genome-scale experiments , 2006, Nucleic Acids Res..