Reconstructing the evolution of the mitochondrial ribosomal proteome

For production of proteins that are encoded by the mitochondrial genome, mitochondria rely on their own mitochondrial translation system, with the mitoribosome as its central component. Using extensive homology searches, we have reconstructed the evolutionary history of the mitoribosomal proteome that is encoded by a diverse subset of eukaryotic genomes, revealing an ancestral ribosome of alpha-proteobacterial descent that more than doubled its protein content in most eukaryotic lineages. We observe large variations in the protein content of mitoribosomes between different eukaryotes, with mammalian mitoribosomes sharing only 74 and 43% of its proteins with yeast and Leishmania mitoribosomes, respectively. We detected many previously unidentified mitochondrial ribosomal proteins (MRPs) and found that several have increased in size compared to their bacterial ancestral counterparts by addition of functional domains. Several new MRPs have originated via duplication of existing MRPs as well as by recruitment from outside of the mitoribosomal proteome. Using sensitive profile–profile homology searches, we found hitherto undetected homology between bacterial and eukaryotic ribosomal proteins, as well as between fungal and mammalian ribosomal proteins, detecting two novel human MRPs. These newly detected MRPs constitute, along with evolutionary conserved MRPs, excellent new screening targets for human patients with unresolved mitochondrial oxidative phosphorylation disorders.

[1]  R. Agrawal,et al.  Proteomics and electron microscopic characterization of the unusual mitochondrial ribosome-related 45S complex in Leishmania tarentolae. , 2007, Molecular and biochemical parasitology.

[2]  D. Court,et al.  Importance of the 5 S rRNA-binding ribosomal proteins for cell viability and translation in Escherichia coli. , 2007, Journal of molecular biology.

[3]  Narmada Thanki,et al.  CDD: a conserved domain database for interactive domain family analysis , 2006, Nucleic Acids Res..

[4]  Christian von Mering,et al.  STRING 7—recent developments in the integration and prediction of protein interactions , 2006, Nucleic Acids Res..

[5]  G. Comi,et al.  Infantile encephalopathy and defective mitochondrial DNA translation in patients with mutations of mitochondrial elongation factors EFG1 and EFTu. , 2007, American journal of human genetics.

[6]  E. Shoubridge,et al.  Distinct clinical phenotypes associated with a mutation in the mitochondrial translation elongation factor EFTs. , 2006, American journal of human genetics.

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

[8]  R. Agrawal,et al.  Isolation and characterization of mitochondrial ribosomes and ribosomal subunits from Leishmania tarentolae. , 2006, Molecular and biochemical parasitology.

[9]  R. Gutell,et al.  A structural model for the large subunit of the mammalian mitochondrial ribosome. , 2006, Journal of molecular biology.

[10]  Martin Ott,et al.  Mba1, a membrane‐associated ribosome receptor in mitochondria , 2006, The EMBO journal.

[11]  Sean R. Collins,et al.  Global landscape of protein complexes in the yeast Saccharomyces cerevisiae , 2006, Nature.

[12]  Yuji Inagaki,et al.  Comprehensive multigene phylogenies of excavate protists reveal the evolutionary positions of "primitive" eukaryotes. , 2006, Molecular biology and evolution.

[13]  Laura C. Greaves,et al.  Mitochondrial DNA mutations in human disease , 2006, IUBMB life.

[14]  L. Bonen,et al.  Comparative analysis of bacterial-origin genes for plant mitochondrial ribosomal proteins. , 2006, Molecular biology and evolution.

[15]  Emmet A. O'Brien,et al.  GOBASE—a database of organelle and bacterial genome information , 2005, Nucleic Acids Res..

[16]  Robert D. Finn,et al.  Pfam: clans, web tools and services , 2005, Nucleic Acids Res..

[17]  Katsumi Isono,et al.  Identification and comparative analysis of the large subunit mitochondrial ribosomal proteins of Neurospora crassa. , 2006, FEMS microbiology letters.

[18]  Thomas J Naughton,et al.  Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified , 2006, BMC Evolutionary Biology.

[19]  S. Dimauro,et al.  hCOX18 and hCOX19: two human genes involved in cytochrome c oxidase assembly. , 2005, Biochemical and biophysical research communications.

[20]  T. W. O'brien,et al.  Nuclear MRP genes and mitochondrial disease. , 2005, Gene.

[21]  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.

[22]  Johannes Söding,et al.  Protein homology detection by HMM?CHMM comparison , 2005, Bioinform..

[23]  A. Coulson,et al.  Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans , 2005, Nature.

[24]  G. Rödel,et al.  Evidence for the association of yeast mitochondrial ribosomes with Cox11p, a protein required for the CuB site formation of cytochrome c oxidase , 2005, Current Genetics.

[25]  Joanna Towpik.  REGULATION OF MITOCHONDRIAL TRANSLATION IN YEAST , 2005 .

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

[27]  E. Shoubridge,et al.  Mutant mitochondrial elongation factor G1 and combined oxidative phosphorylation deficiency. , 2004, The New England journal of medicine.

[28]  Ann Saada,et al.  Defective mitochondrial translation caused by a ribosomal protein (MRPS16) mutation , 2004, Annals of neurology.

[29]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[30]  K. Isono,et al.  Cloning and analysis of the nuclear genes for two mitochondrial ribosomal proteins in yeast , 1989, Molecular and General Genetics MGG.

[31]  Rolf Apweiler,et al.  The Integr8 project - a resource for genomic and proteomic data , 2004, Silico Biol..

[32]  Cyrus Chothia,et al.  The SUPERFAMILY database in 2004: additions and improvements , 2004, Nucleic Acids Res..

[33]  S Blair Hedges,et al.  BMC Evolutionary Biology BioMed Central , 2003 .

[34]  R. Agrawal,et al.  Structure of the Mammalian Mitochondrial Ribosome Reveals an Expanded Functional Role for Its Component Proteins , 2003, Cell.

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

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

[37]  T. W. O'brien.  Properties of Human Mitochondrial Ribosomes , 2003, IUBMB life.

[38]  S. Dimauro,et al.  Mitochondrial respiratory-chain diseases. , 2003, The New England journal of medicine.

[39]  W. Neupert,et al.  Protein Insertion into the Inner Membrane of Mitochondria , 2002, IUBMB life.

[40]  Katsumi Isono,et al.  Tag-mediated isolation of yeast mitochondrial ribosome and mass spectrometric identification of its new components. , 2002, European journal of biochemistry.

[41]  A. Tzagoloff,et al.  Characterization of COX19, a Widely Distributed Gene Required for Expression of Mitochondrial Cytochrome Oxidase* , 2002, The Journal of Biological Chemistry.

[42]  E. Glaser,et al.  Probing the membrane topology of a subunit of the mitochondrial protein translocase, Tim44, with biotin maleimide. , 2002, Biochemical and biophysical research communications.

[43]  J. Palmer,et al.  Genes for Two Mitochondrial Ribosomal Proteins in Flowering Plants Are Derived from Their Chloroplast or Cytosolic Counterparts Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010483. , 2002, The Plant Cell Online.

[44]  L. Spremulli,et al.  The Large Subunit of the Mammalian Mitochondrial Ribosome , 2001, The Journal of Biological Chemistry.

[45]  E. Shoubridge.  Nuclear genetic defects of oxidative phosphorylation. , 2001, Human molecular genetics.

[46]  K Watanabe,et al.  Proteomic Analysis of the Mammalian Mitochondrial Ribosome , 2001, The Journal of Biological Chemistry.

[47]  K Watanabe,et al.  Structural Compensation for the Deficit of rRNA with Proteins in the Mammalian Mitochondrial Ribosome , 2001, The Journal of Biological Chemistry.

[48]  L. Spremulli,et al.  The Small Subunit of the Mammalian Mitochondrial Ribosome , 2001, The Journal of Biological Chemistry.

[49]  W. Neupert,et al.  Mba1, a Novel Component of the Mitochondrial Protein Export Machinery of the Yeast Saccharomyces cerevisiae , 2001, The Journal of cell biology.

[50]  M. Fromont-Racine,et al.  Identification of 12 New Yeast Mitochondrial Ribosomal Proteins Including 6 That Have No Prokaryotic Homologues* , 2001, The Journal of Biological Chemistry.

[51]  S. Dimauro,et al.  The genetics and pathology of oxidative phosphorylation , 2001, Nature Reviews Genetics.

[52]  L. Spremulli,et al.  A new face on apoptosis: death‐associated protein 3 and PDCD9 are mitochondrial ribosomal proteins , 2001, FEBS letters.

[53]  D. Nierlich,et al.  Heart-specific splice-variant of a human mitochondrial ribosomal protein (mRNA processing; tissue specific splicing). , 2000, Gene.

[54]  W. Doolittle,et al.  A kingdom-level phylogeny of eukaryotes based on combined protein data. , 2000, Science.

[55]  J. Broach,et al.  Carboxyl methylation of the phosphoprotein phosphatase 2A catalytic subunit promotes its functional association with regulatory subunits in vivo , 2000, The EMBO journal.

[56]  L. Spremulli,et al.  A Proteomics Approach to the Identification of Mammalian Mitochondrial Small Subunit Ribosomal Proteins* , 2000, The Journal of Biological Chemistry.

[57]  L. Spremulli,et al.  Interaction of Mammalian Mitochondrial Ribosomes with the Inner Membrane* , 2000, The Journal of Biological Chemistry.

[58]  B. Lang,et al.  A novel motif for identifying rps3 homologs in fungal mitochondrial genomes. , 2000, Trends in biochemical sciences.

[59]  Yudong D. He,et al.  Functional Discovery via a Compendium of Expression Profiles , 2000, Cell.

[60]  Hervé Philippe,et al.  Early–branching or fast–evolving eukaryotes? An answer based on slowly evolving positions , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[61]  J. Liu,et al.  Mammalian mitochondrial ribosomal proteins (4). Amino acid sequencing, characterization, and identification of corresponding gene sequences. , 2000, The Journal of biological chemistry.

[62]  A. Chacińska,et al.  Coupling of mitochondrial translation with the formation of respiratory complexes in yeast mitochondria. , 2000, Acta biochimica Polonica.

[63]  D. Eisenberg,et al.  A combined algorithm for genome-wide prediction of protein function , 1999, Nature.

[64]  William Arbuthnot Sir Lane,et al.  A Protein Phosphatase Methylesterase (PME-1) Is One of Several Novel Proteins Stably Associating with Two Inactive Mutants of Protein Phosphatase 2A* , 1999, The Journal of Biological Chemistry.

[65]  M. Saraste.  Oxidative phosphorylation at the fin de siècle. , 1999, Science.

[66]  A. Kimchi,et al.  Structure–function analysis of an evolutionary conserved protein, DAP3, which mediates TNF‐α‐ and Fas‐induced cell death , 1999, The EMBO journal.

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

[68]  B. Thiede,et al.  Mammalian mitochondrial ribosomal proteins (2). Amino acid sequencing, characterization, and identification of corresponding gene sequences. , 1999, The Journal of biological chemistry.

[69]  B. Wittmann-Liebold,et al.  Mammalian Mitochondrial Ribosomal Proteins , 1998, The Journal of Biological Chemistry.

[70]  S F Altschul,et al.  Iterated profile searches with PSI-BLAST--a tool for discovery in protein databases. , 1998, Trends in biochemical sciences.

[71]  J. Smeitink,et al.  The nuclear-encoded human NADH:ubiquinone oxidoreductase NDUFA8 subunit: cDNA cloning, chromosomal localization, tissue distribution, and mutation detection in complex-I-deficient patients , 1998, Human Genetics.

[72]  M. Sørensen,et al.  Ribosomal protein S1 is required for translation of most, if not all, natural mRNAs in Escherichia coli in vivo. , 1998, Journal of molecular biology.

[73]  T. Morio,et al.  A ribosomal protein gene cluster is encoded in the mitochondrial DNA of Dictyostelium discoideum: UGA termination codons and similarity of gene order to Acanthamoeba castellanii , 1998, Current Genetics.

[74]  M. Siegmann,et al.  A novel 52 kDa protein induces apoptosis and concurrently activates c-Jun N-terminal kinase 1 (JNK1) in mouse C3H10T1/2 fibroblasts. , 1998, Gene.

[75]  B. Wittmann-Liebold,et al.  Mitochondrial ribosomal proteins (MRPs) of yeast. , 1998, The Biochemical journal.

[76]  C. Ton,et al.  Identification and primary structure of five human NADH-ubiquinone oxidoreductase subunits. , 1997, Biochemical and biophysical research communications.

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

[78]  K. Isono,et al.  Identification and characterization of the genes for mitochondrial ribosomal proteins of Saccharomyces cerevisiae. , 1997, European journal of biochemistry.

[79]  A. Myers,et al.  Cloning and characterization of MRP10, a yeast gene coding for a mitochondrial ribosomal protein , 1997, Current Genetics.

[80]  C. Ouzounis,et al.  KOW: a novel motif linking a bacterial transcription factor with ribosomal proteins. , 1996, Trends in biochemical sciences.

[81]  W. Schröder,et al.  Transfer of rps19 to the nucleus involves the gain of an RNP‐binding motif which may functionally replace RPS13 in Arabidopsis mitochondria. , 1996, The EMBO journal.

[82]  G. B. Golding,et al.  The origin of the eukaryotic cell. , 1996, Trends in biochemical sciences.

[83]  B. Hemmings,et al.  Differential methylation and altered conformation of cytoplasmic and nuclear forms of protein phosphatase 2A during cell cycle progression , 1995, The Journal of cell biology.

[84]  Sean R. Eddy,et al.  Maximum Discrimination Hidden Markov Models of Sequence Consensus , 1995, J. Comput. Biol..

[85]  L. Isaksson,et al.  Ribosome activity and modification of 16S RNA are influenced by deletion of ribosomal protein S20 , 1993, Molecular microbiology.

[86]  K. Fearon,et al.  Structure and function of MRP20 and MRP49, the nuclear genes for two proteins of the 54 S subunit of the yeast mitochondrial ribosome. , 1992, The Journal of biological chemistry.

[87]  M. Kitakawa,et al.  Extended N‐terminal sequencing of proteins of the large ribosomal subunit from yeast mitochondria , 1991, FEBS letters.

[88]  H. Hartman,et al.  The origin of the eukaryotic cell. , 1984, Speculations in science and technology.

[89]  C. Leaver,et al.  Isolation and characterization of mitochondrial ribosomes from higher plants. , 1972, The Biochemical journal.

[90]  A. Tsugita,et al.  [Protein synthesis in mitochondria]. , 1965, Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme.