Evolution and structural organization of the mitochondrial contact site (MICOS) complex and the mitochondrial intermembrane space bridging (MIB) complex.

We have analyzed the distribution of mitochondrial contact site and cristae organizing system (MICOS) complex proteins and mitochondrial intermembrane space bridging complex (MIB) proteins over (sub)complexes and over species. The MICOS proteins are associated with the formation and maintenance of mitochondrial cristae. Indeed, the presence of MICOS genes in genomes correlates well with the presence of cristae: all cristae containing species have at least one MICOS gene and cristae-less species have none. Mic10 is the most widespread MICOS gene, while Mic60 appears be the oldest one, as it originates in the ancestors of mitochondria, the proteobacteria. In proteobacteria the gene occurs in clusters with genes involved in heme synthesis while the protein has been observed in intracellular membranes of the alphaproteobacterium Rhodobacter sphaeroides. In contrast, Mic23 and Mic27 appear to be the youngest MICOS proteins, as they only occur in opisthokonts. The remaining MICOS proteins, Mic10, Mic19, Mic25 and Mic12, the latter we show to be orthologous to human C19orf70/QIL1, trace back to the root of the eukaryotes. Of the remaining MIB proteins, also DNAJC11 shows a high correlation with the presence of cristae. In mitochondrial protein complexome profiles, the MIB complex occurs as a defined complex and as separate subcomplexes, potentially reflecting various assembly stages. We find three main forms of the complex: A) The MICOS complex, containing all the MICOS proteins, B) a membrane bridging subcomplex, containing in addition SAMM50, MTX2 and the previously uncharacterized MTX3, and C) the complete MIB complex containing in addition DNAJC11 and MTX1.

[1]  J. Poulain,et al.  In Silico Survey of the Mitochondrial Protein Uptake and Maturation Systems in the Brown Alga Ectocarpus siliculosus , 2011, PloS one.

[2]  J. Martinou,et al.  Dual role of mitofilin in mitochondrial membrane organization and protein biogenesis. , 2011, Developmental cell.

[3]  Anastasios D. Tsaousis,et al.  A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi , 2008, Nature.

[4]  H. Braun,et al.  Defining the Protein Complex Proteome of Plant Mitochondria1[W] , 2011, Plant Physiology.

[5]  G. von Heijne,et al.  Materials and Methods Figs. S1 to S3 References and Notes Global Topology Analysis of the Escherichia Coli Inner Membrane Proteome , 2022 .

[6]  Mason R. Mackey,et al.  ChChd3, an Inner Mitochondrial Membrane Protein, Is Essential for Maintaining Crista Integrity and Mitochondrial Function , 2010, The Journal of Biological Chemistry.

[7]  L. Hederstedt,et al.  The hemX gene of the Bacillus subtilis hernAXCDBL operon encodes a membrane protein , negatively affecting the steady-state cellular concentration of HemA ( glutamyl-tRNA reductase ) , 2008 .

[8]  G. Cavallaro.  Genome-wide analysis of eukaryotic twin CX9C proteins. , 2010, Molecular bioSystems.

[9]  H. Braun,et al.  3D Gel Map of Arabidopsis Complex I , 2013, Front. Plant Sci..

[10]  Thomas D. Cuypers,et al.  Iterative orthology prediction uncovers new mitochondrial proteins and identifies C12orf62 as the human ortholog of COX14, a protein involved in the assembly of cytochrome c oxidase , 2012, Genome Biology.

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

[12]  J. Xie,et al.  The mitochondrial inner membrane protein Mitofilin exists as a complex with SAM50, metaxins 1 and 2, coiled‐coil‐helix coiled‐coil‐helix domain‐containing protein 3 and 6 and DnaJC11 , 2007, FEBS letters.

[13]  Robert D. Finn,et al.  HMMER web server: 2015 update , 2015, Nucleic Acids Res..

[14]  M. Yamashita,et al.  The Propionibacterium freudenreichii hemYHBXRL gene cluster, which encodes enzymes and a regulator involved in the biosynthetic pathway from glutamate to protoheme , 1997, Applied Microbiology and Biotechnology.

[15]  A. M. van der Bliek,et al.  A novel mitochondrial outer membrane protein, MOMA-1, that affects cristae morphology in Caenorhabditis elegans , 2011, Molecular biology of the cell.

[16]  G. von Heijne,et al.  Protein Complexes of the Escherichia coli Cell Envelope* , 2005, Journal of Biological Chemistry.

[17]  E. Bock,et al.  [Structural and functional changes in reactivating cells of Nitrobacter winogradskyi Buch]. , 1971, Archiv fur Mikrobiologie.

[18]  R. Zarivach,et al.  Structure prediction of magnetosome-associated proteins , 2014, Front. Microbiol..

[19]  W. Kühlbrandt,et al.  Central role of Mic10 in the mitochondrial contact site and cristae organizing system. , 2015, Cell metabolism.

[20]  M. Huynen,et al.  An anaerobic mitochondrion that produces hydrogen , 2005, Nature.

[21]  T. Przytycka,et al.  Phylogenetic Analysis of Mitochondrial Outer Membrane β-Barrel Channels , 2011, Genome biology and evolution.

[22]  Y. Hiraoka,et al.  ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe , 2006, Nature Biotechnology.

[23]  A. Krogh,et al.  Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. , 2001, Journal of molecular biology.

[24]  Bettina Warscheid,et al.  Role of MINOS in mitochondrial membrane architecture: cristae morphology and outer membrane interactions differentially depend on mitofilin domains. , 2012, Journal of molecular biology.

[25]  Miklós Müller,et al.  Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation , 2003, Nature.

[26]  C. Mannella,et al.  Electron Tomographic and Ultrastructural Analysis of the Cryptosporidium parvum Relict Mitochondrion, its Associated Membranes, and Organelles , 2005, The Journal of eukaryotic microbiology.

[27]  M. Huynen,et al.  Expansion of the human mitochondrial proteome by intra- and inter-compartmental protein duplication , 2009, Genome Biology.

[28]  Jolein Gloerich,et al.  Analysis of 953 Human Proteins from a Mitochondrial HEK293 Fraction by Complexome Profiling , 2013, PloS one.

[29]  E. Shoubridge,et al.  A molecular chaperone for mitochondrial complex I assembly is mutated in a progressive encephalopathy. , 2005, The Journal of clinical investigation.

[30]  S. Jakobs,et al.  MINOS1 is a conserved component of mitofilin complexes and required for mitochondrial function and cristae organization , 2012, Molecular biology of the cell.

[31]  E. Bock,et al.  Struktur- und Funktionsänderungen in reaktivierenden Zellen von Nitrobacter winogradskyi Buch. , 1971, Archiv für Mikrobiologie.

[32]  R. Waller,et al.  The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria , 2004, The Journal of cell biology.

[33]  J. B. Hanson,et al.  Biochemical and Cytological Changes Accompanying Growth and Differentiation in the Roots of Zea mays , 1958, The Journal of biophysical and biochemical cytology.

[34]  L. Condron,et al.  HemX is required for production of 2-ketogluconate, the predominant organic anion required for inorganic phosphate solubilization by Burkholderia sp. Ha185. , 2015, Environmental microbiology reports.

[35]  J. Juang,et al.  Genetic interactions between the Drosophila Abelson (Abl) tyrosine kinase and failed axon connections (fax), a novel protein in axon bundles. , 1995, Genetics.

[36]  Benedikt Westermann,et al.  A mitochondrial-focused genetic interaction map reveals a scaffold-like complex required for inner membrane organization in mitochondria , 2011, The Journal of cell biology.

[37]  George Kollias,et al.  A Splicing Mutation in the Novel Mitochondrial Protein DNAJC11 Causes Motor Neuron Pathology Associated with Cristae Disorganization, and Lymphoid Abnormalities in Mice , 2014, PloS one.

[38]  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.

[39]  P. Oefner,et al.  Proteome analysis of mitochondrial outer membrane from Neurospora crassa , 2006, Proteomics.

[40]  M. Mann,et al.  MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification , 2008, Nature Biotechnology.

[41]  Jeremy G. Wideman,et al.  Ancient Homology of the Mitochondrial Contact Site and Cristae Organizing System Points to an Endosymbiotic Origin of Mitochondrial Cristae , 2015, Current Biology.

[42]  Miklós Müller.  Biochemical cytology of trichomonad flagellates. I. Subcellular localization of hydrolases, dehydrogenases, and catalase in Tritrichomonas foetus. , 1973 .

[43]  A. Reichert,et al.  Complexome profiling identifies TMEM126B as a component of the mitochondrial complex I assembly complex. , 2012, Cell metabolism.

[44]  U. Singha,et al.  Role of Tob55 on mitochondrial protein biogenesis in Trypanosoma brucei. , 2010, Molecular and biochemical parasitology.

[45]  I. J. van der Klei,et al.  Mitofilin complexes: conserved organizers of mitochondrial membrane architecture , 2012, Biological chemistry.

[46]  S. Jakobs,et al.  Mic10 oligomerizes to bend mitochondrial inner membranes at cristae junctions. , 2015, Cell metabolism.

[47]  A. Sedar,et al.  MITOCHONDRIA OF PROTOZOA , 1956, The Journal of biophysical and biochemical cytology.

[48]  Ina Koch,et al.  NOVA: a software to analyze complexome profiling data , 2015, Bioinform..

[49]  R. Rogers,et al.  The Entamoeba histolytica Mitochondrion-Derived Organelle (Crypton) Contains Double-Stranded DNA and Appears To Be Bound by a Double Membrane , 2000, Infection and Immunity.

[50]  R. Jagasia,et al.  Formation of cristae and crista junctions in mitochondria depends on antagonism between Fcj 1 and , 2017 .

[51]  Denice C. Bay,et al.  Phylogenetic and coevolutionary analysis of the β-barrel protein family comprised of mitochondrial porin (VDAC) and Tom40. , 2012, Biochimica et biophysica acta.

[52]  Julian Tonti-Filippini,et al.  Experimental Analysis of the Arabidopsis Mitochondrial Proteome Highlights Signaling and Regulatory Components, Provides Assessment of Targeting Prediction Programs, and Indicates Plant-Specific Mitochondrial Proteins Online version contains Web-only data. Article, publication date, and citation inf , 2004, The Plant Cell Online.

[53]  H. Schägger,et al.  Blue native PAGE , 2006, Nature Protocols.

[54]  Li Li,et al.  The mitochondrial inner membrane protein mitofilin controls cristae morphology. , 2005, Molecular biology of the cell.

[55]  G. Palade,et al.  AN ELECTRON MICROSCOPE STUDY OF THE MITOCHONDRIAL STRUCTURE , 1953, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[56]  A. Lupas,et al.  Predicting coiled coils from protein sequences , 1991, Science.

[57]  Michael J. Dagley,et al.  The Essentials of Protein Import in the Degenerate Mitochondrion of Entamoeba histolytica , 2010, PLoS pathogens.

[58]  Stephan Kutik,et al.  Evolution of mitochondrial protein biogenesis. , 2009, Biochimica et biophysica acta.

[59]  L. Zolla,et al.  Oligomeric characterization of the photosynthetic apparatus of Rhodobacter sphaeroides R26.1 by nondenaturing electrophoresis methods. , 2010, Journal of proteome research.

[60]  Sebastian Straub,et al.  Detailed Analysis of the Human Mitochondrial Contact Site Complex Indicate a Hierarchy of Subunits , 2015, PloS one.

[61]  S. Koob,et al.  The non-glycosylated isoform of MIC26 is a constituent of the mammalian MICOS complex and promotes formation of crista junctions. , 2015, Biochimica et biophysica acta.

[62]  Christian von Mering,et al.  STRING: a database of predicted functional associations between proteins , 2003, Nucleic Acids Res..

[63]  Trevor Lithgow,et al.  Assembling the mitochondrial outer membrane , 2004, Nature Structural &Molecular Biology.

[64]  M. Mann,et al.  Parts per Million Mass Accuracy on an Orbitrap Mass Spectrometer via Lock Mass Injection into a C-trap*S , 2005, Molecular & Cellular Proteomics.

[65]  C. Flynn,et al.  Proteome profile of functional mitochondria from human skeletal muscle using one-dimensional gel electrophoresis and HPLC-ESI-MS/MS. , 2009, Journal of proteomics.

[66]  K. Adolph.  Characterization of the cDNA and amino acid sequences of Xenopus Metaxin 3, and relationship to Xenopus Metaxins 1 and 2 , 2005, DNA sequence : the journal of DNA sequencing and mapping.

[67]  Y. Bahk,et al.  Caenorhabditis elegans mitofilin homologs control the morphology of mitochondrial cristae and influence reproduction and physiology , 2010, Journal of cellular physiology.

[68]  Alex Bateman,et al.  TreeFam v9: a new website, more species and orthology-on-the-fly , 2013, Nucleic Acids Res..

[69]  E. Birney,et al.  Pfam: the protein families database , 2013, Nucleic Acids Res..

[70]  G. G. Stokes.  "J." , 1890, The New Yale Book of Quotations.

[71]  Edward L. Huttlin,et al.  QIL1 is a novel mitochondrial protein required for MICOS complex stability and cristae morphology , 2015, eLife.

[72]  C. Zierdt,et al.  Ultrastructure and light microscope appearance ofBlastocystis hominis in a patient with enteric disease , 1976, Zeitschrift für Parasitenkunde.

[73]  D. Schüler,et al.  Comparative Genome Analysis of Four Magnetotactic Bacteria Reveals a Complex Set of Group-Specific Genes Implicated in Magnetosome Biomineralization and Function , 2007, Journal of bacteriology.

[74]  D. Stokes,et al.  Membrane invagination in Rhodobacter sphaeroides is initiated at curved regions of the cytoplasmic membrane, then forms both budded and fully detached spherical vesicles , 2010, Molecular microbiology.

[75]  I. Kerr,et al.  Analysis of the Sam50 translocase of Excavate organisms supports evolution of divergent organelles from a common endosymbiotic event , 2013, Bioscience reports.

[76]  G. Palade,et al.  The fine structure of mitochondria , 1952, The Anatomical record.

[77]  Alan J. Robinson,et al.  MitoMiner: a data warehouse for mitochondrial proteomics data , 2011, Nucleic Acids Res..

[78]  D. Engelman,et al.  The GxxxG motif: a framework for transmembrane helix-helix association. , 2000, Journal of molecular biology.

[79]  Sang Ki Park,et al.  Uniform nomenclature for the mitochondrial contact site and cristae organizing system , 2014, The Journal of cell biology.

[80]  B. Snel,et al.  STRING: a web-server to retrieve and display the repeatedly occurring neighbourhood of a gene. , 2000, Nucleic acids research.

[81]  Mark H. Ellisman,et al.  Quantitative Evaluation of the Mitochondrial Proteomes of Drosophila melanogaster Adapted to Extreme Oxygen Conditions , 2013, PloS one.

[82]  Erik L. L. Sonnhammer,et al.  A Hidden Markov Model for Predicting Transmembrane Helices in Protein Sequences , 1998, ISMB.

[83]  G. von Heijne,et al.  Tissue-based map of the human proteome , 2015, Science.

[84]  Miss A.O. Penney.  (b) , 1974, The New Yale Book of Quotations.

[85]  J. Poulain,et al.  Genome sequence of the stramenopile Blastocystis, a human anaerobic parasite , 2011, Genome Biology.

[86]  Jyoti S Choudhary,et al.  Phosphoproteomic Analysis of the Mouse Brain Cytosol Reveals a Predominance of Protein Phosphorylation in Regions of Intrinsic Sequence Disorder*S , 2008, Molecular & Cellular Proteomics.