Origin of mitochondria by intracellular enslavement of a photosynthetic purple bacterium

Mitochondria originated by permanent enslavement of purple non-sulphur bacteria. These endosymbionts became organelles through the origin of complex protein-import machinery and insertion into their inner membranes of protein carriers for extracting energy for the host. A chicken-and-egg problem exists: selective advantages for evolving import machinery were absent until inner membrane carriers were present, but this very machinery is now required for carrier insertion. I argue here that this problem was probably circumvented by conversion of the symbiont protein-export machinery into protein-import machinery, in three phases. I suggest that the first carrier entered the periplasmic space via pre-existing β-barrel proteins in the bacterial outer membrane that later became Tom40, and inserted into the inner membrane probably helped by a pre-existing inner membrane protein, thereby immediately providing the protoeukaryote host with photosynthesate. This would have created a powerful selective advantage for evolving more efficient carrier import by inserting Tom70 receptors. Massive gene transfer to the nucleus inevitably occurred by mutation pressure. Finally, pressure from harmful, non-selected gene transfer to the nucleus probably caused evolution of the presequence mechanism, and photosynthesis was lost.

[1]  R. Lewin,et al.  Origins of Plastids , 2012, Springer US.

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

[3]  R. Lister,et al.  Mitochondrial Protein Import: Convergent Solutions for Receptor Structure , 2006, Current Biology.

[4]  T. Lithgow,et al.  Convergent Evolution of Receptors for Protein Import into Mitochondria , 2006, Current Biology.

[5]  Gáspár Jékely,et al.  Evolution of intraflagellar transport from coated vesicles and autogenous origin of the eukaryotic cilium. , 2006, BioEssays : news and reviews in molecular, cellular and developmental biology.

[6]  Enrico Schleiff,et al.  Membrane protein insertion: mixing eukaryotic and prokaryotic concepts , 2005, EMBO reports.

[7]  A. Hehl,et al.  Protein Import, Replication, and Inheritance of a Vestigial Mitochondrion*[boxs] , 2005, Journal of Biological Chemistry.

[8]  T. Cavalier-smith,et al.  Myosin domain evolution and the primary divergence of eukaryotes , 2005, Nature.

[9]  T. Becker,et al.  The Evolutionarily Related β-Barrel Polypeptide Transporters from Pisum sativum and Nostoc PCC7120 Contain Two Distinct Functional Domains* , 2005, Journal of Biological Chemistry.

[10]  H. Kmita,et al.  An Inception Report on the TOM Complex of the Amoeba Acanthamoeba castellanii, a Simple Model Protozoan in Mitochondria Studies , 2005, Journal of bioenergetics and biomembranes.

[11]  H. Weiner,et al.  Bacterial signal peptide recognizes HeLa cell mitochondrial import receptors and functions as a mitochondrial leader sequence , 2005, Cellular and Molecular Life Sciences CMLS.

[12]  M. van der Giezen,et al.  Degenerate mitochondria , 2005, EMBO reports.

[13]  D. Horner,et al.  A Novel ADP/ATP Transporter in the Mitosome of the Microaerophilic Human Parasite Entamoeba histolytica , 2005, Current Biology.

[14]  M. Preuss,et al.  Evolution of Mitochondrial Oxa Proteins from Bacterial YidC , 2005, Journal of Biological Chemistry.

[15]  J. Herrmann Evolution of mitochondrial Oxa proteins from bacterial YidC: Inherited and acquired functions of a conserved protein insertion machinery , 2005 .

[16]  Sujith Puthiyaveetil,et al.  Energy transduction anchors genes in organelles. , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[17]  W. Neupert,et al.  Conserved N-terminal Negative Charges in the Tim17 Subunit of the TIM23 Translocase Play a Critical Role in the Import of Preproteins into Mitochondria* , 2005, Journal of Biological Chemistry.

[18]  W. Neupert,et al.  Assembly of the TOB Complex of Mitochondria* , 2005, Journal of Biological Chemistry.

[19]  Douglas A Lauffenburger,et al.  Directional persistence of EGF-induced cell migration is associated with stabilization of lamellipodial protrusions. , 2005, Biophysical journal.

[20]  W. Neupert,et al.  Signal-anchored Proteins Follow a Unique Insertion Pathway into the Outer Membrane of Mitochondria* , 2005, Journal of Biological Chemistry.

[21]  F. Gannon SARS, Mars and chocolate bars , 2005, EMBO reports.

[22]  Huilin Li,et al.  The outer membrane usher forms a twin-pore secretion complex. , 2004, Journal of molecular biology.

[23]  B Franz Lang,et al.  Mitochondria of protists. , 2004, Annual review of genetics.

[24]  B. Chait,et al.  Components of Coated Vesicles and Nuclear Pore Complexes Share a Common Molecular Architecture , 2004, PLoS biology.

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

[26]  N. Pfanner,et al.  Essential role of Mia40 in import and assembly of mitochondrial intermembrane space proteins , 2004, The EMBO journal.

[27]  M. Steel,et al.  A genome phylogeny for mitochondria among alpha-proteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes. , 2004, Molecular biology and evolution.

[28]  Fredj Tekaia,et al.  Continued Colonization of the Human Genome by Mitochondrial DNA , 2004, PLoS biology.

[29]  T. Kuroiwa,et al.  Triple Immunofluorescent Labeling of FtsZ, Dynamin, and EF-Tu Reveals a Loose Association Between the Inner and Outer Membrane Mitochondrial Division Machinery in the Red Alga Cyanidioschyzon merolae , 2004, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[30]  E. Karlberg,et al.  Computational inference of scenarios for alpha-proteobacterial genome evolution. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[31]  T. Cavalier-smith,et al.  The Membranome and Membrane Heredity in Development and Evolution , 2004 .

[32]  N. Pfanner,et al.  Biogenesis of the Protein Import Channel Tom40 of the Mitochondrial Outer Membrane , 2004, Journal of Biological Chemistry.

[33]  T. Lithgow,et al.  Bacterial proteins predisposed for targeting to mitochondria. , 2004, Molecular biology and evolution.

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

[35]  J. Frank,et al.  Folding kinetics and structure of OEP16. , 2004, Biophysical journal.

[36]  N. Pfanner,et al.  Pam16 has an essential role in the mitochondrial protein import motor , 2004, Nature Structural &Molecular Biology.

[37]  T. Becker,et al.  Preprotein recognition by the Toc complex , 2004, The EMBO journal.

[38]  Ryan Lister,et al.  A plant outer mitochondrial membrane protein with high amino acid sequence identity to a chloroplast protein import receptor , 2004, FEBS letters.

[39]  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.

[40]  K. Adams,et al.  Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. , 2003, Molecular phylogenetics and evolution.

[41]  N. Pfanner,et al.  Mitochondria Use Different Mechanisms for Transport of Multispanning Membrane Proteins through the Intermembrane Space , 2003, Molecular and Cellular Biology.

[42]  T. Cavalier-smith,et al.  The root of the eukaryote tree pinpointed , 2003, Current Biology.

[43]  T. Endo,et al.  Functional cooperation and separation of translocators in protein import into mitochondria, the double-membrane bounded organelles , 2003, Journal of Cell Science.

[44]  S. Bron,et al.  Complementary Impact of Paralogous Oxa1-like Proteins of Bacillus subtilis on Post-translocational Stages in Protein Secretion* , 2003, The Journal of Biological Chemistry.

[45]  Albert Sickmann,et al.  Protein Insertion into the Mitochondrial Inner Membrane by a Twin-Pore Translocase , 2003, Science.

[46]  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.

[47]  D. Horner,et al.  Mitochondria and hydrogenosomes are two forms of the same fundamental organelle. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[48]  T. Cavalier-smith Genomic reduction and evolution of novel genetic membranes and protein-targeting machinery in eukaryote-eukaryote chimaeras (meta-algae). , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[49]  T. Cavalier-smith,et al.  Rooting the Eukaryote Tree by Using a Derived Gene Fusion , 2002, Science.

[50]  T. Cavalier-smith The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. , 2002, International journal of systematic and evolutionary microbiology.

[51]  H. Tabak,et al.  Identification of a Peroxisomal ATP Carrier Required for Medium-Chain Fatty Acid β-Oxidation and Normal Peroxisome Proliferation in Saccharomyces cerevisiae , 2001, Molecular and Cellular Biology.

[52]  K. Mihara,et al.  Characterization of the Signal That Directs Tom20 to the Mitochondrial Outer Membrane , 2000, The Journal of cell biology.

[53]  T. Cavalier-smith,et al.  Membrane heredity and early chloroplast evolution. , 2000, Trends in plant science.

[54]  N. Pfanner,et al.  Biogenesis of Tim proteins of the mitochondrial carrier import pathway: differential targeting mechanisms and crossing over with the main import pathway. , 1999, Molecular biology of the cell.

[55]  J. Soll,et al.  The preprotein translocase of the mitochondrial inner membrane: function and evolution. , 1999, Journal of molecular biology.

[56]  W. Martin,et al.  The hydrogen hypothesis for the first eukaryote , 1998, Nature.

[57]  P. Covello,et al.  On the evolution of RNA editing. , 1993, Trends in genetics : TIG.

[58]  T. Fenchel,et al.  A purple protist , 1993, Nature.

[59]  E. Nisbet Giant African lakes revisited , 1993, Nature.

[60]  T. Cavalier-smith,et al.  Intron phylogeny: a new hypothesis. , 1991, Trends in genetics : TIG.

[61]  F. Hartl,et al.  Mitochondrial protein import. , 1987, Biochimica et biophysica acta.

[62]  T. Cavalier-smith,et al.  The Simultaneous Symbiotic Origin of Mitochondria, Chloroplasts, and Microbodies , 1987, Annals of the New York Academy of Sciences.

[63]  T. Cavalier-smith,et al.  Protozoa as Hosts for Endosymbioses and the Conversion of Symbionts into Organelles1,2 , 1985 .

[64]  T. Cavalier-smith Endosymbiotic Origin Of The Mitochondrial Envelope , 1983 .

[65]  C. Woese Endosymbionts and mitochondrial origins , 1977, Journal of Molecular Evolution.

[66]  S. Aaronson,et al.  The cell content and secretion of water-soluble vitamins by several freshwater algae , 1977, Archives of Microbiology.

[67]  D. Smith,et al.  Constant release of photosynthate from marine phytoplankton , 1976, Applied and environmental microbiology.

[68]  G. Codd,et al.  Enzymes of glycollate formation and oxidation in two members of the rhodospirillaceae (Purple non-sulphur bacteria) , 1975, Archives of Microbiology.

[69]  Philip John,et al.  Paracoccus denitrificans and the evolutionary origin of the mitochondrion , 1975, Nature.

[70]  C. Clark,et al.  Mitochondrion-derived organelles in protists and fungi. , 2005, International review of cytology.

[71]  Aubrey D N J de Grey,et al.  Forces maintaining organellar genomes: is any as strong as genetic code disparity or hydrophobicity? , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[72]  T. Cavalier-smith,et al.  Chromalveolate diversity and cell megaevolution: interplay of membranes, genomes and cytoskeleton. , 2004 .

[73]  T. Cavalier-smith Protist phylogeny and the high-level classification of Protozoa , 2003 .

[74]  T. Cavalier-smith,et al.  The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial megaclassification. , 2002, International journal of systematic and evolutionary microbiology.

[75]  T. Cavalier-smith The Origin, Losses and Gains of Chloroplasts , 1992 .

[76]  F. R. Whatley,et al.  Paracoccus denitrificans Davis (Micrococcus denitrificans Beijerinck) as a Mitochondrion , 1978 .

[77]  Identification of the Mitochondrial ATP-Mg/P i Transporter BACTERIAL EXPRESSION, RECONSTITUTION, FUNCTIONAL CHARACTERIZATION, AND TISSUE DISTRIBUTION* , 2022 .