An Evolutionary Network of Genes Present in the Eukaryote Common Ancestor Polls Genomes on Eukaryotic and Mitochondrial Origin

To test the predictions of competing and mutually exclusive hypotheses for the origin of eukaryotes, we identified from a sample of 27 sequenced eukaryotic and 994 sequenced prokaryotic genomes 571 genes that were present in the eukaryote common ancestor and that have homologues among eubacterial and archaebacterial genomes. Maximum-likelihood trees identified the prokaryotic genomes that most frequently contained genes branching as the sister to the eukaryotic nuclear homologues. Among the archaebacteria, euryarchaeote genomes most frequently harbored the sister to the eukaryotic nuclear gene, whereas among eubacteria, the α-proteobacteria were most frequently represented within the sister group. Only 3 genes out of 571 gave a 3-domain tree. Homologues from α-proteobacterial genomes that branched as the sister to nuclear genes were found more frequently in genomes of facultatively anaerobic members of the rhiozobiales and rhodospirilliales than in obligate intracellular ricketttsial parasites. Following α-proteobacteria, the most frequent eubacterial sister lineages were γ-proteobacteria, δ-proteobacteria, and firmicutes, which were also the prokaryote genomes least frequently found as monophyletic groups in our trees. Although all 22 higher prokaryotic taxa sampled (crenarchaeotes, γ-proteobacteria, spirochaetes, chlamydias, etc.) harbor genes that branch as the sister to homologues present in the eukaryotic common ancestor, that is not evidence of 22 different prokaryotic cells participating at eukaryote origins because prokaryotic “lineages” have laterally acquired genes for more than 1.5 billion years since eukaryote origins. The data underscore the archaebacterial (host) nature of the eukaryotic informational genes and the eubacterial (mitochondrial) nature of eukaryotic energy metabolism. The network linking genes of the eukaryote ancestor to contemporary homologues distributed across prokaryotic genomes elucidates eukaryote gene origins in a dialect cognizant of gene transfer in nature.

[1]  W. Martin,et al.  Mitochondria as We Don't Know Them , 2002 .

[2]  S. Kelly,et al.  Archaeal phylogenomics provides evidence in support of a methanogenic origin of the Archaea and a thaumarchaeal origin for the eukaryotes , 2010, Proceedings of the Royal Society B: Biological Sciences.

[3]  J. Archibald,et al.  The eukaryotic tree of life: endosymbiosis takes its TOL. , 2008, Trends in ecology & evolution.

[4]  W. Martin,et al.  Genes of cyanobacterial origin in plant nuclear genomes point to a heterocyst-forming plastid ancestor. , 2008, Molecular biology and evolution.

[5]  J A Lake,et al.  Was the nucleus the first endosymbiont? , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Tanya Z. Berardini,et al.  The Arabidopsis Information Resource (TAIR): gene structure and function annotation , 2007, Nucleic Acids Res..

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

[8]  Jinling Huang,et al.  Did an ancient chlamydial endosymbiosis facilitate the establishment of primary plastids? , 2007, Genome Biology.

[9]  James R. Brown,et al.  Archaea and the prokaryote-to-eukaryote transition. , 1997, Microbiology and molecular biology reviews : MMBR.

[10]  W. Martin,et al.  ANNOTATED ENGLISH TRANSLATION OF MERESCHKOWSKY'S 1905 PAPER 'UBER NATUR UND URSPRUNG DER CHROMATOPHOREN IM PFLANZENREICHE' , 1999 .

[11]  Harald Huber,et al.  A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont , 2002, Nature.

[12]  Alexandros Stamatakis,et al.  RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models , 2006, Bioinform..

[13]  W. Martin,et al.  Networks of Gene Sharing among 329 Proteobacterial Genomes Reveal Differences in Lateral Gene Transfer Frequency at Different Phylogenetic Depths , 2010, Molecular biology and evolution.

[14]  D. Raoult,et al.  The rhizome of Reclinomonas americana, Homo sapiens, Pediculus humanus and Saccharomyces cerevisiae mitochondria , 2011, Biology Direct.

[15]  J. Lake,et al.  The ring of life provides evidence for a genome fusion origin of eukaryotes , 2004, Nature.

[16]  T. Cavalier-smith,et al.  The origin of nuclei and of eukaryotic cells , 1975, Nature.

[17]  Michel Casse,et al.  Origin and evolution of the elements , 1993 .

[18]  E. Koonin.  The Logic of Chance: The Nature and Origin of Biological Evolution , 2011 .

[19]  B. Lang,et al.  Mitochondrial Evolution , 1999 .

[20]  T. Shinozawa,et al.  The Origin of Eukaryotes Is Suggested as the Symbiosis of Pyrococcus into γ-Proteobacteria by Phylogenetic Tree Based on Gene Content , 2004, Journal of Molecular Evolution.

[21]  I. Longden,et al.  EMBOSS: the European Molecular Biology Open Software Suite. , 2000, Trends in genetics : TIG.

[22]  J. Lake,et al.  Genomic evidence for two functionally distinct gene classes. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[23]  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.

[24]  P. Thuriaux,et al.  Transcription in archaea: similarity to that in eucarya. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[25]  James A. Lake,et al.  Origin of the eukaryotic nucleus determined by rate-invariant analysis of rRNA sequences , 1988, Nature.

[26]  Tibor Vellai,et al.  A New Aspect to the Origin and Evolution of Eukaryotes , 1998, Journal of Molecular Evolution.

[27]  N. Moran,et al.  Bacterial Genes in the Aphid Genome: Absence of Functional Gene Transfer from Buchnera to Its Host , 2010, PLoS genetics.

[28]  W. Martin,et al.  The origin of mitochondria in light of a fluid prokaryotic chromosome model , 2007, Biology Letters.

[29]  P. Forterre.  A new fusion hypothesis for the origin of Eukarya: better than previous ones, but probably also wrong. , 2011, Research in microbiology.

[30]  G. Gould,et al.  On a possible relationship between bacterial endospore formation and the origin of eukaryotic cells. , 1979, Journal of theoretical biology.

[31]  Dan Graur,et al.  Heads or tails: a simple reliability check for multiple sequence alignments. , 2007, Molecular biology and evolution.

[32]  N. Lane.  Energetics and genetics across the prokaryote-eukaryote divide , 2011, Biology Direct.

[33]  Eugene V. Koonin,et al.  Introns and the origin of nucleus–cytosol compartmentalization , 2006, Nature.

[34]  W. Martin,et al.  Ancestral genome sizes specify the minimum rate of lateral gene transfer during prokaryote evolution , 2007, Proceedings of the National Academy of Sciences.

[35]  E. Koonin,et al.  A korarchaeal genome reveals insights into the evolution of the Archaea , 2008, Proceedings of the National Academy of Sciences.

[36]  W. Martin.  Mosaic bacterial chromosomes: a challenge en route to a tree of genomes. , 1999, BioEssays : news and reviews in molecular, cellular and developmental biology.

[37]  S. Harris,et al.  The archaebacterial origin of eukaryotes , 2008, Proceedings of the National Academy of Sciences.

[38]  Tatiana Tatusova,et al.  NCBI Reference Sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins , 2004, Nucleic Acids Res..

[39]  W. Doolittle,et al.  How big is the iceberg of which organellar genes in nuclear genomes are but the tip? , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[40]  K. Schleifer,et al.  Coexistence of tubulins and ftsZ in different Prosthecobacter species. , 2007, Molecular biology and evolution.

[41]  P. Forterre,et al.  Bacteria with a eukaryotic touch: A glimpse of ancient evolution? , 2010, Proceedings of the National Academy of Sciences of the United States of America.

[42]  Adam Godzik,et al.  Strong functional patterns in the evolution of eukaryotic genomes revealed by the reconstruction of ancestral protein domain repertoires , 2011, Genome Biology.

[43]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[44]  W. Martin,et al.  Higher-plant chloroplast and cytosolic 3-phosphoglycerate kinases: a case of endosymbiotic gene replacement , 2004, Plant Molecular Biology.

[45]  E. Koonin.  Darwinian evolution in the light of genomics , 2008, Nucleic acids research.

[46]  J. McInerney,et al.  Eukaryotic genes of archaebacterial origin are more important than the more numerous eubacterial genes, irrespective of function , 2010, Proceedings of the National Academy of Sciences.

[47]  K. Katoh,et al.  MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. , 2002, Nucleic acids research.

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

[49]  Thijs J. G. Ettema,et al.  A Phylometagenomic Exploration of Oceanic Alphaproteobacteria Reveals Mitochondrial Relatives Unrelated to the SAR11 Clade , 2011, PloS one.

[50]  W. Martin,et al.  The energetics of genome complexity , 2010, Nature.

[51]  David Bryant,et al.  Genome Networks Root the Tree of Life between Prokaryotic Domains , 2010, Genome biology and evolution.

[52]  Eric Bapteste,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:Pattern pluralism and the Tree of Life hypothesis , 2007 .

[53]  Ricardo Guerrero,et al.  The last eukaryotic common ancestor (LECA): Acquisition of cytoskeletal motility from aerotolerant spirochetes in the Proterozoic Eon , 2006, Proceedings of the National Academy of Sciences.

[54]  D. Ussery,et al.  Comparison of 61 Sequenced Escherichia coli Genomes , 2010, Microbial Ecology.

[55]  W. Martin,et al.  Eukaryotic evolution, changes and challenges , 2006, Nature.

[56]  W. Ford Doolittle,et al.  Genes in pieces: were they ever together? , 1978, Nature.

[57]  W. Martin,et al.  How many genes in Arabidopsis come from cyanobacteria? An estimate from 386 protein phylogenies. , 2001, Trends in genetics : TIG.

[58]  L. Orgel,et al.  Phylogenetic Classification and the Universal Tree , 1999 .

[59]  J. Stiller.  Experimental design and statistical rigor in phylogenomics of horizontal and endosymbiotic gene transfer , 2011, BMC Evolutionary Biology.

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

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

[62]  T Martin Embley,et al.  Hydrogenosomes, Mitochondria and Early Eukaryotic Evolution , 2003, IUBMB life.

[63]  Doolittle Wf.  Phylogenetic Classification and the Universal Tree , 1999 .

[64]  Francesca D. Ciccarelli,et al.  Modification of Gene Duplicability during the Evolution of Protein Interaction Network , 2011, PLoS Comput. Biol..

[65]  S. Whelan,et al.  A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. , 2001, Molecular biology and evolution.

[66]  W. Martin.  A briefly argued case that mitochondria and plastids are descendants of endosymbionts, but that the nuclear compartment is not , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[67]  Marc A Suchard,et al.  Phylogeography and population dynamics of dengue viruses in the Americas. , 2012, Molecular biology and evolution.

[68]  Eörs Szathmáry,et al.  The Major Transitions in Evolution , 1997 .

[69]  Daniel J. G. Lahr,et al.  Estimating the timing of early eukaryotic diversification with multigene molecular clocks , 2011, Proceedings of the National Academy of Sciences.

[70]  Purificación López-García,et al.  Symbiosis Between Methanogenic Archaea and δ-Proteobacteria as the Origin of Eukaryotes: The Syntrophic Hypothesis , 1998, Journal of Molecular Evolution.

[71]  W. Martin,et al.  A proteomic survey of Chlamydomonas reinhardtii mitochondria sheds new light on the metabolic plasticity of the organelle and on the nature of the alpha-proteobacterial mitochondrial ancestor. , 2009, Molecular biology and evolution.

[72]  S. Henikoff,et al.  Amino acid substitution matrices from protein blocks. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[73]  Tal Dagan,et al.  Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution , 2008, Proceedings of the National Academy of Sciences.

[74]  M. Posewitz,et al.  Anaerobic Acclimation in Chlamydomonas reinhardtii ANOXICGENEEXPRESSION,HYDROGENASEINDUCTION,ANDMETABOLICPATHWAYS * , 2007 .

[75]  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.

[76]  Ryan J. Yoder,et al.  Phylogenomic evidence for a common ancestor of mitochondria and the SAR11 clade , 2011, Scientific reports.

[77]  Ahmed Moustafa,et al.  Chlamydiae Has Contributed at Least 55 Genes to Plantae with Predominantly Plastid Functions , 2008, PloS one.

[78]  Maureen A. O’Malley,et al.  Prokaryotic evolution and the tree of life are two different things , 2009, Biology Direct.

[79]  Mayo Roettger,et al.  A machine-learning approach reveals that alignment properties alone can accurately predict inference of lateral gene transfer from discordant phylogenies. , 2009, Molecular biology and evolution.

[80]  Tatiana A. Tatusova,et al.  NCBI Reference Sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins , 2004, Nucleic Acids Res..

[81]  W. Martin,et al.  Pyruvate Formate-lyase and a Novel Route of Eukaryotic ATP Synthesis in Chlamydomonas Mitochondria* , 2006, Journal of Biological Chemistry.

[82]  Sean D Hooper,et al.  On the nature of gene innovation: duplication patterns in microbial genomes. , 2003, Molecular biology and evolution.

[83]  J. McInerney,et al.  The prokaryotic tree of life: past, present... and future? , 2008, Trends in ecology & evolution.

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

[85]  L. Hug,et al.  Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic “supergroups” , 2009, Proceedings of the National Academy of Sciences.

[86]  W. Martin,et al.  The tree of one percent , 2006, Genome Biology.

[87]  E. Rocha,et al.  Horizontal Transfer, Not Duplication, Drives the Expansion of Protein Families in Prokaryotes , 2011, PLoS genetics.

[88]  M. Choudhary,et al.  Bacterial genome chimaerism and the origin of mitochondria. , 2011, Canadian journal of microbiology.

[89]  T. Richards,et al.  Cell Evolution: Gene Transfer Agents and the Origin of Mitochondria , 2011, Current Biology.

[90]  P. Forterre.  Thermoreduction, a hypothesis for the origin of prokaryotes. , 1995, Comptes rendus de l'Academie des sciences. Serie III, Sciences de la vie.

[91]  W. Martin,et al.  Directed networks reveal genomic barriers and DNA repair bypasses to lateral gene transfer among prokaryotes. , 2011, Genome research.

[92]  Michael Y. Galperin,et al.  Planctomycetes and eukaryotes: A case of analogy not homology , 2011, BioEssays : news and reviews in molecular, cellular and developmental biology.

[93]  Benjamin M. Wheeler,et al.  The dynamic genome of Hydra , 2010, Nature.

[94]  Arthur R. Grossman,et al.  Anaerobic Acclimation in Chlamydomonas reinhardtii , 2007, Journal of Biological Chemistry.

[95]  M. Wagner,et al.  The Planctomycetes, Verrucomicrobia, Chlamydiae and sister phyla comprise a superphylum with biotechnological and medical relevance. , 2006, Current opinion in biotechnology.

[96]  J. McInerney,et al.  The public goods hypothesis for the evolution of life on Earth , 2011, Biology Direct.

[97]  Davide Pisani,et al.  Supertrees disentangle the chimerical origin of eukaryotic genomes. , 2007, Molecular biology and evolution.

[98]  E. Koonin,et al.  Evolution of diverse cell division and vesicle formation systems in Archaea , 2010, Nature Reviews Microbiology.

[99]  M. Steel,et al.  Recovering evolutionary trees under a more realistic model of sequence evolution. , 1994, Molecular biology and evolution.

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

[101]  Anton J. Enright,et al.  An efficient algorithm for large-scale detection of protein families. , 2002, Nucleic acids research.

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

[103]  D. Devos,et al.  Intermediate Steps , 2010, Science.

[104]  D Penny,et al.  Genomics and the Irreducible Nature of Eukaryote Cells , 2006, Science.

[105]  W. Martin.  Archaebacteria (Archaea) and the origin of the eukaryotic nucleus. , 2005, Current opinion in microbiology.

[106]  Fumiko Ohta,et al.  Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D , 2004, Nature.

[107]  Burkhard Becker,et al.  Chlamydial genes shed light on the evolution of photoautotrophic eukaryotes , 2008, BMC Evolutionary Biology.

[108]  P. Forterre,et al.  The origin of eukaryotes and their relationship with the Archaea: are we at a phylogenomic impasse? , 2010, Nature Reviews Microbiology.

[109]  W. Martin,et al.  Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes , 2004, Nature Reviews Genetics.

[110]  D. Lipman,et al.  A genomic perspective on protein families. , 1997, Science.

[111]  E. Koonin,et al.  The Deep Archaeal Roots of Eukaryotes , 2008, Molecular biology and evolution.