On the Origin of Cells and Viruses: A Comparative-Genomic Perspective

It is proposed that the pre-cellular stage of biological evolution, including the Last Universal Common Ancestor (LUCA) of modern cellular life forms, occurred within networks of inorganic compartments that hosted a diverse mix of virus-like genetic elements. This viral model of cellular origin recapitulates the early ideas of J.B.S. Haldane, sketched in his 1928 essay on the origin of life. However, unlike in Haldane's day, there is substantial empirical support for this scenario from three major lines of evidence provided by comparative genomics: (i) the lack of homology among the core components of the DNA replication systems between the two primary lines of descent of cellular life forms, archaea and bacteria, (ii) the similar lack of homology between the enzymes of lipid biosynthesis in conjunction with distinct membrane chemistries in archaea and bacteria, and (iii) the spread of several viral hallmark genes, which encode proteins with key functions in viral replication and morphogenesis, among nume...

[1]  Eugene V Koonin,et al.  Temporal order of evolution of DNA replication systems inferred by comparison of cellular and viral DNA polymerases , 2006, Biology Direct.

[2]  E. Koonin,et al.  The ancient Virus World and evolution of cells , 2006, Biology Direct.

[3]  J. Claverie Viruses take center stage in cellular evolution , 2006, Genome Biology.

[4]  N. Goldenfeld,et al.  Collective evolution and the genetic code. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[5]  E. Koonin,et al.  Evolution of complexity in the viral world: the dawn of a new vision. , 2006, Virus research.

[6]  Patrick Forterre,et al.  The origin of viruses and their possible roles in major evolutionary transitions. , 2006, Virus research.

[7]  Eugene V Koonin,et al.  Evolutionary genomics of nucleo-cytoplasmic large DNA viruses. , 2006, Virus research.

[8]  N. Grishin,et al.  A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action , 2006, Biology Direct.

[9]  P. Forterre Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: a hypothesis for the origin of cellular domain. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[10]  J. Ziebuhr,et al.  Nidovirales: Evolving the largest RNA virus genome , 2006, Virus Research.

[11]  E. Mancini,et al.  Hexameric molecular motors: P4 packaging ATPase unravels the mechanism , 2006, Cellular and Molecular Life Sciences CMLS.

[12]  D. Chandler,et al.  Dynamic pathways for viral capsid assembly. , 2005, Biophysical journal.

[13]  A. Mushegian,et al.  Natural history of S-adenosylmethionine-binding proteins , 2005, BMC Structural Biology.

[14]  Eugene V Koonin,et al.  On the origin of genomes and cells within inorganic compartments , 2005, Trends in Genetics.

[15]  Patrick Forterre,et al.  Luca : À la recherche du plus proche ancêtre commun universel , 2005 .

[16]  Phillip D. Zamore,et al.  Ribo-gnome: The Big World of Small RNAs , 2005, Science.

[17]  P. Forterre The two ages of the RNA world, and the transition to the DNA world: a story of viruses and cells. , 2005, Biochimie.

[18]  Jean-Michel Claverie,et al.  Mimivirus and the emerging concept of "giant" virus. , 2005, Virus research.

[19]  R. Doolittle,et al.  Evolutionary aspects of whole-genome biology. , 2005, Current opinion in structural biology.

[20]  F. Delsuc,et al.  Phylogenomics and the reconstruction of the tree of life , 2005, Nature Reviews Genetics.

[21]  E. Koonin Virology: Gulliver among the Lilliputians , 2005, Current Biology.

[22]  Robert L Charlebois,et al.  Chlamydia: 780.57 (sd = 1.81), range 778–784, n =7 Cyanobacteria: 820.50 (sd = 23.53), range 776–844, n =8 , 2022 .

[23]  D. S. Weiss,et al.  Bacterial cell division and the septal ring , 2004, Molecular microbiology.

[24]  Purificación López-García,et al.  Ancestral lipid biosynthesis and early membrane evolution. , 2004, Trends in biochemical sciences.

[25]  L. Mindich Packaging, replication and recombination of the segmented genome of bacteriophage Phi6 and its relatives. , 2004, Virus research.

[26]  Eugene V. Koonin,et al.  Comparative genomics, minimal gene-sets and the last universal common ancestor , 2003, Nature Reviews Microbiology.

[27]  C. Ouzounis,et al.  The balance of driving forces during genome evolution in prokaryotes. , 2003, Genome research.

[28]  P. Forterre The great virus comeback-- from an evolutionary perspective. , 2003, Research in microbiology.

[29]  J. Errington,et al.  Cytokinesis in Bacteria , 2003, Microbiology and Molecular Biology Reviews.

[30]  Wen-Hsiung Li,et al.  Molecular evolution meets the genomics revolution , 2003, Nature Genetics.

[31]  N. Pace,et al.  The genetic core of the universal ancestor. , 2003, Genome research.

[32]  Gregory J. Morgan Historical review: viruses, crystals and geodesic domes. , 2003, Trends in biochemical sciences.

[33]  W. Martin,et al.  On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[34]  Michael Y. Galperin,et al.  Algorithms for computing parsimonious evolutionary scenarios for genome evolution, the last universal common ancestor and dominance of horizontal gene transfer in the evolution of prokaryotes , 2003, BMC Evolutionary Biology.

[35]  D. Bamford,et al.  Nonspecific Nucleoside Triphosphatase P4 of Double-Stranded RNA Bacteriophage φ6 Is Required for Single-Stranded RNA Packaging and Transcription , 2002, Journal of Virology.

[36]  Patrick Forterre,et al.  The origin of DNA genomes and DNA replication proteins. , 2002, Current opinion in microbiology.

[37]  Elias Zintzaras,et al.  "Living" under the challenge of information decay: the stochastic corrector model vs. hypercycles. , 2002, Journal of theoretical biology.

[38]  Eugene V Koonin,et al.  Monophyly of class I aminoacyl tRNA synthetase, USPA, ETFP, photolyase, and PP‐ATPase nucleotide‐binding domains: implications for protein evolution in the RNA world , 2002, Proteins.

[39]  C. Woese On the evolution of cells , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[40]  E. Koonin,et al.  Trends in protein evolution inferred from sequence and structure analysis. , 2002, Current opinion in structural biology.

[41]  Eugene V Koonin,et al.  Comparative genomics and evolution of proteins involved in RNA metabolism. , 2002, Nucleic acids research.

[42]  W. Donachie FtsK: Maxwell's Demon? , 2002, Molecular cell.

[43]  E. Koonin,et al.  Genome alignment, evolution of prokaryotic genome organization, and prediction of gene function using genomic context. , 2001, Genome research.

[44]  M. Rossmann,et al.  Structure of the bacteriophage φ29 DNA packaging motor , 2000, Nature.

[45]  P Bork,et al.  Gene context conservation of a higher order than operons. , 2000, Trends in biochemical sciences.

[46]  E. Koonin,et al.  The Impact of Comparative Genomics on Our Understanding of Evolution , 2000, Cell.

[47]  R. Nakamoto,et al.  Molecular mechanisms of rotational catalysis in the F(0)F(1) ATP synthase. , 2000, Biochimica et biophysica acta.

[48]  Gary J. Olsen,et al.  Aminoacyl-tRNA Synthetases, the Genetic Code, and the Evolutionary Process , 2000, Microbiology and Molecular Biology Reviews.

[49]  C. Catalano The terminase enzyme from bacteriophage lambda: a DNA-packaging machine , 2000, Cellular and Molecular Life Sciences CMLS.

[50]  P. Forterre,et al.  The Rooting of the Universal Tree of Life Is Not Reliable , 1999, Journal of Molecular Evolution.

[51]  H Philippe,et al.  Where is the root of the universal tree of life? , 1999, BioEssays : news and reviews in molecular, cellular and developmental biology.

[52]  Hervé Philippe,et al.  The Root of the Tree of Life in the Light of the Covarion Model , 1999, Journal of Molecular Evolution.

[53]  Detlef D. Leipe,et al.  Did DNA replication evolve twice independently? , 1999, Nucleic acids research.

[54]  P. Forterre Displacement of cellular proteins by functional analogues from plasmids or viruses could explain puzzling phylogenies of many DNA informational proteins , 1999, Molecular microbiology.

[55]  E V Koonin,et al.  Evolution of aminoacyl-tRNA synthetases--analysis of unique domain architectures and phylogenetic trees reveals a complex history of horizontal gene transfer events. , 1999, Genome research.

[56]  P. Forterre,et al.  The last universal common ancestor (LUCA), simple or complex? , 1999, The Biological bulletin.

[57]  C. Woese The universal ancestor. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

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

[59]  S. Gould,et al.  The exaptive excellence of spandrels as a term and prototype. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[60]  W. Doolittle,et al.  Archaea and the Origin(s) of DNA Replication Proteins , 1997, Cell.

[61]  E. Koonin,et al.  The genome of molluscum contagiosum virus: analysis and comparison with other poxviruses. , 1997, Virology.

[62]  E. Koonin,et al.  A minimal gene set for cellular life derived by comparison of complete bacterial genomes. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[63]  P. Bork,et al.  Non-orthologous gene displacement. , 1996, Trends in genetics : TIG.

[64]  E. Szathmáry,et al.  Group selection of early replicators and the origin of life. , 1987, Journal of theoretical biology.

[65]  M. Eigen,et al.  The hypercycle. A principle of natural self-organization. Part A: Emergence of the hypercycle. , 1977, Die Naturwissenschaften.

[66]  George E. Fox,et al.  The concept of cellular evolution , 1977, Journal of Molecular Evolution.

[67]  V. Agol,et al.  An aspect of the origin and evolution of viruses , 1976, Origins of life.

[68]  M. Eigen Selforganization of matter and the evolution of biological macromolecules , 1971, Naturwissenschaften.

[69]  D. Baltimore Viral genetic systems. , 1971, Transactions of the New York Academy of Sciences.

[70]  A. Oparin [The origin of life]. , 1938, Nordisk medicin.

[71]  Leon Goldovsky,et al.  A minimal estimate for the gene content of the last universal common ancestor--exobiology from a terrestrial perspective. , 2006, Research in microbiology.

[72]  Paula Traktman,et al.  In a nutshell: structure and assembly of the vaccinia virion. , 2006, Advances in virus research.

[73]  R. Tuma,et al.  Assembly of double-stranded RNA bacteriophages. , 2005, Advances in virus research.

[74]  Eugene V Koonin,et al.  Comparative genomics of the FtsK-HerA superfamily of pumping ATPases: implications for the origins of chromosome segregation, cell division and viral capsid packaging. , 2004, Nucleic acids research.

[75]  G. Darai,et al.  Poxvirus Homologues of Cellular Genes , 2004, Virus Genes.

[76]  S. Grimes,et al.  Bacteriophage φ29 DNA packaging , 2002 .

[77]  B. Snel,et al.  Genomes in flux: the evolution of archaeal and proteobacterial gene content. , 2002, Genome research.

[78]  P. Forterre,et al.  The nature of the last universal ancestor and the root of the tree of life, still open questions. , 1992, Bio Systems.

[79]  R. Matthews The origin of viruses from cells. , 1983, International review of cytology. Supplement.

[80]  A. Klug,et al.  The structure of small viruses. , 1960, Advances in virus research.