Advertisement

Origins of Life and Evolution of Biospheres

, Volume 35, Issue 6, pp 537–554 | Cite as

The Last Common Ancestor: What's in a name?

  • Luis Delaye
  • Arturo Becerra
  • Antonio Lazcano
Phylogeny

Abstract

Twenty completely sequenced cellular genomes from the three major domains were analyzed using twice one-way BLAST searches in order to define the set of the most conserved protein-encoding sequences to characterize the gene complement of the last common ancestor of extant life. The resulting set is dominated by different putative ATPases, and by molecules involved in gene expression and RNA metabolism. DEAD-type RNA helicase and enolase genes, which are known to be part of the RNA degradosome, are as conserved as many transcription and translation genes. This suggests the early evolution of a control mechanism for gene expression at the RNA level, providing additional support to the hypothesis that during early cellular evolution RNA molecules played a more prominent role. Conserved sequences related to biosynthetic pathways include those encoding putative phosphoribosyl pyrophosphate synthase and thioredoxin, which participate in nucleotide metabolism. Although the information contained in the available databases corresponds only to a minor portion of biological diversity, the sequences reported here are likely to be part of an essential and highly conserved pool of proteins domains common to all organisms.

Keywords

last common ancestor cenancestor RNA/protein world progenote 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, Z., Miller, W. and Lipman, D.J.: 1997, Gapped BLAST and PSI-BLAST: A New Generation of Protein Database Search Programs, Nucleic Acid Res. 25, 3389–3402.CrossRefPubMedGoogle Scholar
  2. Anantharaman, V., Koonin, E.V. and Aravind, L.: 2002, Comparative genomics and evolution of proteins involved in RNA metabolism, Nucleic Acid Res. 30, 1427–1464.CrossRefPubMedGoogle Scholar
  3. Bateman, A., Coin, L., Durbin, R., Finn, R.D., Hollich, V., Griffiths-Jones, S., Khanna, A., Marshall, M., Moxon, S., Sonnhammer, E. L., Studholme, D. J., Yeats, C. and Eddy, S. R.: 2004, The Pfam Protein Families Database, Nucleic Acids Res. 32, 138–141.CrossRefGoogle Scholar
  4. Becerra, A., Islas, S., Leguina, J.I., Silva, E. and Lazcano, A.: 1997, Polyphyletic Gene Losses Can Bias Backtrack Characterizations of the Cenancestor, J. Mol. Evol. 45, 115–118.PubMedGoogle Scholar
  5. Becerra-Bracho, A., Velasco, A.M., Islas, S., Silva, E., Lloret, S. and Lazcano, A.: 2000, Molecular Biology and the Reconstruction of Microbial Phylogenies: Des Laisions Dangereuses? In J. Chela-Flores, G. Lemerchand, and J. Oró (eds), Origins from the Big-Bang to Biology: Proceedings of the First Ibero-American School of Astrobiology, Klüwer Academic Publishers, Dordrecht, pp. 135–150.Google Scholar
  6. Blum, E., Py, B., Carpousis, A.J. and Higgins, C.F.: 1997, Polyphosphate Kinase is a Component of the Escherichia coli RNA degradosome, Mol. Microbiol. 26, 387–398.CrossRefPubMedGoogle Scholar
  7. Böhlke, K., Pisani, F.M., Vorgias, C.E., Frey, B., Sobek, H., Rossi, M. and Antranikian, G.: 2000, PCR Performance of the B-type DNA Polymerase from the Thermophilic Euryarchaeon Thermococcus aggregans Improved by Mutations in the Y-GG/A Motif, Nucleic Acid Res. 28: 3910–3917.Google Scholar
  8. Brown, J.R.: 2003, Ancient Horizontal Gene Transfer, Nature Rev. Genet. 4, 121–132.CrossRefGoogle Scholar
  9. Brown, J.R., Douady, C.J., Italia, M.J., Marshall, W.E. and Stanhope, M.J.: 2001, Universal Trees Based on Large Combined Protein Sequence Data Sets, Nature Genet 28, 281–285.CrossRefPubMedGoogle Scholar
  10. Castresana, J.: 2001, Comparative Genomics and Bioenergetics, Biochem. Biophys. Acta 1506, 147–162.PubMedGoogle Scholar
  11. Castresana, J., Lubben, M., Saraste, M. and Higgins, D.G.: 1994, Evolution of Cytochrome Oxidase, and Enzyme Older than Atmospheric Oxygen, EMBO J. 13, 2516–2525.PubMedGoogle Scholar
  12. Delaye, L. and Lazcano, A.: 2000, RNA-Binding Peptides as Molecular Fossils in J. Chela-Flores, G. Lemerchand, and J. Oró (eds), Origins from the Big-Bang to Biology: Proceedings of the First Ibero-American School of Astrobiology, Kluwer Academic Publishers, Dordrecht, pp. 285–288.Google Scholar
  13. Delaye, L., Becerra, A. and Lazcano, A.: 2002, The Nature of the Last Common Ancestor in Lluis Ribas de Pouplana (ed), The Genetic Code and the Origin of Life, Landes Bioscience, Georgetown, in press.Google Scholar
  14. Doolittle, W.F.: 1999, Phylogenetic Classification and the Universal Tree, Science 284: 2124–2128.CrossRefPubMedGoogle Scholar
  15. Doolittle, W.F.: 2000, The Nature of the Universal Ancestor and the Evolution of the Proteome, Curr. Opinion Struct. Biol. 10, 355–358.CrossRefGoogle Scholar
  16. Edgell, D.R. and Doolittle, W.F.: 1997, Archaea and the Origins, of DNA Replication Proteins, Cell 89, 995–998.CrossRefPubMedGoogle Scholar
  17. Fitch, W.M. and Upper, K.: 1987, The Phylogeny of tRNA Sequences Provides Evidence of Ambiguity Reduction in the Origin of the Genetic Code, Cold Spring Harbor Symp. Quant. Biol. 52, 759–767.PubMedGoogle Scholar
  18. Fitz-Gibbon, S.T. and House, C.H.: 1999, Whole Genome-Based Phylogenetic Analysis of Free-Living Organisms, Nucleic Acids Res. 27, 4218–4222.CrossRefPubMedGoogle Scholar
  19. Forterre, P.: 1999, Displacement of Cellular Proteins by Functional Analogues from Plasmids or Viruses Could Explain Puzzling Phylogenies of Many DNA Informational Proteins, Mol. Microbiol. 33, 457–465.CrossRefPubMedGoogle Scholar
  20. Fox, G.E., Luehrsen, K.R. and Woese, C.R.: 1982, Archaebacterial 5S Ribosomal RNA, Zbl. Bakt. Hyg. I Abt. Orig. C3, 330–345.Google Scholar
  21. Forterre, P.: 2002, The Origin of DNA Genomes and DNA Replication Proteins, Curr. Opin. Microbiol. 5, 525–532.CrossRefPubMedGoogle Scholar
  22. Freeland, S.J., Knight, R.D. and Landweber, L.F.: 1999, Do Proteins Predate DNA? Science 286, 690–692.CrossRefPubMedGoogle Scholar
  23. Glansdorff, N.: 2000, About the Last Common Ancestor, the Universal Life-Tree and Lateral Gene Transfer: A Reappraisal, Mol. Microbiol. 38, 177–185.CrossRefPubMedGoogle Scholar
  24. Gogarten, J.P. and Taiz, L.: 1992, Evolution of Proton-Pumping ATPase: Rooting the Tree of Life, Photosyn. Res. 33: 137–146.CrossRefGoogle Scholar
  25. Haldane, J.B.S.: 1965, Data Needed for the Blueprint of the First Organism. In Fox, S. W. (ed), The Origin of Prebiological Systems and their Molecular Matrices, Academic Press, New York, pp. 11–15.Google Scholar
  26. Harris, J.K., Kelley, S.T., Spiegelman, G.B. and Pace, N.R.: 2003, The Genetic Core of the Universal Ancestor, Genome Res. 13: 407–412.CrossRefPubMedGoogle Scholar
  27. Kandler, O.: 1994, The early diversification of life. In Stefan Bengtson: (ed), Early Life on Earth: Nobel Symposium No. 84, Columbia University Press/Nobel Foundation, New York, pp. 152–160.Google Scholar
  28. Kanehisa, M. and Goto, S.: 2000, KEGG: Kyoto Encyclopedia of Genes and Genomes, Nucleic Acids Res 28: 27–30.CrossRefPubMedGoogle Scholar
  29. Klenk, H.-P., Palm, P., Zillig, W.: 1993, DNA-Dependent RNA Polymerases as Phylogenetic Markers Molecules, Syst. Appl. Microbiol. 16, 138–147.Google Scholar
  30. Koonin, E.V.: 2003, Comparative Genomics, Minimal Gene-Sets and the Last Universal Common Ancestor, Nature Reviews 1, 127–136.CrossRefPubMedGoogle Scholar
  31. Koshland, D.E.: 2002, The Seven Pillars of Life, Science 295, 2215–2216.CrossRefPubMedGoogle Scholar
  32. Lazcano, A., Guerrero, R., Margulis, L. and Oró, J.: 1988, The Evolutionary Transition from RNA to DNA in Early Cells, J. Mol. Evol. 27, 283–290.CrossRefPubMedGoogle Scholar
  33. Lazcano, A.: 1995, Cellular Evolution During the Early Archean: What Happened Between the Progenote and the Cenancestor? Microbiologia SEM 11, 185–198.Google Scholar
  34. Lazcano, A., Fox, G.E. and Oró, J.: 1992, Life before DNA: The Origin and Early Evolution of Early Archean Cells. In R.P. Mortlock: (ed), The Evolution of Metabolic Function, CRC Press, Boca Raton, FL, pp. 237–295.Google Scholar
  35. Lazcano, A. and Miller, S.L.: 1994, How Long did it Take for Life to Begin and Evolve to Cyanobacteria? J. Mol. Evol. 39, 546–554.CrossRefPubMedGoogle Scholar
  36. Leipe, D.D., Aravind, L. and Koonin, E.V.: 1999, Did DNA Replication Evolve Twice Independently? Nucleic Acid Res. 27, 3389–3401.CrossRefPubMedGoogle Scholar
  37. Line, M.A.: 2002, The Enigma of the Origin of Life and its Timing, Microbiology 148, 21–27.PubMedGoogle Scholar
  38. Mushegian, A.R. and Koonin, E.V.: 1996, A Minimal Gene Set for Cellular Life Derived by Comparison of Complete Bacterial Genomes, Proc. Natl. Acad. Sci. USA 93, 10268–10273.CrossRefPubMedGoogle Scholar
  39. Ochman, H., Lawrence, J.G. and Groisman, E.A.: 2000, Lateral Gene Transfer and the Nature of Bacterial Innovation, Nature 405, 299–304.CrossRefPubMedGoogle Scholar
  40. Olsen, G.J. and Woese, C.R.: 1997, Archael Genomics: An Overview, Cell 89, 991–994.CrossRefPubMedGoogle Scholar
  41. Oparin, A.I.: 1961, Life: Its nature, origin and development: Oliver and Boyd, Edinburgh,Google Scholar
  42. Philippe, H. and Forterre, P.: 1999, The Rooting of the Universal Tree of Life is not Reliable, J. Mol. Evol. 49, 509–523.PubMedGoogle Scholar
  43. Reanney, D.C.: 1979, RNA Splicing and Polynucleotide Evolution, Nature 227, 597–600.Google Scholar
  44. Rich, A.: 1962, On the Problems of Evolution and Biochemical Information Transfer. In Kasha, M. and Pullman, B.: (eds), Horizons in Biochemistry, Academic Press, New York, pp. 103–126.Google Scholar
  45. Riera, J., Robb, F.T., Weiss, R. and Fontecave, M.: 1997, Ribonucleotide Reductase in the Archaeon Pyrococcus Furiosus: A Critical Enzyme in the Evolution of DNA Genomes, Proc. Natl. Acad. Sci. USA 94, 475–478.CrossRefPubMedGoogle Scholar
  46. Rivera, M.C. and Lake, J.A.: 2004, The Ring of Life Provides Evidence for a Genome Fusion Origin of Eukaryotes, Nature 431: 152–155.CrossRefPubMedGoogle Scholar
  47. Schmid, S.R. and Linder, P.: 1992, D-E-A-D Protein Family of Putative RNA Helicases, Mol. Microbiol. 6, 283–292.PubMedGoogle Scholar
  48. Seifert, J.L., Martin, K.A., Abdi, F., Wagner, W.R. and Fox, G.E.: 1997, Conserved Gene Clusters in Bacterial Genomes Provide Further Support for the Primacy of RNA. J. Mol. Evol. 45, 467–472.PubMedGoogle Scholar
  49. Snel, B., Bork, P. and Huynen, M.A.: 1999, Genome Phylogeny Based on Gene Content, Nature Genet. 21: 108–110.CrossRefPubMedGoogle Scholar
  50. Snel, B., Bork, P. and Huynen, M.A.: 2002, Genomes in Flux: The Evolution of Archaeal and Proteobacterial Gene Content, Genome Res. 12: 17–25.CrossRefPubMedGoogle Scholar
  51. Tauer, A. and Benner, S.A.: 1996, The B12-Dependent Ribonucleotide Reductase from the Archaebacterium Thermoplasma acidophila: An Evolutionary Solution to the Ribonucleotide Reductase Conundrum, Proc. Natl. Acad. Sci. USA 94: 53–58.CrossRefGoogle Scholar
  52. Tatusov, R.L., Koonin, E.V. and Lipman, D.J.: 1997, A Genomic Perspective on Protein Families, Science 278: 631–637.CrossRefPubMedGoogle Scholar
  53. Tekaia, F., Lazcano, A. and Dujon, B.: 1999, The Genomic Tree as Revealed from Whole Proteome Comparisons, Genome Res. 9, 550–557.PubMedGoogle Scholar
  54. Woese, C.R. and Fox, G.E.: 1977, The Concept of Cellular Evolution, J. Mol. Evol. 10, 1–6.CrossRefPubMedGoogle Scholar
  55. Woese, C.R.: 1983, The Primary Lines of Descent and the Universal Ancestor. In D. S. Bendall (ed), Evolution from Molecules to Men, Cambridge University Press, Cambridge, pp. 209–233.Google Scholar
  56. Woese, C.R.: 1987, Bacterial Evolution. Microbiol, Reviews 51, 221–271.Google Scholar
  57. Woese, C.R.: 1998, The Universal Ancestor, Proc. Natl. Acad. Sci. USA 95, 6854–6859.CrossRefPubMedGoogle Scholar
  58. Woese, C.R., Kandler, O. and Wheelis M.L.: 1990, Towards a Natural System of Organisms: Proposal for the Domains Archaea, Bacteria, and Eucarya, Proc. Natl. Acad. Sci. U S A. 87, 4576–4579.PubMedGoogle Scholar
  59. Zhaxybayeva O. and Gogarten, J.P.: 2004, Cladogenesis, Coalescence and the Evolution of the Three Domains of Life, Trends Genet. 20, 182–187.CrossRefPubMedGoogle Scholar
  60. Zhaxybayeva O., Lapierre, P. and Gogarten, J. P.: 2004, Genome Mosaicism and Organismical Lineages, Trends Genet. 20, 254–260.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science + Business Media, Inc. 2005

Authors and Affiliations

  1. 1.Facultad de Ciencias, UNAM Apdo.Mexico

Personalised recommendations