Abstract
By exploiting three-dimensional structure comparison, which is more sensitive than conventional sequence-based methods for detecting remote homology, we have identified a set of 140 ancestral protein domains using very restrictive criteria to minimize the potential error introduced by horizontal gene transfer. These domains are highly likely to have been present in the Last Universal Common Ancestor (LUCA) based on their universality in almost all of 114 completed prokaryotic (Bacteria and Archaea) and eukaryotic genomes. Functional analysis of these ancestral domains reveals a genetically complex LUCA with practically all the essential functional systems present in extant organisms, supporting the theory that life achieved its modern cellular status much before the main kingdom separation (Doolittle 2000). In addition, we have calculated different estimations of the genetic and functional versatility of all the superfamilies and functional groups in the prokaryote subsample. These estimations reveal that some ancestral superfamilies have been more versatile than others during evolution allowing more genetic and functional variation. Furthermore, the differences in genetic versatility between protein families are more attributable to their functional nature rather than the time that they have been evolving. These differences in tolerance to mutation suggest that some protein families have eroded their phylogenetic signal faster than others, hiding in many cases, their ancestral origin and suggesting that the calculation of 140 ancestral domains is probably an underestimate.
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Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M, Sonnhammer EL (2002) The Pfam protein families database. Nucleic Acids Res 30:276–280
Buchan DW, Rison SC, Bray JE, Lee D, Pearl F, Thornton JM, Orengo CA (2003) Gene3D: structural assignments for the biologist and bioinformaticist alike. Nucleic Acids Res 31:469–473
Castresana J (2001) Comparative genomics and bioenergetics. Biochim Biophys Acta 1506:147–162
Dobrindt U, Hacker J (2001) Whole genome plasticity in pathogenic bacteria. Curr Opin Microbiol 4:550–557
Doolittle WF (2000) The nature of the universal ancestor and the evolution of the proteome. Curr Opin Struct Biol 10:355–358
Dufresne A, Garczarek L, Partensky F (2005) Accelerated evolution associated with genome reduction in a free-living prokaryote. Genome Biol 6:R14
Giovannoni SJ, Tripp HJ, Givan S, Podar M, Vergin KL, Baptista D, Bibbs L, Eads J, Richardson TH, Noordewier M, Rappe MS, Short JM, Carrington JC, Mathur EJ (2005) Genome streamlining in a cosmopolitan oceanic bacterium. Science 309:1242–1245
Koonin EV (2003) Comparative genomics minimal gene-sets and the last universal commonancestor. Nat Rev Microbiol 1:127–136
Lee D, Grant A, Buchan D, Orengo CA (2003) Structural perspective on genome evolution. Curr Opin Struct Biol 13:359–369
Leipe DD, Aravind L, Koonin EV (1999) Did DNA replication evolve twice independently? Nucleic Acids Res 27:3389–3401
McGuffin LJ, Street SA, Bryson K, Sorensen SA, Jones DT (2004) The Genomic Threading Database: a comprehensive resource for structural annotations of the genomes from key organisms. Nucleic Acids Res 32:D196–D199
Metzler DE, ed (2002) Biochemistry. The chemical reactions of living cells, 2nd ed. Academic Press, New York
Mira A, Ochman H, Moran NA (2001) Deletional bias and the evolution of bacterial genomes. Trends Genet 17:589–596
Mirkin BG, Fenner TI, Galperin MY, Koonin EV (2003) 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. BMC Evol Biol 3:2
Moran NA (2002) Microbial minimalism: genome reduction in bacterial pathogens. Cell 108:583–586
Morett E, Korbel JO, Rajan E, Saab-Rincon G, Olvera L, Olvera M, Schmidt S, Snel B, Bork P (2003) Systematic discovery of analogous enzymes in thiamine biosynthesis. Nat Biotechnol 21:790–795
Nelson DL, Cox MM, eds (2000) Lehninger principles of biochemistry, 3rd ed. Worth, New York
Nimwegen E (2003) Scaling laws in the functional content of genomes. Trends Genet 19:479–484
Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304
Orengo CA (1999) CORA—topological fingerprints for protein structural families. Protein Sci 8:699–715
Orengo CA, Michie AD, Jones S, Jones DT, Swindells MB, Thornton JM (1997) CATH—a hierarchic classification of protein domain structures. Structure 5:1093–1108
Ranea JA, Buchan DW, Thornton JM, Orengo CA (2004) Evolution of protein superfamilies and bacterial genome size. J Mol Biol 336:871–887
Ranea JA, Grant A, Thornton JM, Orengo CA (2005) Microeconomic principles explain an optimal genome size in bacteria. Trends Genet 21:21–25
Ranea JA (2005) Micro(be)-economics. Heredity 96:337–338
Shigenobu S, Watanabe H, Hattori M, Sakaki Y, Ishikawa H (2000) Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp APS. Nature 407:81–86
Siegel S, Castellan N (1988) Nonparametric statistics for the behavioural sciences, 2nd ed. Anker JD (ed). McGraw-Hill International Editions, Singapore
Sillero A, Selivanov VA, Cascante M (2006) Pentose phosphate and Calvin cycles: similarities and three-dimensional views. Biochem Mol Biol Edu 34:275–277
Sillitoe I, Dibley M, Bray J, Addou S, Orengo C (2005) Assessing strategies for improved superfamily recognition. Protein Sci 14:1800–1810
Tatusov RL, Koonin EV, Lipman DJ (1997) A genomic perspective on protein families. Science 278:631–637
Tatusov RL, Natale DA, Garkavtsev IV, Tatusova TA, Shankavaram UT, Rao BS, Kiryutin B, Galperin MY, Fedorova ND, Koonin EV (2001) The COG database: new developments in phylogenetic classification of proteins from complete genomes. Nucleic Acids Res 29:22–28
Taylor WR, Orengo CA (1989) Protein structure alignment. J Mol Biol 208:1–22
Todd AE, Orengo CA, Thornton JM (2001) Evolution of function in protein superfamilies from a structural perspective. J Mol Biol 307:1113–1143
Valdar WS (2002) Scoring residue conservation. Proteins 48:227–241
Voet D, Voet J, eds (2004) Biochemistry, 3rd ed. Wiley & Sons, New York
Wayne WD (1995) Biostatistics, 6th ed. Wiley, New York
Whitfield J (2004) Origins of life: born in a watery commune. Nature 427:674–676
Woese C (1998) The universal ancestor. Proc Natl Acad Sci USA 95:6854–6859
Woese CR (2002) On the evolution of cells. Proc Natl Acad Sci USA 99:8742–8747
Acknowledgments
We would like to thank Beatriz Simas Magalhaes for her useful advice and comments, Stathis Sideris for help with the figures, and Corin Yeats for text review. This work was supported by grants from the MRC (Christine A. Orengo) and European Union (Juan A. G. Ranea). A.S. was a visiting professor at UCL (from UAM) aided by the Spanish Ministry of Education and Science and supported by grants from Direccion General de Investigacion Cientifica y Tecnica (08/0021.1/2001) and Instituto de Salud Carlos III, RMN (C03/08) Madrid, Spain.
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Ranea, J.A.G., Sillero, A., Thornton, J.M. et al. Protein Superfamily Evolution and the Last Universal Common Ancestor (LUCA). J Mol Evol 63, 513–525 (2006). https://doi.org/10.1007/s00239-005-0289-7
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DOI: https://doi.org/10.1007/s00239-005-0289-7