Structural Phylogenomics Retrodicts the Origin of the Genetic Code and Uncovers the Evolutionary Impact of Protein Flexibility

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Caetano Anollés, Gustavo ^a   Wang, Minglei ^a   Caetano Anollés, Derek ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID TRANSFER RNA LIGASE; DIPEPTIDASE; DIPEPTIDE; NUCLEIC ACID; POLYPEPTIDE; RNA; SERINE TRANSFER RNA LIGASE; TRANSFER RNA; TYROSINE TRANSFER RNA LIGASE;

AMINO ACID ANALYSIS; AMINO ACID COMPOSITION; AMINO ACID SEQUENCE; AMINOACYLATION; ANTICODON; ARTICLE; CATALYSIS; COEVOLUTION; ENZYME ACTIVITY; ENZYME BINDING; EVOLUTIONARY ADAPTATION; GENE STRUCTURE; GENETIC CODE; GENETIC VARIABILITY; MOLECULAR MECHANICS; NONHUMAN; PHENOTYPIC VARIATION; PHYLOGENOMICS; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; RNA STRUCTURE;

ALGORITHMS; AMINO ACIDS; AMINO ACYL-TRNA SYNTHETASES; BINDING SITES; CATALYTIC DOMAIN; EVOLUTION, MOLECULAR; GENETIC CODE; GENOMICS; MODELS, GENETIC; MODELS, MOLECULAR; PEPTIDES; PHYLOGENY; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN STRUCTURE, TERTIARY; PROTEINS; RNA, TRANSFER;

EID: 84882621993     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072225     Document Type: Article

References (122)

1. Ribas de Pouplana L, Schimmel P, (2001) Aminoacyl-tRNA synthetases: potential markers of genetic code development. Trends Biochem Sci 26: 591-596.
2. Ling J, Reynolds N, Ibba M, (2009) Aminoacyl-tRNA synthesis and translational quality control. Annu Rev Microbiol 63: 61-78.
3. Reynolds NM, Lazazzera BA, Ibba M, (2010) Cellular mechanisms that control mistranslation. Nature Rev Microbiol 8: 849-856.
4. Guo M, Yang X-L, Schimmel P, (2010) New functions of aminoacyl-tRNA synthetases beyond translation. Nature Rev 11: 668-674.
5. Caetano-Anollés G, Wang M, Caetano-Anollés D, Mittenthal JE, (2009) The origin, evolution and structure of the protein world. Biochem J 417: 621-637.
6. Caetano-Anollés D, Kim KM, Mittenthal JE, Caetano-Anollés G, (2011) Proteome evolution and the metabolic origins of translation and cellular life. J Mol Evol 72: 14-32.
7. Caetano-Anollés G, Kim KM, Caetano-Anollés D, (2012) The phylogenomic roots of modern biochemistry: Origins of proteins, cofactors and protein biosynthesis. J Mol Evol 74: 1-34.
8. Murzin A, Brenner SE, Hubbard T, Clothia C, (1995) SCOP: a structural classification of proteins for the investigation of sequences and structures. J Mol Biol 247: 536-540.
9. Caetano-Anollés G, Caetano-Anollés D, (2003) An evolutionarily structured universe of protein architecture. Genome Res 13: 1563-1571.
10. Wang M, Yafremava LS, Caetano-Anollés D, Mittenthal JE, Caetano-Anollés G, (2007) Reductive evolution of architectural repertoires in proteomes and the birth of the tripartite world. Genome Res 17: 1572-1585.
11. Kim KM, Caetano-Anollés G, (2010) Emergence and evolution of modern molecular functions inferred from phylogenomic analysis of ontological data. Mol Biol Evol 27: 1710-1733.
12. Dupont CL, Butcher A, Valas RE, Bourne PE, Caetano-Anollés G, (2010) History of biological metal utilization inferred through phylogenomic analysis of protein structures. Proc Natl Acad Sci USA 107: 10567-10572.
13. Wang M, Jiang Y-Y, Kim KM, Qu G, Ji H-F, et al. (2011) A molecular clock of protein folds and its power in tracing the early history of aerobic metabolism and planet oxygenation. Mol Biol Evol 28: 567-582.
14. Kim KM, Qin T, Jiang Y-Y, Xiong M, Caetano-Anollés D, et al. (2012) Protein domain structure uncovers the origin of aerobic metabolism and the rise of planetary oxygen. Structure 20: 67-76.
15. Saito M, (2012) The rise of oxygen and aerobic biochemistry. Structure 20: 1-2.
16. Danchin A, Fang G, Noria S, (2007) The extant core bacterial proteome is an archive of the origin of life. Proteomics 7: 875-889.
17. Goncearenco A, Berezovsky IN, (2012) Exploring the evolution of protein function in Archaea. BMC Evol Biol 12: 75.
18. Sobolevsky Y, Guimaraes RC, Trifonov EN (2013) Towards functional repertoire of the earliest proteins. J Biomol Struct Dyn, DOI:10.1080/07391102.2012.735623.
19. David LA, Alm EJ, (2010) Rapid evolutionary innovation during an Archaean genetic expansion. Nature 469: 93-96.
20. Caetano-Anollés G, Kim HS, Mittenthal JE, (2007) The origin of modern metabolic networks inferred from phylogenomic analysis of protein architecture. Proc Natl Acad Sci USA 104: 9358-9363.
21. Ye J, Osborne AR, Groll M, Rapoport TA, (2004) RecA-like motor ATPases - lessons from structures. Biochim Biophys Acta 1659: 1-18.
22. Sun F-J, Caetano-Anollés G, (2009) The evolutionary history of the structure of 5S ribosomal RNA. J Mol Evol 69: 430-443.
23. Harish A, Caetano-Anollés G, (2012) Ribosomal history reveals origins of modern protein synthesis. PLoS ONE 7: e32776.
24. Schimmel P, Giege R, Moras D, Yokoyama S, (1993) An operational RNA code for amino acids and possible relation to the genetic code. Proc Natl Acad Sci USA 90: 8763-8768.
25. Giegé R, Sissler M, Florentz C, (1998) Universal rules and idiosyncratic features in tRNA identity. Nucleic Acids Res 26: 5017-5035.
26. Vasil'eva V, Moor NA, (2007) Interaction of aminoacyl-tRNA synthetases with tRNA: General principles and distinguishing characteristics of the high-molecular-weight substrate recognition. Biochemistry 72: 247-263.
27. Yadavalli SS, Ibba M, (2012) Quality control in aminoacyl-tRNA synthesis: Its role in translational fidelity. Adv Protein Chem Struct Biol 86: 1-43.
28. Sun F-J, Caetano-Anollés G, (2008) The origin and evolution of tRNA inferred from phylogenetic analysis of structure. J Mol Evol 66: 21-35.
29. Sun F-J, Caetano-Anollés G, (2008) Evolutionary patterns in the sequence and structure of transfer RNA: A window into early translation and the genetic code. PLoS ONE 3: e2799.
30. Hennig W (1966) Phylogenetic systematics. Urbana: University of Illinois Press.
31. de Pinna MC, (1991) Concepts and tests of homology in the cladistic paradigm. Cladistics 7: 361-394.
32. Lienau EK, DeSalle R, Rosenfeld JA, Planet PJ, (2006) Reciprocal illumination in the gene content tree of life. Syst Biol 55: 441-453.
33. Farris JS, (2008) Parsimony and explanatory power. Cladistics 24: 1-23.
34. Lienau EK, DeSalle R, (2009) Evidence, content and corroboration and the tree of life. Acta Biotheor 57: 187-199.
35. Hale SP, Auld DS, Schmidt E, Schimmel P, (1997) Discrete determinants in transfer RNA for editing and aminoacylation. Science 276: 1250-52.
36. Delarue M, (2007) An asymmetric underlying rule in the assignment of codons: possible clue to a quick early evolution of the genetic code via successive binary choices. RNA 13: 1-9.
37. Rodin SN, Rodin AS, (2008) On the origin of the genetic code: signatures of its primordial complementarity in tRNAs and aminoacyl-tRNA synthetases. Heredity 100: 341-355.
38. Rodin S, Ohno S, (1997) Four primordial modes of tRNA-synthetase recognition, determined by the (G,C) operational code. Proc Natl Acad Sci USA 94: 5183-5188.
39. Ycas M, (1974) On earlier states of the biochemical system. J Theor Biol 44: 145-160.
40. Kacsey H, Beeby R, (1984) On the origin of enzyme species by means of natural selection. J Mol Evol 20: 38-51.
41. Zull JE, Smith SK, (1990) Is genetic code redundancy related to retention of structural information in both DNA strands? Trends Biochem Sci 15: 257-261.
42. Mocibob M, Ivic N, Bilokapic S, Maier T, Luic M, et al. (2010) Homologs of aminoacyl-tRNA synthetases acylate carrier proteins and provide a link between ribosomal and nonribosomal peptide synthesis. Proc Natl Acad Sci USA 107: 14585-14590.
43. Gondry M, Sauguet L, Belin P, Thai R, Amouroux R, et al. (2009) Cyclodipeptide synthetases are a family of tRNA-dependent peptide-bond-forming enzymes. Nature Chem Biol 5: 414-420.
44. Nakashima H, Nishikawa K, Ooi T, (1986) The folding type of a protein is relevant to the amino acid composition. J Biochem. 99: 153-162.
45. Roy S, Martinez D, Platero H, Lane T, Werner-Washburne M, (2009) Exploiting amino acid composition for predicting protein-protein interactions. PLoS ONE 4: e7813.
46. Caetano-Anolles G, Yafremava LS, Mittenthal JM (2010) Modularity and dissipation in the evolution of molecular function, structures and networks. In: Caetano-Anollés G, editor. Evolutionary bioinformatics and systems biology: Hoboken, NJ: Wiley-Blackwell. 431-450.
47. Miller SI, (1953) A production of amino acids under possible primitive Earth conditions. Science 117: 528-529.
48. Ikehara K, (2005) Possible steps to the emergence of life: The [GADV]-protein world hypothesis. Chem Rec 5: 107-118.
49. Jakschitz T, Rode BM, (2012) Evolution from simple inorganic compounds to chiral peptides. Chem Soc Rev 41: 5484-5489.
50. Boniecki MT, Martinis SA, (2012) Coordination of tRNA synthetase active sites for chemical fidelity. J Biol Chem 287: 11285-11289.
51. Pham Y, Kuhlman B, Butterfoss GL, Hu H, Weinreb V, et al. (2010) Tryptophanyl-tRNA synthetase urzyme: A model to recapitulate molecular evolution and investigate intramolecular complementation. J. Biol. Chem. 285: 38590-38601.
52. Li L, Weinreb V, Francklyn C, Carter Jr CW, (2010) Histidyl-tRNA synthetase urzymes: Class I and II aminoacyl tRNA synthetase urzymes have comparable catalytic activities for cognate amino acid activation. J. Biol. Chem. 286: 10387-10395.
53. Eriani G, Delarue M, Poch O, Gangloff J, Moras D, (1990) Partition of aminoacyl-tRNA synthetases into two classes based on mutually exclusive sets of conserved motifs. Nature 347: 203-206.
54. Shitivelband S, Hou Y-M, (2005) Breaking the stereo barrier of amino acid attachment to tRNA by a single nucleotide. J Mol Biol 348: 513-521.
55. Suzuki T, Ueda T, Watanabe K, (1997) The 'polysemous' codon- a codon with multiple amino acid assignment caused by dual specificity of tRNA identity. EMBO J 16: 1122-1134.
56. Caetano-Anollés K, Caetano-Anollés G, (2013) Structural phylogenomics reveals gradual evolutionary replacement of abiotic chemistries by protein enzymes in purine metabolism. PLoS ONE 8: e59300.
57. Wong JT, (2005) Coevolution theory of the genetic code at age thirty. Bioessays 27: 416-425.
58. Hartman H, (1975) Speculations of the evolution of the genetic code. Orig Life 6: 423-427.
59. Karchenko EP, (1976) Principles concerning composition of the genetic code and the possible course of its evolution. Zh Evol Biokhim Fiziol 12: 280-281.
60. Di Giulio M, (1992) On the origin of the transfer RNA molecule. J Theor Biol 159: 199-214.
61. Riddle DS, Santiago JV, Bray-Hall ST, Doshi N, Grantcharova VP, et al. (1997) Functional rapidly folding proteins from simplified amino acid sequences. Nature Struct Biol 4: 805-809.
62. Leszczynski JF, Rose GD, (1986) Loops in globular proteins: a novel category of secondary structure. Science 234: 849-855.
63. Debes C, Wang M, Caetano-Anollés G, Gräter F, (2013) Evolutionary optimization of protein folding. PLoS Comput Biol 9: e1002861.
64. Chao F-A, Morelli A, Haughner JC III, Chuchfield L, Hagmann LN, et al. (2013) Structure and dynamics of a primordial catalytic fold generated by in vitro evolution. Nature Chem Biol 9: 81-83.
65. Trifonov EN, Frenkel ZM, (2009) Evolution of protein modularity. Curr Op Struct Biol 18: 335-340.
66. Caetano-Anollés G, Seufferheld M, (2013) The coevolutionary roots of biochemistry and cellular organization challenge the RNA world paradigm. J Mol Microbiol Biotechnol 23: 152-177.
67. Bilgin T, Kurnaz IA, Wagner A, (2013) Selection shapes the robustness of ligand-binding amino acids. J Mol Evol 76: 343-349.
68. Zhou T, Weems M, Wilke CO, (2009) Translationally optimal codons associate with structurally sensitive sites in proteins. Mol Biol Evol 26: 1571-1580.
69. Ancel LW, Fontana W, (2000) Plasticity, evolvability, and modularity in RNA. J Exp Zool (Mol Dev Evol) 288: 242-283.
70. Sober E, (2004) The contest between parsimony and likelihood. Syst Biol 53: 644-653.
71. Ekman D, Elofsson A, (2010) Identifying and quantifying orphan protein sequences in fungi. J Mol Biol 396: 396-405.
72. Carvunis A-R, Rolland T, Wapinsky I, Calderwood MA, Yildirim MA, et al. (2012) Proto-genes and de novo gene birth. Nature 487: 370-374.
73. Gough J, Karplus K, Hughey R, Chothia C, (2001) Assignment of homology to genome sequences using a library of Hidden Markov Models that represent all proteins of known structure. J Mol Biol 313: 903-919.
74. Caetano-Anollés G, Nasir A, (2012) Benefits of using molecular structure and abundance in phylogenomic analysis. Front Gene 3: 172.
75. Kim KM, Caetano-Anollés G, (2011) The proteomic complexity and rise of the primordial ancestor of diversified life. BMC Evol Biol 11: 140.
76. Hillis DM, Huelsenbeck JP, (1992) Signal, noise, and reliability in molecular phylogenetic analysis. J Hered 83: 189-195.
77. Nasir A, Kim KM, Caetano-Anollés G, (2012) Giant viruses coexisted with the cellular ancestors and represent a distinct supergroup along with superkingdoms Archaea, Bacteria and Eukarya. BMC Evol Biol 12: 156.
78. Wang M, Caetano-Anollés G, (2009) The evolutionary mechanics of domain organization in proteomes and the rise of modularity in the protein world. Structure 17: 66-78.
79. Heard SB, (1996) Patterns of phylogenetic tree balance with variable or evolving speciation rates. Evolution 50: 2141-2148.
80. Webster AJ, Payne RJH, Pagel M, (2007) Molecular phylogenies link rates of evolution and speciation. Science 301: 478.
81. Venditti C, Meade A, Pagel M, (2006) Detecting the node-density artifact in phylogeny reconstruction. Syst Biol 55: 637-643.
82. Caetano-Anollés G, (2002) Evolved RNA secondary structure and the rooting of the universal tree of life. J Mol Evol 54: 333-345.
83. Caetano-Anollés G, (2002) Tracing the evolution of RNA structure in ribosomes. Nucleic Acids Res 30: 2575-2587.
84. Sun F-J, Fleurdépine S, Bousquet-Antonelli C, Caetano-Anollés G, Deragon J-M, (2007) Common evolutionary trends for SINE RNA structures. Trends Genet 23: 26-33.
85. Sun F-J, Caetano-Anollés G, (2008) Evolutionary patterns in the sequence and structure of transfer RNA: early origins of Archaea and viruses. PLoS Comput. Biol 4: e1000018.
86. Sun F-J, Caetano-Anollés G, (2010) The ancient history of the structure of ribonuclease P and the early origins of Archaea. BMC Bioinformatics 11: 153.
87. Sun F-J, Harish A, Caetano-Anolles G (2010) Phylogenetic utility of RNA structure: evolution's arrow and emergence of modern biochemistry and diversified life. In: Caetano-Anollés G, editor. Evolutionary bioinformatics and systems biology: Hoboken, NJ: Wiley-Blackwell.pp. 329-360.
88. Bailor MH, Sun X, Al-Hashimi HM, (2010) Topology links RNA secondary structure with global conformation, dynamics, and adaptation. Science 327: 202-206.
89. O'Donoghue P, Luthey-Schulten Z, (2003) On the evolution of structure in aminoacyl-tRNA synthetases. Microbiol. Mol Biol Rev 67: 550-573.
90. Fournier GP, Andam CP, Alm EJ, Gogarten JP, (2011) Molecular evolution of aminoacyl tRNA synthetase proteins in the early history of life. Orig Life Evol Biosph 41: 621-632.
91. Jühling F, Mörl M, Hartmann RR, Sprinzl M, Stadler PF, et al. (2009) tRNAdb 2009: compiliation of tRNA sequences and tRNA genes. Nucleic Acids Res 37: D159-D162.
92. Kabsch W, Sander C, (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22: 2577-2637.
93. Wang G, Dunbrack Jr RL, (2003) PISCES: a protein sequence culling server. Bioinformatics 19: 1589-1591.
94. Forslund K, Henricson A, Hollich V, Sonnhammer E, (2008) Domain tree-based analysis of protein architecture evolution. Mol Biol Evol 25: 254-264.
95. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, et al. (2000) The Protein Data Bank. Nucleic Acids Res 28: 235-242.
96. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: Tool for the unification of biology. Nature Genetics 25: 25-29.
97. Holm L, Rosenström P, (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res 38: W545-W549.
98. Guerler A, Knapp E-W, (2008) Novel protein folds and their non- sequential structural analogs. Protein Sci 17: 1374-1382.
99. Parker ET, Cleaves HJ, Dworkin JP, Galvin DP, Callahan M, et al. (2011) Primordial synthesis of amines and amino acids in a 1958 Miller H2S-rich spark discharge experiment. Proc Natl Acad Sci USA 106: 5526-5531.
100. Mittenthal JE, Caetano-Anollés D, Caetano-Anollés G, (2012) Biphasic patterns of diversification and the emergence of modules. Front Gene 3: 147.
101. Cusack S, Hartlein M, Leberman R, (1991) Sequence, structure and evolutionary relationships between class 2 aminoacyl-tRNAsynthetases. Nucleic Acid Res 19: 3489-3498.
102. Carter Jr CW, (1993) Cognition, mechanism and evolutionary relationships in aminoacyl-tRNA synthetases. Annu Rev Biochem 62: 715-748.
103. Taylor WR, (2007) Evolutionary transitions in protein fold space. Curr Opin Struct Biol 17: 354-361.
104. Fersht AR, Dingwall C, (1979) An editing mechanism for the methionyl-tRNA synthe- tase in the selection of amino acids in protein synthesis. Biochemistry 18: 1250-1256.
105. Jakubowski H (2005) Accuracy of aminoacyl-tRNA synthetases: proofreading of amino acids. In: Ibba M, Francklyn C, Cusack S, editors. The aminoacyl-tRNA synthetases. Austin, TX: Landes Bioscience. 354-96.
106. Gruic-Sovulj I, Rokov-Plavec J, Weygand-Durasevic I, (2007) Hydrolysis of noncognate aminoacyl-adenylates by a class II aminoacyl-tRNA synthetase lacking an editing domain. FEBS Lett 581: 5110-14.
107. Zhao MW, Zhu B, Hao R, Xu MG, Eriani G, et al. (2005) Leucyl-tRNA synthetase from the ancestral bacterium Aquifex aeolicus contains relics of synthetase evolution. EMBO J 24: 1430-39.
108. Splan KE, Ignatov ME, Musier-Forsyth K, (2008) Transfer RNA modulates the editing mechanism used by class II prolyl-tRNA synthetase. J Biol Chem 283: 7128-34.
109. Fersht AR, Shindler JS, Tsui WC, (1980) Probing the limits of protein-amino acid chain recognition with the aminoacyl-tRNA synthetases. Discrimination against phenylalanine by tyrosyl-tRNA synthetases. Biochemistry 19: 5520-5524.
110. Wakasugi K, Quinn CL, Tao N, Schimmel P, (1997) Genetic code in evolution: switching species-specific aminoacylation with a peptide transplant. EMBO J 17: 297-305.
111. Schmidt E, Schimmel P, (1994) Mutational isolation of a sieve for editing in a transfer RNA synthetase. Science 264: 265-267.
112. Wolf YI, Aravind L, Grishin NV, Koonnin EV, (1999) Evolution of aminoacyl-tRNA synthetases - Analysis of unique domain architectures and phylogenetic trees reveals a complex history of horizontal gene transfer events. Genome Res 9: 689-710.
113. Chothia C, (1976) The nature of the accessible and buried surfaces in proteins. J Mol Biol 105: 1-14.
114. Eichert A, Oberthuer D, Betzel C, Gessner R, Erdmann VA, et al. (2011) The Seryl-tRNA synthetase/tRNASer acceptor stem interface is mediated via a specific network of water molecules. Biochem Biophys Res Comm 412: 532-536.
115. Bilokapic S, Maier T, Ahel D, Gruic-Sovulj I, Söll D, et al. (2006) Structure of the unusual seryl-tRNA synthetase reveals a distinct zinc-dependent mode of structure recognition. EMBO J 24: 2498-2509.
116. Rodin S, Ohno S, (1995) Two types of aminoacyl-tRNA synthetases could be originally encoded by complementary strands of the same nucleic acid. Orig Life Evol Biosph 25: 565-589.
117. Ribas de Pouplana L, Schimmel P, (2001) Two classes of tRNA synthetases suggested by sterically compatible dockings on tRNA acceptor stem. Cell 104: 191-193.
118. Terada T, Nureki O, Ishitani R, Ambrogelly A, Ibba S, et al. (2002) Functional convergence of two lysyl-tRNA synthetases with unrelated topologies. Nature Struct Biol 9: 257-262.
119. Vetting MW, Hedge SS, Blanchard JS, (2010) The structure and mechanism of the Mycobacterium tuberculosis cyclodityrosine synthetase. Nature Chem Biol 6: 797-799.
120. Sauguet L, Moutiez M, Li Y, Belin P, Seguin J, et al. (2011) Cyclodipeptide synthases, a family of class-I aminoacyl-tRNA synthetase-like enzymes involved in non-ribosomal peptide synthesis. Nucleic Acids Res 39: 4475-4489.
121. Bonnefond L, Arai T, Sakaguchi Y, Suzuki T, Ishitani R, et al. (2011) Structural basis for nonribosomal peptide synthesis by an aminoacyl-tRNA synthetase paralog. Proc Natl Acad Sci USA 108: 3912-3917.
122. Rodin AS, Szathmáry E, Rodin SN, (2011) On the origin of genetic code and tRNA before translation. Biol Direct 6: 14.