Structural Phylogenomics Reveals Gradual Evolutionary Replacement of Abiotic Chemistries by Protein Enzymes in Purine Metabolism

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Caetano Anollés, Kelsey ^a,b   Caetano Anollés, Gustavo ^a  

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

^b THE CHICAGO SCHOOL OF PROFESSIONAL PSYCHOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; ARTICLE; BIOCHEMISTRY; ENZYME ACTIVITY; ENZYME ANALYSIS; GENE STRUCTURE; GEOLOGICAL TIME; MOLECULAR CLOCK; MOLECULAR EVOLUTION; PHYLOGENOMICS; PROTEIN DOMAIN; PROTEIN FOLDING; PURINE METABOLISM; RIBOSOME; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

EVOLUTION, MOLECULAR; GENOMICS; PHYLOGENY; PROTEINS; PURINES;

EID: 84874833757     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059300     Document Type: Article

References (61)

1. Caetano-Anollés G, Yafremava LS, Gee H, Caetano-Anollés D, Mittenthal JE, (2009) The origin and evolution of modern metabolism. Intl J Biochem Cell Biol 41: 285-297.
2. 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.
3. 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.
4. Kim H-S, Mittenthal J, Caetano-Anollés G, (2006) MANET: tracing evolution of protein architecture in metabolic networks. BMC Bioinformatics 7: 351.
5. Caetano-Anollés G, Kim H-S, Mittenthal JE, (2007) The origin of modern metabolic networks inferred from phylogenomic analysis of protein architecture. Proc Natl Acad Sci USA 104: 9358-9363.
6. 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.
7. Caetano-Anollés G, Caetano-Anollés D, (2003) An evolutionarily structured universe of protein architecture. Genome Res 13: 1563-1571.
8. 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.
9. Kim KM, Caetano-Anollés G, (2011) The proteomic complexity and rise of the primordial ancestor of diversified life. BMC Evol Biol 11: 140.
10. Kim KM, Caetano-Anollés G, (2012) The evolutionary history of protein fold families and proteomes confirms that the archaeal ancestor is more ancient than the ancestors of other superkingdoms. BMC Evol Biol 12: 13.
11. Berg JM, Tymoczko JL, Stryer L (2002) Biochemistry 5th ed. WH Freeman & Co., New York.
12. Orengo CA, Michie AD, Jones S, Jones DJ, Swindells MB, et al. (1997) CATH: a hierarchic classification of protein domain structures. Structure 5: 1093-1108.
13. Ponting CP, Russell RR, (2002) The natural history of protein domains. Annu Rev Biophys Biomol Struct. 31: 45-71.
14. Reeves GA, Dallman TJ, Redfern OC, Akpor A, Orengo CA, (2006) Structural diversity of domain superfamilies in the CATH database. J Mol Biol 360: 725-741.
15. Teichmann SA, Rison SC, Thornton JM, Riley M, Gough J, et al. (2001) The evolution and structural anatomy of the small molecule metabolic pathways in Escherichia coli. J Mol Biol 311: 693-708.
16. Teichmann SA, Rison SCG, Thornton JM, Riley M, Gough J, et al. (2001) Small-molecule metabolism: an enzyme mosaic. Trends Biotech. 19: 482-486.
17. 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.
18. 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.
19. 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 (2011).
20. 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.
21. Jiang Y-Y, Kong D-K, Qin T, Li X, Caetano-Anollés G, et al. (2012) The impact of oxygen on metabolic evolution: A chemoinformatic investigation. PLoS Comp Biol 8: e1002426.
22. Nasir A, Naeem A, Kahn MJ, Lopez-Nicora HD, Caetano-Anollés G, (2011) Annotation of protein domains reveals remarkable conservation in the functional make up of proteomes across superkingdoms. Genes 2: 869-911.
23. Harish A, Caetano-Anollés G, (2012) Ribosomal history reveals origins of modern protein synthesis. PLoS ONE 7: e32776.
24. 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.
25. Bromham L, Penny D, (2003) The modern molecular clock. Nat Rev Genet 4: 216-224.
26. Graur D, Martin W, (2004) Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision. Trends Genet. 20: 80-86.
27. Bercerra A, Lazcano A, (1998) The role of gene duplication in the evolution of purine nucleotide salvage pathways. Orig Life Evol Biosphere 28: 539-553.
28. Zubay G, (1993) To what extent do biochemical pathways mimic prebiotic pathways? Chemtracts Biochem Mol Biol 4: 317-323.
29. Zubay G, (1994) A feasible prebiotic pathway to the purines. Chemtracts Biochem Mol Biol 5: 179-198.
30. Srinivasan V, Morowitz HJ, (2009) Analysis of the intermediary metabolism of a reductive chemoautotroph. Biol Bull 217: 222-232.
31. Caetano-Anollés G, Seufferheld MJ (2012) The coevolutionary roots of biochemistry and cellular organization challenge the RNA world paradigm. J Mol Microbiol Biotechnol, ms. in press.
32. Sun F-J, Caetano-Anollés G, (2009) The evolutionary history of the structure of 5S ribosomal RNA. J Mol Evol 69: 430-443.
33. 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.
34. Danchin A, Fang G, Noria S, (2007) The extant core bacterial proteome is an archive of the origin of life. Proteomics 7: 875-889.
35. Ycas M, (1874) On earlier states of the biochemical system. J Theor Biol 44: 145-60.
36. Kacser H, Beeby R, (1984) On the origin of enzyme species by means of natural selection. J Mol Evol 20: 38-51.
37. Lazcano A, Miller SL, (1999) On the origin of metabolic pathways. J Mol Evol 49: 424-431.
38. Pereto J, (2012) Out of fuzzy chemistry: from prebiotic chemistry to metabolic networks. Chem Soc Rev 41: 5394-5403.
39. Ferris JP, (1984) The chemistry of life's origin. Chem. Eng. News 62: 22-35.
40. Ferris JP, Hagan Jr WJ, (1984) HCN and chemical evolution: The possible role of cyano compounds in prebiotic synthesis. Tetrahedron 40: 1093-1120.
41. Ferris JP, (2005) Catalysis and prebiotic synthesis. Rev Mineral Geochem 59: 187-210.
42. Zubay G, Mui T, (2001) Prebiotic synthesis of nucleotides. Orig. Life Evol. Biosph. 31: 87-102.
43. Oró J, Kimball AP, (1962) Synthesis of purines under possible primitive Earth conditions. II. Purine intermediates from hydrogen cyanide. Arch. Biochem. Biophys. 96: 293-313.
44. Saladino R, Barontini M, Cossetti C, Di Mauro E, Crestini C, (2011) The effect of borate minerals on the synthesis of nucleic acid bases, amino acids and biogenic carboxylic acids from formamide. Orig. Life Evol. Biosph. 41: 317-330.
45. Holm NG, (2012) The significance of Mg in prebiotic chemistry. Geobiology 10: 269-279.
46. Benner SA, Kim H-J, Carrigan MA, (2012) Asphalt, water, and the prebiotic synthesis of ribose, ribonucleosides, and RNA. Acc Chem Res 45: 2025-2034.
47. Delidovich IV, Simonov AN, Pestunova OP, Parmon VN, (2009) Catalytic condensation of glycolaldehyde and glyceraldehyde with formaldehyde in neutral and weakly alkaline aqueous media: kinetics and mechanism. Kinetics Catalysis 50: 297-303 (2009).
48. Lambert JB, Gurusamy-Thangavelu SA, Ma K, (2010) The silicate-mediated formose reaction: bottom-up synthesis of sugar silicates. Science 327: 984-986.
49. Fuller WD, Sanchez RA, Orgel LE, (1972) Studies in prebiotic synthesis IV. Synthesis of purine nucleosides. J Mol Biol 67: 25-33.
50. Powner MW, Gerland B, Sutherland JD, (2009) Synthesis of activated pyrimidine ribonucleotides in prebiotically plausible conditions. Nature 459: 239-242.
51. Osterberg R, Orgel LE, (1972) Polyphosphate and trimetaphosphate formation under potentially prebiotic conditions. J. Mol. Evol. 1: 241-248.
52. Osterberg R, Orgel LE, Lohrmann R, (1973) Further studies of urea-catalyzed phosphorylation reactions. J Mol Evol 2: 231-234.
53. Lohrmann R, (1977) Formation of nucleoside-5′-phosphoramidates under potentially prebiological conditions. J Mol Evol 10: 137-154.
54. Grant T, (2002) Testing methods: The evaluation of discovery operations in evolutionary biology. Cladistics 18: 94-111.
55. 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 31: 903-919.
56. Swofford DL (1999) Phylogenetic analysis using parsimony and other programs (PAUP*), version 4. Sinauer Assoc, Sunderland, MA.
57. Illegård K, Ardell DH, Elofsson A, (2009) Structure is three to ten times more conserved than sequence - a study of structural response in protein cores. Proteins 77: 499-508.
58. Näsvall J, Sun L, Roth JR, Andersson DI, (2012) Real-time evolution of new genes by innovation, amplification, and divergence. Science 338: 384-387.
59. Kim HS, Mittenthal JE, Caetano-Anollés G, (2013) Widespread recruitment of ancient domain structures in modern enzymes during metabolic evolution. J Integr Bioinform 10: 214.
60. Caetano-Anollés G, Nasir A, (2012) Benefits of using molecular structure and abundance in phylogenomic analysis. Front Genet 3: 172.
61. Anand R, Hoskin AA, Stubbe J, Ealick SE, (2004) Domain organization of Salmonella typhimurium formylglycinamide ribonucleotide amidotransferase revealed by X-ray crystallography. Biochemistry 43: 10328-10342.