Abstract
An RNA World that predated the modern world of polypeptide and polynucleotide is one of the most widely accepted models in origin of life research. In this model, the translation system shepherded the RNA World into the extant biology of DNA, RNA, and protein. Here, we examine the RNA World Hypothesis in the context of increasingly detailed information available about the origins, evolution, functions, and mechanisms of the translation system. We conclude that the translation system presents critical challenges to RNA World Hypotheses. Firstly, a timeline of the RNA World is problematic when the ribosome is incorporated. The mechanism of peptidyl transfer of the ribosome appears distinct from evolved enzymes, signaling origins in a chemical rather than biological milieu. Secondly, we have no evidence that the basic biochemical toolset of life is subject to substantive change by Darwinian evolution, as required for the transition from the RNA world to extant biology. Thirdly, we do not see specific evidence for biological takeover of ribozyme function by protein enzymes. Finally, we can find no basis for preservation of the ribosome as ribozyme or the universality of translation, if it were the case that other information transducing ribozymes, such as ribozyme polymerases, were replaced by protein analogs and erased from the phylogenetic record. We suggest that an updated model of the RNA World should address the current state of knowledge of the translation system.
Similar content being viewed by others
References
Ada GL, Perry BT (1954) The nucleic acid content of influenza virus. Aust J Exp Biol 32:453–468
Amunts A, Brown A, Bai XC, Llacer JL, Hussain T, Emsley P, Long F, Murshudov G, Scheres SH, Ramakrishnan V (2014) Structure of the yeast mitochondrial large ribosomal subunit. Science 343:1485–1489
Anbar AD (2008) Oceans. Elements and evolution. Science 322:1481–1483
Anger AM, Armache JP, Berninghausen O, Habeck M, Subklewe M, Wilson DN, Beckmann R (2013) Structures of the human and drosophila 80S ribosome. Nature 497:80–85
Armache JP, Jarasch A, Anger AM, Villa E, Becker T, Bhushan S, Jossinet F, Habeck M, Dindar G, Franckenberg S, Marquez V, Mielke T, Thomm M, Berninghausen O, Beatrix B, Soding J, Westhof E, Wilson DN, Beckmann R (2010) Cryo-EM structure and rRNA model of a translating eukaryotic 80S ribosome at 5.5 Å resolution. Proc Natl Acad Sci USA 107:19748–19753
Athavale SS, Petrov AS, Hsiao C, Watkins D, Prickett CD, Gossett JJ, Lie L, Bowman JC, O’Neill E, Bernier CR, Hud NV, Wartell RM, Harvey SC, Williams LD (2012) RNA folding and catalysis mediated by iron (II). PLoS ONE 7:e38024
Attwater J, Tagami S, Kimoto M, Butler K, Kool ET, Wengel J, Herdewijn P, Hirao I, Holliger P (2013) Chemical fidelity of an RNA polymerase ribozyme. Chem Sci 4:2804–2814
Ban N, Nissen P, Hansen J, Moore PB, Steitz TA (2000) The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289:905–920
Belousoff MJ, Davidovich C, Zimmerman E, Caspi Y, Wekselman I, Rozenszajn L, Shapira T, Sade-Falk O, Taha L, Bashan A, Weiss MS, Yonath A (2010) Ancient machinery embedded in the contemporary ribosome. Biochem Soc Trans 38:422–427
Benner SA, Ellington AD, Tauer A (1989) Modern metabolism as a palimpsest of the RNA world. Proc Natl Acad Sci USA 86:7054–7058
Ben-Shem A, Jenner L, Yusupova G, Yusupov M (2010) Crystal structure of the eukaryotic ribosome. Science 330:1203–1209
Berk V, Zhang W, Pai RD, Cate JH (2006) Structural basis for mRNA and tRNA positioning on the ribosome. Proc Natl Acad Sci USA 103:15830–15834
Bernhardt HS (2012) The RNA world hypothesis: The worst theory of the early evolution of life (except for all the others). Biol Direct 7:23
Bokov K, Steinberg SV (2009) A hierarchical model for evolution of 23S ribosomal RNA. Nature 457:977–980
Bu D, Zhao Y, Cai L, Xue H, Zhu X, Lu H, Zhang J, Sun S, Ling L, Zhang N, Li G, Chen R (2003) Topological structure analysis of the protein-protein interaction network in budding yeast. Nucleic Acids Res 31:2443–2450
Butland G, Peregrin-Alvarez JM, Li J, Yang W, Yang X, Canadien V, Starostine A, Richards D, Beattie B, Krogan N, Davey M, Parkinson J, Greenblatt J, Emili A (2005) Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 433:531–537
Cafferty BJ, Hud NV (2014) Abiotic synthesis of RNA in water: a common goal of prebiotic chemistry and bottom-up synthetic biology. Curr Opin Chem Biol 22:146–157
Cafferty BJ, Gallego I, Chen MC, Farley KI, Eritja R, Hud NV (2013) Efficient self-assembly in water of long noncovalent polymers by nucleobase analogues. J Am Chem Soc 135:2447–2450
Callahan MP, Smith KE, Cleaves HJ 2nd, Ruzicka J, Stern JC, Glavin DP, House CH, Dworkin JP (2011) Carbonaceous meteorites contain a wide range of extraterrestrial nucleobases. Proc Natl Acad Sci USA 108:13995–13998
Carrasco N, Hiller DA, Strobel SA (2011) Minimal transition state charge stabilization of the oxyanion during peptide bond formation by the ribosome. Biochemistry 50:10491–10498
Carter CW, Li L, Weinreb V, Collier M, Gonzalez-Rivera K, Jimenez-Rodriguez M, Erdogan O, Kuhlman B, Ambroggio X, Williams T, Chandrasekharan SN (2014) The rodin-ohno hypothesis that two enzyme superfamilies descended from one ancestral gene: An unlikely scenario for the origins of translation that will not be dismissed. Biol Direct 9:23
Cate JH, Yusupov MM, Yusupova GZ, Earnest TN, Noller HF (1999) X-ray crystal structures of 70S ribosome functional complexes. Science 285:2095–2104
Caton JS, Bauer ML, Hidari H (2000) Metabolic components of energy expenditure in growing beef cattle—review. Asian Aust J Anim Sci 13:702–710
Cech TR (2002) Ribozymes, the first 20 years. Biochem Soc Trans 30:1162–1166
Cech TR (2009) Crawling out of the RNA world. Cell 136:599–602
Chao F-C, Schachman HK (1956) The isolation and characterization of a macromolecular ribonucleoprotein from yeast. Arch Biochem Biophys 61:220–230
Chen MC, Cafferty BJ, Mamajanov I, Gallego I, Khanam J, Krishnamurthy R, Hud NV (2014) Spontaneous prebiotic formation of a β-ribofuranoside that self-assembles with a complementary heterocycle. J Am Chem Soc 136:5640–5646
Clark MA, Moran NA, Baumann P, Wernegreen JJ (2000) Cospeciation between bacterial endosymbionts (buchnera) and a recent radiation of aphids (uroleucon) and pitfalls of testing for phylogenetic congruence. Evolution 54:517–525
Crick FH (1968) The origin of the genetic code. J Mol Biol 38:367–379
Crick F (1970) Central dogma of molecular biology. Nature 226:561–563
Dale T, Uhlenbeck OC (2005) Amino acid specificity in translation. Trends Biochem Sci 30:659–665
Dawkins R (2006) The selfish gene: 30th anniversary edition. Oxford University Press, Oxford
Demeshkina N, Jenner L, Westhof E, Yusupov M, Yusupova G (2013) New structural insights into the decoding mechanism: translation infidelity via a g.U pair with Watson-Crick geometry. FEBS Lett 587:1848–1857
Dvir S, Velten L, Sharon E, Zeevi D, Carey LB, Weinberger A, Segal E (2013) Deciphering the rules by which 5′-UTR sequences affect protein expression in yeast. Proc Natl Acad Sci USA 110:E2792–2801
Eigen M (1993) Viral quasispecies. Sci Am 269:42–49
Ekici OD, Paetzel M, Dalbey RE (2008) Unconventional serine proteases: Variations on the catalytic ser/his/asp triad configuration. Protein Sci 17:2023–2037
Fahnestock S, Rich A (1971) Ribosome-catalyzed polyester formation. Science 173:340–343
Fahnestock S, Neumann H, Shashoua V, Rich A (1970) Ribosome-catalyzed ester formation. Biochemistry 9:2477–2483
Fournier GP, Neumann JE, Gogarten JP (2010) Inferring the ancient history of the translation machinery and genetic code via recapitulation of ribosomal subunit assembly orders. PLoS ONE 5:e9437
Fox GE (2010) Origin and evolution of the ribosome. Cold Spring Harb Perspect Biol 2:a003483
Fox GE, Tran Q, Yonath A (2012) An exit cavity was crucial to the polymerase activity of the early ribosome. Astrobiology 12:57–60
Gerbi SA (1996) Expansion segments: regions of variable size that interrupt the universal core secondary structure of ribosomal RNA. In: Zimmermann RA, Dahlberg AE (eds) Ribosomal RNA—structure, evolution, processing, and function in protein synthesis. CRC Press, Boca Raton, pp 71–87
Gilbert W (1986) Origin of life: the RNA world. Nature 319:618–618
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
Gray MW (2012) Mitochondrial evolution. Cold Spring Harbor Perspect Biol 4(9):a011403
Greber BJ, Boehringer D, Leitner A, Bieri P, Voigts-Hoffmann F, Erzberger JP, Leibundgut M, Aebersold R, Ban N (2014) Architecture of the large subunit of the mammalian mitochondrial ribosome. Nature 505:515–519
Guerrier-Takada C, Gardiner K, Marsh T, Pace N, Altman S (1983) The RNA moiety of ribonuclease p is the catalytic subunit of the enzyme. Cell 35:849–857
Guo M, Schimmel P (2012) Structural analyses clarify the complex control of mistranslation by tRNA synthetases. Curr Opin Struct Biol 22:119–126
Harms J, Schluenzen F, Zarivach R, Bashan A, Gat S, Agmon I, Bartels H, Franceschi F, Yonath A (2001) High resolution structure of the large ribosomal subunit from a mesophilic eubacterium. Cell 107:679–688
Hartman MC, Josephson K, Lin CW, Szostak JW (2007) An expanded set of amino acid analogs for the ribosomal translation of unnatural peptides. PLoS ONE 2:e972
Hashem Y, des Georges A, Fu J, Buss SN, Jossinet F, Jobe A, Zhang Q, Liao HY, Grassucci RA, Bajaj C, Westhof E, Madison-Antenucci S, Frank J (2013) High-resolution cryo-electron microscopy structure of the Trypanosoma brucei ribosome. Nature 494:385–389
Hassouna N, Michot B, Bachellerie JP (1984) The complete nucleotide sequence of mouse 28S rRNA gene. Implications for the process of size increase of the large subunit rRNA in higher eukaryotes. Nucleic Acids Res 12:3563–3583
Hazen RM, Ferry JM (2010) Mineral evolution: mineralogy in the fourth dimension. Elements 6:9–12
Higgs PG, Lehman N (2015) The RNA world: molecular cooperation at the origins of life. Nat Rev Genet 16:7–17
Hiller DA, Strobel SA (2011) The chemical versatility of RNA. Philos Trans R Soc Lond B Biol Sci 366:2929–2935
Holzmann J, Frank P, Loffler E, Bennett KL, Gerner C, Rossmanith W (2008) RNase P without RNA: identification and functional reconstitution of the human mitochondrial tRNA processing enzyme. Cell 135:462–474
Hsiao C, Williams LD (2009) A recurrent magnesium-binding motif provides a framework for the ribosomal peptidyl transferase center. Nucleic Acids Res 37:3134–3142
Hsiao C, Mohan S, Kalahar BK, Williams LD (2009) Peeling the onion: ribosomes are ancient molecular fossils. Mol Biol Evol 26:2415–2425
Hsiao C, Chou I-C, Okafor CD, Bowman JC, O’Neill EB, Athavale SS, Petrov AS, Hud NV, Wartell RM, Harvey SC, Williams LD (2013a) Iron(II) plus RNA can catalyze electron transfer. Nat Chem 5:525–528
Hsiao C, Lenz TK, Peters JK, Fang PY, Schneider DM, Anderson EJ, Preeprem T, Bowman JC, O’Neill EB, Lie L, Athavale SS, Gossett JJ, Trippe C, Murray J, Petrov AS, Wartell RM, Harvey SC, Hud NV, Williams LD (2013b) Molecular paleontology: a biochemical model of the ancestral ribosome. Nucleic Acids Res 41:3373–3385
Hud NV, Cafferty BJ, Krishnamurthy R, Williams LD (2013) The origin of RNA and “my grandfather’s axe”. Chem Biol 20:466–474
Jacob F (1977) Evolution and tinkering. Science 196:1161–1166
Jeffares DC, Poole AM, Penny D (1998) Relics from the RNA world. J Mol Evol 46:18–36
Jenner L, Romby P, Rees B, Schulze-Briese C, Springer M, Ehresmann C, Ehresmann B, Moras D, Yusupova G, Yusupov M (2005) Translational operator of mRNA on the ribosome: how repressor proteins exclude ribosome binding. Science 308:120–123
Jenner L, Melnikov S, de Loubresse NG, Ben-Shem A, Iskakova M, Urzhumtsev A, Meskauskas A, Dinman J, Yusupova G, Yusupov M (2012) Crystal structure of the 80S yeast ribosome. Curr Opin Struct Biol 22:759–767
Jones TE, Alexander RW, Pan T (2011) Misacylation of specific nonmethionyl trnas by a bacterial methionyl-tRNA synthetase. Proc Natl Acad Sci USA 108:6933–6938
Kang TJ, Suga H (2008) Ribosomal synthesis of nonstandard peptides. Biochem Cell Biol 86:92–99
Kaufman RJ (2004) Regulation of mRNA translation by protein folding in the endoplasmic reticulum. Trends Biochem Sci 29:152–158
Khaitovich P, Mankin AS, Green R, Lancaster L, Noller HF (1999) Characterization of functionally active subribosomal particles from Thermus aquaticus. Proc Natl Acad Sci USA 96:85–90
Khorana HG (1965) Polynucleotide synthesis and the genetic code. Fed Proc 24:1473–1487
Klein DJ, Schmeing TM, Moore PB, Steitz TA (2001) The kink-turn: a new RNA secondary structure motif. EMBO J 20:4214–4221
Klein DJ, Moore PB, Steitz TA (2004) The contribution of metal ions to the structural stability of the large ribosomal subunit. RNA 10:1366–1379
Knight RD, Freeland SJ, Landweber LF (2001a) Rewiring the keyboard: Evolvability of the genetic code. Nat Rev Genet 2:49–58
Knight RD, Landweber LF, Yarus M (2001b) How mitochondria redefine the code. J Mol Evol 53:299–313
Koonin EV (2014) The origins of cellular life. Antonie Van Leeuwenhoek Int J General Mol Microbiol 106:27–41
Kruger K, Grabowski PJ, Zaug AJ, Sands J, Gottschling DE, Cech TR (1982) Self-splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequence of tetrahymena. Cell 31:147–157
Krupkin M, Matzov D, Tang H, Metz M, Kalaora R, Belousoff MJ, Zimmerman E, Bashan A, Yonath A (2011) A vestige of a prebiotic bonding machine is functioning within the contemporary ribosome. Philos Trans R Soc Lond B Biol Sci 366:2972–2978
Ledoux S, Uhlenbeck OC (2008) Different aa-trnas are selected uniformly on the ribosome. Mol Cell 31:114–123
Letunic I, Bork P (2011) Interactive tree of life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39:W475–478
Leung EK, Suslov N, Tuttle N, Sengupta R, Piccirilli JA (2011) The mechanism of peptidyl transfer catalysis by the ribosome. Annu Rev Biochem 80:527–555
Li L, Francklyn C, Carter CW Jr (2013) Aminoacylating urzymes challenge the RNA world hypothesis. J Biol Chem 288:26856–26863
Lu Y, Freeland S (2006) On the evolution of the standard amino-acid alphabet. Genome Biol 7:102
Machado CA, Robbins N, Gilbert MT, Herre EA (2005) Critical review of host specificity and its coevolutionary implications in the fig/fig-wasp mutualism. Proc Natl Acad Sci USA 102(Suppl 1):6558–6565
McCutcheon JP, McDonald BR, Moran NA (2009) Origin of an alternative genetic code in the extremely small and gc-rich genome of a bacterial symbiont. PLoS Genet 5:e1000565
Mears JA, Cannone JJ, Stagg SM, Gutell RR, Agrawal RK, Harvey SC (2002) Modeling a minimal ribosome based on comparative sequence analysis. J Mol Biol 321:215–234
Melnikov S, Ben-Shem A, Garreau de Loubresse N, Jenner L, Yusupova G, Yusupov M (2012) One core, two shells: bacterial and eukaryotic ribosomes. Nat Struct Mol Biol 19:560–567
Michot B, Bachellerie JP (1987) Comparisons of large subunit rRNAs reveal some eukaryote-specific elements of secondary structure. Biochimie 69:11–23
Michot B, Qu L-H, Bachellerie J-P (1990) Evolution of large-subunit rRNA structure. Eur J Biochem 188:219–229
Mondragon A (2013) Structural studies of RNase P. Annu Rev Biophys 42:537–557
Neveu M, Kim HJ, Benner SA (2013) The “strong” RNA world hypothesis: fifty years old. Astrobiology 13:391–403
Nissen P, Hansen J, Ban N, Moore PB, Steitz TA (2000) The structural basis of ribosome activity in peptide bond synthesis. Science 289:920–930
Noller HF, Kop J, Wheaton V, Brosius J, Gutell RR, Kopylov AM, Dohme F, Herr W, Stahl DA, Gupta R, Woese CR (1981) Secondary structure model for 23S ribosomal RNA. Nucleic Acids Res 9:6167–6189
Ohta A, Murakami H, Suga H (2008) Polymerization of alpha-hydroxy acids by ribosomes. ChemBioChem 9:2773–2778
Olsen GJ, Woese CR (1993) Ribosomal RNA: A key to phylogeny. FASEB J. 7:113–123
Orgel LE (1968) Evolution of the genetic apparatus. J Mol Biol 38:381–393
Pauling L (1946) Molecular architecture and biological reactions. Chem Eng News 24:1375–1377
Petrov AS, Bernier CR, Hershkovitz E, Xue Y, Waterbury CC, Grover MA, HS C, Hud NV, Wartell RM, Williams LD (2013) Secondary structure and domain architecture of the 23S rRNA. Nucleic Acids Res 41:7522–7535
Petrov AS, Bernier CR, Gulen B, Waterbury CC, Hershkovitz E, Hsiao C, Harvey SC, Hud NV, Fox GE, Wartell RM, Williams LD (2014a) Secondary structures of rRNAs from all three domains of life. PLoS ONE 9:e88222
Petrov AS, Bernier CR, Hsiao C, Norris AM, Kovacs NA, Waterbury CC, Stepanov VG, Harvey SC, Fox GE, Wartell RM, Hud NV, Williams LD (2014b) Evolution of the ribosome at atomic resolution. Proc Natl Acad Sci USA 111:10251–10256
Poole AM, Jeffares DC, Penny D (1998) The path from the RNA world. J Mol Evol 46:1–17
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The silva ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596
Rabl J, Leibundgut M, Ataide SF, Haag A, Ban N (2011) Crystal structure of the eukaryotic 40S ribosomal subunit in complex with initiation factor 1. Science 331:730–736
Rich A (1962) On the problems of evolution and biochemical information transfer. In: Kasha M, Pullman B (eds) Horizons in biochemistry. Academic, New York, pp 103–126
Roberts E, Sethi A, Montoya J, Woese CR, Luthey-Schulten Z (2008) Molecular signatures of ribosomal evolution. Proc Natl Acad Sci USA 105:13953–13958
Robertson MP, Ellington AD (2000) Design and optimization of effector-activated ribozyme ligases. Nucleic Acids Res 28:1751–1759
Robertson MP, Joyce GF (2012) The origins of the RNA world. Cold Spring Harb Perspect Biol 4(5):a003608
Robertson MP, Joyce GF (2014) Highly efficient self-replicating RNA enzymes. Chem Biol 21:238–245
Robertus JD, Kraut J, Alden RA, Birktoft JJ (1972) Subtilisin: a stereochemical mechanism involving transition-state stabilization. Biochemistry 11:4293–4303
Rodnina MV, Beringer M, Wintermeyer W (2007) How ribosomes make peptide bonds. Trends Biochem Sci 32:20–26
Roesser JR, Chorghade MS, Hecht SM (1986) Ribosome-catalyzed formation of an abnormal peptide analog. Biochemistry 25:6361–6365
Schimmel P (2008) Development of tRNA synthetases and connection to genetic code and disease. Protein Sci 17:1643–1652
Schmeing TM, Ramakrishnan V (2009) What recent ribosome structures have revealed about the mechanism of translation. Nature 461:1234–1242
Schmitt-Kopplin P, Gabelica Z, Gougeon RD, Fekete A, Kanawati B, Harir M, Gebefuegi I, Eckel G, Hertkorn N (2010) High molecular diversity of extraterrestrial organic matter in murchison meteorite revealed 40 years after its fall. Proc Natl Acad Sci USA 107:2763–2768
Schroeder GK, Wolfenden R (2007) The rate enhancement produced by the ribosome: an improved model. Biochemistry 46:4037–4044
Sczepanski JT, Joyce GF (2014) A cross-chiral RNA polymerase ribozyme. Nature 515:440–442
Seelig B, Jaschke A (1999) A small catalytic RNA motif with diels-alderase activity. Chem Biol 6:167–176
Selmer M, Dunham CM, Murphy FV, Weixlbaumer A, Petry S, Kelley AC, Weir JR, Ramakrishnan V (2006) Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313:1935–1942
Sharma MR, Koc EC, Datta PP, Booth TM, Spremulli LL, Agrawal RK (2003) Structure of the mammalian mitochondrial ribosome reveals an expanded functional role for its component proteins. Cell 115:97–108
Sharma MR, Booth TM, Simpson L, Maslov DA, Agrawal RK (2009) Structure of a mitochondrial ribosome with minimal RNA. Proc Natl Acad Sci USA 106:9637–9642
Shechner DM, Bartel DP (2011) The structural basis of RNA-catalyzed RNA polymerization. Nat Struct Mol Biol 18:1036–1042
Sievers A, Beringer M, Rodnina MV, Wolfenden R (2004) The ribosome as an entropy trap. Proc Natl Acad Sci USA 101:7897–7901
Silverman SK, Begley TP (2007) Nucleic acid enzymes (ribozymes and deoxyribozymes): in vitro selection and application Wiley encyclopedia of chemical biology. Wiley, New York
Simonovic M, Steitz TA (2009) A structural view on the mechanism of the ribosome-catalyzed peptide bond formation. Biochim Biophys Acta 1789:612–623
Smith TF, Lee JC, Gutell RR, Hartman H (2008) The origin and evolution of the ribosome. Biol. Direct 3:16
Stadler PF, Stephens CR (2003) Landscapes and effective fitness. Comm Theor Biol 8:389–431
Stallings W (2005) Operating systems, internals and design principles chemical computing group. Quebec
Steitz TA (2008) A structural understanding of the dynamic ribosome machine. Nat Rev Mol Cell Biol 9:242–253
Subtelny AO, Hartman MC, Szostak JW (2008) Ribosomal synthesis of n-methyl peptides. J Am Chem Soc 130:6131–6136 Epub 2008 Apr 6111
Szostak JW, Bartel DP, Luisi PL (2001) Synth Life. Nature 409:387–390
Tan ZP, Forster AC, Blacklow SC, Cornish VW (2004) Amino acid backbone specificity of the Escherichia coli translation machinery. J Am Chem Soc 126:12752–12753
Trappl K, Polacek N (2011) The ribosome: a molecular machine powered by RNA. Met Ions Life Sci 9:253–275
Vaidya N, Manapat ML, Chen IA, Xulvi-Brunet R, Hayden EJ, Lehman N (2012) Spontaneous network formation among cooperative RNA replicators. Nature 491:72–77
Velculescu VE, Zhang L, Zhou W, Vogelstein J, Basrai MA, Bassett DE Jr, Hieter P, Vogelstein B, Kinzler KW (1997) Characterization of the yeast transcriptome. Cell 88:243–251
Victorova LS, Kotusov VV, Azhaev AV, Krayevsky AA, Kukhanova MK, Gottikh BP (1976) Synthesis of thioamide bond catalyzed by E. coli ribosomes. FEBS Lett 68:215–218
Voss NR, Gerstein M, Steitz TA, Moore PB (2006) The geometry of the ribosomal polypeptide exit tunnel. J Mol Biol 360:893–906
Walker SI, Grover MA, Hud NV (2012) Universal sequence replication, reversible polymerization and early functional biopolymers: a model for the initiation of prebiotic sequence evolution. PLoS ONE 7:e34166
Warner JR (1999) The economics of ribosome biosynthesis in yeast. Trends Biochem Sci 24:437–440
Warshel A, Narayszabo G, Sussman F, Hwang JK (1989) How do serine proteases really work? Biochemistry 28:3629–3637
Watanabe K (2010) Unique features of animal mitochondrial translation systems. The non-universal genetic code, unusual features of the translational apparatus and their relevance to human mitochondrial diseases. Proc Jpn Acad Ser B Phys Biol Sci 86:11–39
Wiltrout E, Goodenbour JM, Frechin M, Pan T (2012) Misacylation of tRNA with methionine in Saccharomyces cerevisiae. Nucleic Acids Res 40:10494–10506
Wimberly BT, Brodersen DE, Clemons WM Jr, Morgan-Warren RJ, Carter AP, Vonrhein C, Hartsch T, Ramakrishnan V (2000) Structure of the 30S ribosomal subunit. Nature 407:327–339
Wochner A, Attwater J, Coulson A, Holliger P (2011) Ribozyme-catalyzed transcription of an active ribozyme. Science 332:209–212
Woese CR (1967) Personal communication to francis crick (1967)
Woese CR (2000) Interpreting the universal phylogenetic tree. Proc Natl Acad Sci USA 97:8392–8396
Woese CR (2001) Translation: in retrospect and prospect. RNA 7:1055–1067
Woese CR (2002) On the evolution of cells. Proc Natl Acad Sci USA 99:8742–8747
Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 74:5088–5090
Woese CR, Magrum LJ, Gupta R, Siegel RB, Stahl DA, Kop J, Crawford N, Brosius J, Gutell R, Hogan JJ, Noller HF (1980) Secondary structure model for bacterial 16S ribosomal RNA: phylogenetic, enzymatic and chemical evidence. Nucleic Acids Res 8:2275–2293
Wolf YI, Koonin EV (2007) On the origin of the translation system and the genetic code in the RNA world by means of natural selection, exaptation, and subfunctionalization. Biol Direct 2:14
Zimmermann R, Eyrisch S, Ahmad M, Helms V (2011) Protein translocation across the ER membrane. Biochim Biophys Acta 1808:912–924
Acknowledgments
We thank Drs. Harold Bernhardt, Eric Gaucher, Anton Petrov, Anthony Poole and Roger Wartell for helpful discussion. This work was supported by the NASA Astrobiology Institute.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Bowman, J.C., Hud, N.V. & Williams, L.D. The Ribosome Challenge to the RNA World. J Mol Evol 80, 143–161 (2015). https://doi.org/10.1007/s00239-015-9669-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00239-015-9669-9