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Origins and Early Evolution of the Ribosome

  • George E. FoxEmail author
Chapter

Abstract

The modern ribosomal machinery is very complex, and its core subsystems and many of its individual components are universally found in all three domains of life. This indicates that much of the story of ribosome origins and its subsequent evolution predates the last universal common ancestor (LUCA). Thus, ribosome history relates to other early life issues such as the possibility and nature of an RNA World, the early history of chirality, and always most hopefully the origins of the genetic code. However, this is not the end of the story. As discussed elsewhere in this volume, important events have also occurred since the LUCA, especially in eukaryotic ribosomes that have served to integrate the machinery with other cellular systems. Ribosome origins and subsequent evolution are in reality somewhat separate problems. In addressing the former, this chapter initially examines the source and nature of the peptidyl transferase center (PTC), including where and how the peptide bond is made. This is followed by efforts to understand the subsequent evolution of the ribosome, which led to the addition and refinement of various other functional centers including the decoding center. This is being accomplished using what is in essence a reverse engineering approach to develop a timeline of major events in the ribosome history. Finally, significant events on the timeline are discussed in detail.

Keywords

Ribosomal Protein Peptide Bond Formation Exit Tunnel Peptidyl Transferase Center Accretion Model 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Noller HF. Evolution of protein synthesis from an RNA World. Cold Spring Harb Perspect Biol. 2010;4:a003681.Google Scholar
  2. 2.
    Ban N, Nissen P, Hansen J, Moore PB, Steitz TA. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science. 2000;2000(289):905–20.CrossRefGoogle Scholar
  3. 3.
    Nissen P, Hansen J, Ban N, Moore PB, Steitz TA. The structural basis of ribosome activity in peptide bond synthesis. Science. 2000;289:920–30.CrossRefPubMedGoogle Scholar
  4. 4.
    Maguire BA, Beniaminov AD, Ramu H, Mankin AS, Zimmermann RA. A protein component at the heart of an RNA machine: the importance of protein l27 for the function of the bacterial ribosome. Mol Cell. 2005;20:427–35.CrossRefPubMedGoogle Scholar
  5. 5.
    Selmer M, Dunham CM, Murphy FV 4th, Weixlbaumer A, Petry S, Kelley AC, Weir JR, Ramakrishnan V. Structure of the 70S ribosome complexed with mRNA and tRNA. Science. 2006;313:1935–42.CrossRefPubMedGoogle Scholar
  6. 6.
    Wower IK, Wower J, Zimmermann RA. Ribosomal protein L27 participates in both 50 S subunit assembly and the peptidyl transferase reaction. J Biol Chem. 1998;273:19847–52.CrossRefPubMedGoogle Scholar
  7. 7.
    Maracci C, Wohlgemuth I, Rodnina MV. Activities of the peptidtl transferase center of ribosomes lacking protein L27. RNA. 2015;21:1–6.CrossRefGoogle Scholar
  8. 8.
    White HB III. Coenzymes as fossils of an earlier metabolic state. J Mol Evol. 1976;1976(7):101–4.CrossRefGoogle Scholar
  9. 9.
    Yarus M. Getting past the RNA World: The initial Darwinian Ancestor. Cold Spring Harb Perspect Biol. 2010;3:a003590.Google Scholar
  10. 10.
    Bartel DP, Szostak JW. Isolation of new ribozymes from a large pool of random sequences. Science. 1993;261:1411–8.CrossRefPubMedGoogle Scholar
  11. 11.
    Zaher HS, Unrau PJ. Selection of an improved RNA polymerase ribozyme with superior extension and fidelity. RNA. 2007;13:1017–26.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Attwater J, Wochner A, Holliger P. In-ice evolution of RNA polymerase ribozyme activity. Nat Chem. 2013;5:1011–8.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Mutswchler H, Wochner A, Hollinger P. Freeze-thaw cycles as drivers of complex ribozyme assembly. Nat Chem. 2015;7:502–8.CrossRefGoogle Scholar
  14. 14.
    Wolf YI, Koonin EV. 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. 2007;2:14.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Zhang B, Cech TR. Peptide bond formation by in vitro selected ribozymes. Nature. 1997;1997(390):96–100.Google Scholar
  16. 16.
    Lilley DM. The origins of RNA catalysis in ribozymes. Trends Biochem Sci. 2003;28:495–501.CrossRefPubMedGoogle Scholar
  17. 17.
    Bowman JC, Hud NV, Williams LD. The ribosome challenge to the RNA World. J Mol Evol. 2015;80:143–61.CrossRefPubMedGoogle Scholar
  18. 18.
    Cafferty BJ, Hud NV. Abiotic synthesis of RNA in water: a common goal of prebiotic chemistry and bottom-up synthetic biology. Curr Opin Chem Biol. 2014;22:146–57.CrossRefPubMedGoogle Scholar
  19. 19.
    Sczepanski JT, Joyce GF. A cross-chiral RNA polymerase ribozyme. Nature. 2014;515: 440–2.Google Scholar
  20. 20.
    Van der Gulik P, Massar S, Gilis D, Buhrman H, Rooman M. The first peptides: the evolutionary transition between prebiotic amino acids and early proteins. J Theor Biol. 2009;261:531–9.CrossRefPubMedGoogle Scholar
  21. 21.
    Ferris JP, Hill WR Jr, Rihe L, Orgel LE. Synthesis of long prebiotic oligomers on mineral surfaces. Nature. 1996;381:59–61.CrossRefPubMedGoogle Scholar
  22. 22.
    Stachelhaus T, Marahiel MA. Modular structure of genes encoding multifunctional peptide synthetases required for non-ribosomal peptide synthesis. FEMS Microbiol Lett. 1995;125:3–14.CrossRefPubMedGoogle Scholar
  23. 23.
    Marahiel MA. Working outside the protein-synthesis rules: insights into non-ribosomal peptide synthesis. J Peptide Sci. 2009;15:799–807.CrossRefGoogle Scholar
  24. 24.
    Nagaswamy U, Fox GE. RNA ligation and the origin of tRNA. Orig Life Evol Biosph. 2003;33:199–209.CrossRefPubMedGoogle Scholar
  25. 25.
    Agmon I. The dimeric proto-ribosome: Structural details and possible implications on the origin of life. Int J Mol Sci. 2009;2009(10):2921–34.CrossRefGoogle Scholar
  26. 26.
    Davidovich C, Belousoff M, Wekselman I, Shapira T, Krupkin M, Zimmerman E, Bashan A, Yonath A. The proto-ribosome: an ancient nano-machine for peptide bond formation. Isr J Chem. 2010;50:29–35.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Krupkin M, Matzov D, Tang H, Metz M, Kalaora R, Belousoff MJ, Zimmerman E, Bashan A, Yonath A. A vestige of a prebiotic bonding machine is functioning within the contemporary ribosome. Philos Tran R Soc Lond B Biol Sci. 2011;366:2972–8.CrossRefGoogle Scholar
  28. 28.
    Boer PH, Gray MW. Scambled ribosomal RNA gene pieces in Chlamydomonas reinhardtii mitochondrial DNA. Cell. 1988;55:399–411.CrossRefPubMedGoogle Scholar
  29. 29.
    Schnare MN, Gray MW. Sixteen discrete RNA components in the cytoplasmic ribosome of Euglena gracilis. J Mol Biol. 1990;215:73–83.CrossRefPubMedGoogle Scholar
  30. 30.
    Polacek N, Mankin AS. The ribosomal peptidyl transferase center: Structure, function, evolution, inhibition. Crit Rev Biochem Mol Biol. 2005;40:285–311.CrossRefPubMedGoogle Scholar
  31. 31.
    Katunin VI, Muth GW, Strobel SA, Wintermeyer W, Rodnina MV. Important contribution to catalysis of peptide bond formation by a single ionizing group within the ribosome. Mol Cell. 2002;10:339–46.CrossRefPubMedGoogle Scholar
  32. 32.
    Sievers A, Beringer M, Rodnina MV, Wolfenden R. The ribosome as an entropy trap. Proc Natl Acad Sci USA. 2004;101:7897–901.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Schroeder GK, Wolfenden R. The rate enhancement produced by the ribosome: an improved model. Biochemistry. 2007;46:4037–44.CrossRefPubMedGoogle Scholar
  34. 34.
    Moore PB, Steitz TA. After the ribosome structures: How does peptidyl transferase work? RNA. 2001;9:155–9.CrossRefGoogle Scholar
  35. 35.
    Wohlgemuth I, Beringer M, Rodnina MV. Rapid peptide bond formation on isolated 50S ribosomal subunits. EMBO reports. 2006;7:699–703.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Rodina MV, Beringer M, Wintermeyer W. How ribosomes make peptide bonds. Trends Biochem Sci. 2007;32:20–6.CrossRefGoogle Scholar
  37. 37.
    Zaher HS, Shaw JJ, Strobel SA, Green R. The 2’-OH group of the peptidyl-tRNA stabilizes an active conformation of the ribosomal PTC. EMBO J. 2011;30:2445–53.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Carrasco N, Hiller DA, Strobel SA. Minimal transition state charge stabilization of the oxyanion during peptide bond formation by the ribosome. Biochemistry. 2011;50:10491–8.CrossRefPubMedGoogle Scholar
  39. 39.
    Świderek K, Marti S, Tuñón I, Moliner V, Bertran J. Peptide bond formation mechanism catalyzed by ribosome. J Am Chem Soc. 2015;137:12024–34.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Fahnestock S, Rich A. Ribosome-catalyzed polyester formation Science. 1971;173:340–3.PubMedGoogle Scholar
  41. 41.
    Fahnestock S, Neumann H, Shashoua V, Rich A. Ribosome catalyzed ester formation. Biochemistry. 1970;9:2477–83.CrossRefPubMedGoogle Scholar
  42. 42.
    Victorova LS, Kotusov VV, Azhaev AV, Krayevsky AA, Kukhanova MK, Gottikh BP. Synthesis of thioamide bond catalyzed by E. coli ribosomes. FEBS Lett. 1976;68:215–8.CrossRefPubMedGoogle Scholar
  43. 43.
    Ohta A, Murakami H, Suga H. Polymerization of alpha-hydroxy acids by ribosomes. Chem Bio Chem. 2008;9:2773–8.CrossRefPubMedGoogle Scholar
  44. 44.
    Subtelny AO, Hartman MC, Szostak JW. Ribosomal synthesis of n-methyl peptides. J Am Chem Soc. 2008;130:6131–6.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Tan Z, Forster AC, Blacklow SC, Cornish VW. Amino acid backbone specificity of the Escherichia coli translation machinery. J Am Chem Soc. 2004;126:12752–3.CrossRefPubMedGoogle Scholar
  46. 46.
    Hartman MC, Josephson K, Lin CW, Szostak JW. An expanded set of amino acids analogs for the ribosomal translation of unnatural peptides. PLoS ONE. 2007;2:e972.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Kang TJ, Suga H. Ribosomal synthesis of nonstandard peptides. Biochem Cell Biol. 2008;86:92–9.CrossRefPubMedGoogle Scholar
  48. 48.
    Zavialov AV, Mora L, Buckingham RH, Ehrenberg M. Release of peptide promoted by the GGQ motif of class 1 release factors regulates the GTPase activity of RF3. Mol Cell. 2002;10:789–98.CrossRefPubMedGoogle Scholar
  49. 49.
    Fox GE, Tran Q. Yonath. An exit cavity was crucial to the polymerase activity of the early ribosome. Astrobiology. 2012;12:57–60.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Nakatogawa H, Ito K. The ribosomal exit tunnel functions as a discriminating gate. Cell. 2002;108:629–36.CrossRefPubMedGoogle Scholar
  51. 51.
    Lu J, Deutsch C. Folding zones inside the ribosomal exit tunnel. Nat Struct Mol Biol. 2005;12:1123–9.CrossRefPubMedGoogle Scholar
  52. 52.
    Yonath A. Antibiotics targeting ribosomes: resistance, selectivity, synergism and cellular regulation. Annu. Rev. Biochem. 2005;74:649–79.CrossRefPubMedGoogle Scholar
  53. 53.
    Ito K, Chiba S, Pogliano K. Divergent stalling sequences sense and control cellular physiology. Biochem Biophys Res Commun. 2010;393:1–5.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Ranu H, Mankin A, Vazquez-Laslop N. Programmed drug-dependent ribosome stalling. Mol Microbiol. 2009;71:811–24.CrossRefGoogle Scholar
  55. 55.
    Ramu H, Vazquez-Laslop N, Klepacki D, Dai Q, Piccrilli J, Micura R, Mankin AS. Nascent peptide in the ribosome exit tunnel affects functional properties of the A-site of the peptidyl transferase center. Mol Cell. 2011;41:321–30.CrossRefPubMedGoogle Scholar
  56. 56.
    Chiba S, Kanamori T, Ueda T, Akiyama Y, Pogliano K, Ito K. Recruitment of a species-specific translational arrest module to monitor different cellular processes. Proc Natl Acad Sci USA. 2011;108:6073–8.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Turk RM, Illangasekare M, Yarus M. Catalyzed and spontaneous reactions on ribozyme ribose. J Am Chem Soc. 2011;133:6044–50.CrossRefPubMedGoogle Scholar
  58. 58.
    Schaul S, Berel D, Benjamini Y, Graur D. Revisiting the operational code for amino acids: Ensemble attributes and their implications. RNA. 2010;16:141–53.CrossRefGoogle Scholar
  59. 59.
    Schimmel P, Giege R, Moras D, Yokoyama S. An operational RNA code for amino acids and possible relationship to genetic code. Proc Natl Acad Sci USA 1993;90:8763–8.Google Scholar
  60. 60.
    Schimmel P. Ribas de Pouplana L. Transfer RNA: From Minihelix to Genetic Code. Cell. 1995;81:983–6.CrossRefPubMedGoogle Scholar
  61. 61.
    Francklyn C, Schimmel P. Aminoacylation of RNA minihelices with alanine. Nature. 1989;337:478–81.CrossRefPubMedGoogle Scholar
  62. 62.
    Francklyn C, Schimmel P. Enzymatic aminoacylation of an eight base pair mivrohelix with histidine. Proc Natl Acad Sci USA. 1990;87:8655–9.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Kleine DJ, Moore PB, Steitz TA. The contribution of metal ions to the structural stability of the large ribosomal subunit. RNA. 2004;10:1366–79.CrossRefGoogle Scholar
  64. 64.
    Hsiao C, Mohan S, Kalahar BK, Williams LD. Peeling the Onion: ribosomes are ancient molecular fossils. Mol Biol Evol. 2009;26:2415–25.CrossRefPubMedGoogle Scholar
  65. 65.
    Hsiao C, Chou IC, Okafor CD, Bowman JC, O’Neill EB, Athavale SS, Petrov AS, Hud NV, Wartell RM, Harvey SC, Williams LD. RNA with iron (II) as a cofactor catalyzes electron transfer. Nat Chem. 2013;5:525–8.CrossRefPubMedGoogle Scholar
  66. 66.
    Huang L, Krupkin M, Bashan A, Yonath A, Massa L. Protoribosome by quantum kernel energy method. Proc Natl Acad Sci USA. 2013;110:14900–5.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Rivas M, Tran Q, Fox GE. Nanometer scale pores similar in size to the entrance of the ribosomal exit cavity are a common feature of large RNAs. RNA. 2013;19:1349–54.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Mears JA, Cannone JJ, Stagg SM, Gutell RR, Agrawal RK, Harvey SC. Modeling a minimal ribosome based on comparative sequence analysis. J Mol Biol. 2002;321:215–34.CrossRefPubMedGoogle Scholar
  69. 69.
    Gray MW, Schnare MN. Evolution of RNA gene organization. In: Zimmermann RA, Dahlberg AE, editors. Ribosomal RNA—Structure, evolution, processing, and function in protein synthesis. Boca Raton, Florida: CRC Press; 1996. p. 49–69.Google Scholar
  70. 70.
    Hury J, Nagaswamy U, Larios-Sanz M, Fox GE. Ribosome origins: The relative age of 23S rRNA domains. Orig Life Evol Biosphere. 2006;36:421–9.CrossRefGoogle Scholar
  71. 71.
    Bokov K, Steinberg SV. A hierarchical model for evolution of 23S ribosomal RNA. Nature. 2009;457:977–80.CrossRefPubMedGoogle Scholar
  72. 72.
    Nissen P, Lppolito JA, Ban N, Moore PB, Steitz TA. RNA tertiary interactions in the large ribosomal subunit: the A-minor motif. Proc Natl Acad Sci USA. 2001;98:4899–903.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Réblová K, Šponer JE, Špačková N, Beššeová I, Šponer J. A-minor tertiary interactions in RNA kink-turns. Molecular dynamics and quantum chemical analysis. J Phys Chem B. 2011;115:13897–910.CrossRefPubMedGoogle Scholar
  74. 74.
    Gerbi SA. Expansion segments: Regions of variable size that interrupt the universal core secondary structure of ribosomal RNA. In: Zimmermann RA, Dahlberg AE, editors. Ribosomal RNA—Structure, evolution, processing, and function in protein synthesis. Boca Raton, Florida: CRC Press; 1996. p. 71–87.Google Scholar
  75. 75.
    Gerbi SA. Evolution of ribosomal DNA. In: MacIntyee RJ, editor. Molecular evolutionary genetics. New York: Plenum Publishing Corporation; 1985. p. 419–51774.CrossRefGoogle Scholar
  76. 76.
    Luehrsen KR, Nicholson DE, Eubanks DC, Fox GE. An archaebacterial 5S rRNA contains a long insertion sequence. Nature. 1981;293:755–7.CrossRefPubMedGoogle Scholar
  77. 77.
    Petrov AS, Bernier CR, Hsiao C, Norris AM, Kovacs NA, Waterbury CC, Stepanov VG, Harvey SC, Fox GE, Wartell RM, Hud NV, Williams LD. Evolution of the ribosome at atomic resolution. Proc Natl Acad Sci USA. 2014;111:10251–6.CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Caisova L, Melkonian M. Evolution of helix formation in the ribosome internal transcribed spacer 2 (ITS2) and its significance for RNA secondary structures. J Mol Evol. 2014;78:324–7.CrossRefPubMedGoogle Scholar
  79. 79.
    Petrov AS, Bernier CR, Gulen B, Waterbury CC, Hershkovits E, Hsiao C, Harvey SC, Hud NV, Fox GE, Wartell RM, Williams LD. Secondary structures of tRNAs from all three domains of life. PLoS One. 2014;9:e88222.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Ban N, Beckmann R, Cate JH, Dinman JD, Dragon F, Ellis SR, Lafontaine DL, Lindahl L, Liljas A, Lipton JM, McAlear MA, Moore PB, Noller HF, Ortega J, Panse VG, Ramakrishnan V, Spahn CM, Steitz TA, Tchorzewski M, Tollervey D, Warren AJ, Williamson JR, Wilson D, Yonath A, Yusupov M. A new system for naming ribosomal proteins. Curr Opin Struct Biol. 2014;24:165–9.CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Petrov AS, Gulen B, Norris A, Kovacs NA, Bernier CR, Lanier KA, Fox GE, Harvey SC, Wartell RM, Hud NV, Williams LD. The history of the ribosome and the origin of translation. Proc. Natl. Acad Sci USA. 2015;112:15396–401.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Caetano-Anollés G. Tracing the evolution of RNA structure in ribosomes. Nucl Acids Res. 2002;30:2575–87.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Harish A, Caetano-Anollés G. Ribosomal history reveals origins of modern protein synthesis. PLoS One. 2012;7:e32776.CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Petrov AS, Williams LD. The ancient heart of the ribosomal large subunit: a response to Caetano-Anollés. J Mol Evol. 2015;80:166–70.CrossRefPubMedGoogle Scholar
  85. 85.
    Caetano-Anollés D, Caetano-Anollés G. Ribosomal accretion aprioism and the phylogenetic method: A response to Petrov and Williams. Front Genet. 2015;6:194.PubMedPubMedCentralGoogle Scholar
  86. 86.
    Caetano-Anollés G. Ancestral insertions and expansions of rRNA do not support an origin of the ribosome in its peptidyl transferase center. J Mol Evol. 2015;80:162–5.CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Smith TF, Gutell R, Lee J, Hartmann H. The origin and evolution of the ribosome. Biol Direct. 2008;3:16.CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Campbell J. An RNA repisome as the ancestor of the ribosome. J Mol Evol. 1991;32:3–5.CrossRefPubMedGoogle Scholar
  89. 89.
    Gordon K. Were RNA replication and translation directly coupled in the RNA (+protein) World? J Theor Biol. 1995;173:179–93.CrossRefPubMedGoogle Scholar
  90. 90.
    Poole AM, Jeffares DC, Penny D. The path from the RNA world. J Mol Evol. 1998;46:1–17.CrossRefPubMedGoogle Scholar
  91. 91.
    Blackmond DG. The origin of biological homochirality. Cold Spring Harb Perspect Biol. 2010;2:a002147.CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Fox GE. Origin and evolution of the ribosome. Cold Spring Harb Perspect Biol. 2010;3:a003483.Google Scholar
  93. 93.
    Yamane T, Miller DL, Hopfield JJ. Discrimination between D and L-tyrosyl transfer ribonucleic acids in peptide chain elongation. Biochemistry. 1981;20:7059–68.CrossRefPubMedGoogle Scholar
  94. 94.
    Heckler TG, Roesser JR, Xu C, Chang PI, Hecht SM. Ribosomal binding and dipeptide formation by misacylated tRNAPhe’s. Biochemistry. 1988;27:7254–62.CrossRefPubMedGoogle Scholar
  95. 95.
    Starck SR, Qi X, Olsen BN, Roberts RW. The puromycin route to assess stero- and regiochemical constraints on peptide bond formation in eukaryotic ribosomes. J Am Chem Soc. 2003;125:8090–1.CrossRefPubMedGoogle Scholar
  96. 96.
    Dedkova LM, Fahmi NE, Golovine SY, Hecht SM. Enhanced D-amino acid incorporation into proteins by modified ribosomes. J Am Chem Soc. 2003;125:6616–7.CrossRefPubMedGoogle Scholar
  97. 97.
    Dedkova LM, Fahmi NE, Golovine SY, Hecht SM. Construction of modified ribosomes for incorporation of D-amino acids into proteins. Biochemistry. 2006;45:15541–51.CrossRefPubMedGoogle Scholar
  98. 98.
    Dedkova LM, Fahmi NE, Paul R, del Rosario M, Zhang L, Chen S, Feder G, Hecht SM. β-Puromycin selection of modified ribosomes for in vitro incorporation of β-amino acids. Biochemistry. 2012;51:401–15.CrossRefPubMedGoogle Scholar
  99. 99.
    Soutourina J, Plateau P, Blanquet S. Metabolism of D-aminoacyl-tRNAs in Eschrichia coli and Saccharomyces cerevisiae cells. J Biol Chem. 2000;275:32535–42.CrossRefPubMedGoogle Scholar
  100. 100.
    Yang H, Zheng G, Peng X, Qiang B, Yuan J. D-amino acids and D-Tyr-tRNAtyr deacylase: Stereospecificity of the translation machine revisited. FEBS Lett. 2008;552:95–8.CrossRefGoogle Scholar
  101. 101.
    Di Giulio M. A comparison among the models proposed to explain the origin of the tRNA molecule: A synthesis. J Mol Evol. 2009;69:1–9.CrossRefPubMedGoogle Scholar
  102. 102.
    Maizels N, Weiner AM. The genomic tag hypothesis: modern viruses as molecular fossils of ancient strategies for genomic replication. In: Gesteland RF. Atkins JF editors. The RNA world, Plainview. New York: Cold Springs Harbor Laboratory Press; 1993. p. 577–602.Google Scholar
  103. 103.
    Maizels N, Weiner AM. Phylogeny from function: evidence from the molecular fossil record that tRNA originated in replication, not translation. Proc Natl Acad Sci USA. 1994;91:6729–34.Google Scholar
  104. 104.
    Di Giulio M. On the origin of the transfer RNA molecule. J Theor Biol. 1992;159:199–214.CrossRefPubMedGoogle Scholar
  105. 105.
    Watanabe Y, Suematsu T, Ohtsuki T. Losing the stem-loop structure From metazoan mitochondrial tRNAs and co-evolution of interacting factors. Front Genet. 2014;5:109.CrossRefPubMedPubMedCentralGoogle Scholar
  106. 106.
    Randau L, Munch R, Hohn M, Jahn D, Soll D. Nanoarchaeum equitans creates functional tRNAs from separate genes for their50- and 30-halves. Nature. 2005;433:537–41.CrossRefPubMedGoogle Scholar
  107. 107.
    Carter CW. What RNA world? Why a peptide/RNA partnership merits renewed experimental attention. Life (Basel). 2015;5:294–320.PubMedPubMedCentralGoogle Scholar
  108. 108.
    Smith TF, Hartman H. The evolution of class II aminoacyl-tRNA synthetases and the first code. FEBS Lett. 2015;589:3499–507.Google Scholar
  109. 109.
    Shine J, Dalgarno L. The 3’-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci USA. 1974;71:1342–6.CrossRefPubMedPubMedCentralGoogle Scholar
  110. 110.
    Bernhardt HS, Tate WP. The transition from noncoded to coded protein synthesis: did coding mRNAs arise from stability-enhancing binding partners to tRNA? Biol Direct. 2012;7:4.CrossRefPubMedPubMedCentralGoogle Scholar
  111. 111.
    Barrell BG, Anderson S, Bankier AT, de Bruijn MH, Chen E, Coulson AR, Drouin J, Eperon IC, Nierlich DP, Roe BA, Sanger F, Schreier PH, Smith AJ, Staden R, Young IG. Different pattern of codon recognition by mammalian mitochondrial tRNAs. Proc Natl Acad Sci USA. 1980;77:3164–6.CrossRefPubMedPubMedCentralGoogle Scholar
  112. 112.
    Temperley R. Richter R, DEnnerlein S, Lightowlers, Chrzanowska-Lightowlers Z. Hungry codons promote frameshifting in human mitcchondrial ribosomes. Science. 2010;327:301.CrossRefPubMedGoogle Scholar
  113. 113.
    Lehman N, Jukes TH. Genetic code development by stop codon takeover. J Theor Biol. 1988;135:203–14.CrossRefPubMedGoogle Scholar
  114. 114.
    Fournier GP, Neumann JE, Gogarten JP. Inferring the ancient history of the translation machinery and genetic code via recapitulation of ribosomal subunit assembly orders. PLoS One. 2010;27:1792–801.Google Scholar
  115. 115.
    Wang J, Dasgupta I, Fox GE. Many nonuniversal archaeal ribosomal proteins are found in conserved gene clusters. Archaea. 2009;2:241–51.CrossRefPubMedPubMedCentralGoogle Scholar
  116. 116.
    Fox GE, Naik AK. The evolutionary history of the translation machinery. In Ribas, de Pouplana L, editor), The genetic code and the origin of genetic code. New York, New York: Springer. US. 2004;2007:92–105.Google Scholar
  117. 117.
    Khaitovich P, Mankin AS, Green R, Lancaster L, Noller HF. Characterization of functionally active subribosomal particles from Thermus aquaticus. Proc Natl Acad Sci USA. 1999;96:85–90.CrossRefPubMedPubMedCentralGoogle Scholar
  118. 118.
    Siefert JL, Fox GE. Conserved gene clusters in bacterial genomes provide further support for the primacy of RNA. J Mol Evol. 1997;45:467–72.CrossRefPubMedGoogle Scholar
  119. 119.
    Joyce GF. RNA evolution and the origins of life. Nature. 1989;338:217–24.CrossRefPubMedGoogle Scholar
  120. 120.
    Murzin AG, Brenner SE, Hubbard T, Chothia C. SCOP: a structural classification of proteins database for the investigation of sequences and structures. J Mol Biol. 1995;247:536–40.PubMedGoogle Scholar
  121. 121.
    Hartman H, Smith TF. The evolution of the ribosome and the genetic code. Life (Basel). 2014;4:227–49.Google Scholar
  122. 122.
    Vishwanath P, Favaretto P, Hartman H, Mohr SC, Smith TF. Ribosomal protein-sequence block structure suggests complex prokaryotic evolution with implications for the origin of eukaryotes. Mol Phylogenet Evol. 2004;33:615–25.CrossRefPubMedGoogle Scholar
  123. 123.
    Agrawal V, Kishan RK. Functional evolution of two subtly different (similar) folds. BMC Struct Biol. 2001;1:5.CrossRefPubMedPubMedCentralGoogle Scholar
  124. 124.
    Cannone JJ, Subramanian S, Schnare MN, Collett JR, D’Souza LM, Du Y, Feng B, Lin N, Madabusi LV, Muller KM, Pande N, Shang Z, Yu N, Gutell RR. The comparative RNA web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics. 2002;3:2.CrossRefPubMedPubMedCentralGoogle Scholar
  125. 125.
    Klein DJ, Moore PB, Steitz TA. The roles of ribosomal proteins in the structure assembly, and evolution of the large ribosomal subunit. J Mol Biol. 2004;340:141–77.CrossRefPubMedGoogle Scholar
  126. 126.
    Spirin AS. Ribosome as a molecular machine. FEBS Lett. 2002;514:2–10.CrossRefPubMedGoogle Scholar
  127. 127.
    Gavrilova LP, Kostiashkina VE, Koteliansky NM, Rutkevich NM, Spirin AS. Factor free (“Non-enzymatic”) and factor-dependent systems of translation of polyuridylic acid by Escherichia coli ribosomes. Mol Biol. 1976;101:537–52.CrossRefGoogle Scholar
  128. 128.
    Frank J, Gonzalez RL Jr. Structure and Dynamics of a processive Brownian motor: the translating ribosome. Annu Rev Biochem. 2010;2010(79):381–412.CrossRefGoogle Scholar
  129. 129.
    Woese C. Molecular mechanics of translation: a reciprocating ratchet mechanism. Nature. 1970;226:817–20.CrossRefPubMedGoogle Scholar
  130. 130.
    Robertus JD, Ladner JE, Finch JT, Rhodes D, Brown RS, Clark BF, Klug A. Structure of yeast phenylalanine tRNA at 3S resolution. Nature. 1974;250:546–51.CrossRefPubMedGoogle Scholar
  131. 131.
    Harvey SC, McCammon JA. Intramolecular flexibility in phenylalanine transfer RNA. Nature. 1981;294:286–7.CrossRefPubMedGoogle Scholar
  132. 132.
    Dunkle JA, Wang L, Feldman MB, Pulk A, Chen VB, Kapral GJ, Noeske J, Richardson JS, Blanchard SC. Cate JH. Structures of the bacterial ribosome in classical and hybrid states of tRNA binding. Science. 2011;332:981–4.CrossRefPubMedPubMedCentralGoogle Scholar
  133. 133.
    Paci M, Fox GE. Major centers of motion in the large ribosomal RNAs. Nucl Acids Res. 2015;43:4640–9.CrossRefPubMedPubMedCentralGoogle Scholar
  134. 134.
    Paci M, Fox GE. Centers of motion associated with EF-Tu binding to the ribosome. RNA Biol. 2016;Jan 19.0 [Epub ahead of print].Google Scholar
  135. 135.
    Moazed D, Robertson JM, Noller HF. Interaction of elongation factors EF-G and EF-Tu with a conserved loop in 23S rRNA. Nature. 1998;334:362–4.CrossRefGoogle Scholar
  136. 136.
    Sergiev PV, Bogdanov AA, Dontsova OA. How can elongation factors EF-G and EF-Tu discriminate the functional state of the ribosome using the same binding site? FEBS Lett. 2005;579:5439–42.CrossRefPubMedGoogle Scholar
  137. 137.
    Fox GE, Paci M, Tran Q, Petrov, Williams LD. Ribosome dynamics and the Evolutionary history of ribosomes. Proceedings SPIE Conference 9606 Instruments, Methods and Missions for Astrobiology XVII 2015: 96060G1-96060G-5.Google Scholar
  138. 138.
    Hoffmann A, Bukau B, Kramer G. Structure and function of the molecular chaperone trigger factor. Biochim Biophys Acta. 2010;1803:650–61.CrossRefPubMedGoogle Scholar
  139. 139.
    Frank J, Gao H, Sengupta J, Gao N, Taylor DJ. The process of mRNA-tRNA translocation. Proc Natl Acad Sci USA. 2007;104:19671–8.CrossRefPubMedPubMedCentralGoogle Scholar
  140. 140.
    Grela P, Bernadó P, Svergun D, Kwiatowski J, Abramczyk D, Grankowski N, Tchórzewski M. Structural relationships among the ribosomal stalk proteins from the three domains of life. J Mol Evol. 2008;67:154–67.CrossRefPubMedGoogle Scholar
  141. 141.
    Szymanski M, Barciszewska MZ, Erdmann VA, Barciszewski J. 5 S rRNA: structure and interactions. Biochem J. 2003;371:641–51.CrossRefPubMedPubMedCentralGoogle Scholar
  142. 142.
    Gongadz GM. 5S rRNA and Ribosome. Biochemistry (Moscow). 2011;76:1450–64.CrossRefGoogle Scholar
  143. 143.
    Dohme F, Nierhaus KH. Role of 5S RNA in assembly and function of the 50S subunit from Escherichia coli. Proc Natl Acad Sci USA. 1976;73:2221–5.CrossRefPubMedPubMedCentralGoogle Scholar
  144. 144.
    Erdmann VA, Fahnestock S, Higo K, Nomura M. Role of 5S RNA in the function of 50S ribosomal subunits. Proc Natl Acad Sci USA. 1971;68:2932–6.CrossRefPubMedPubMedCentralGoogle Scholar
  145. 145.
    Forget BG, Weissman SM. Nucleotide sequence of KB cell 5S RNA. Science. 1967;158:1695–9.CrossRefPubMedGoogle Scholar
  146. 146.
    Dontsova OA, Dinman JD. 5S rRNA: Structure and Function from Head to Toe. Int J Biomed Sci. 2005;1:1–7.PubMedPubMedCentralGoogle Scholar
  147. 147.
    Bogdanov AA, Dontsova OA, Dokudovskaya SS, Lavrik IN. Structure and function of 5S rRNA in the ribosome. Biochem Cell Biol. 1995;73:869–76.CrossRefPubMedGoogle Scholar
  148. 148.
    Dokudovskaya S, Dontsova O, Shpanchenko O, Bogdanov A, Brimacombe R. Loop IV of 5S ribosomal RNA has contacts both to domain II and to domain V of the 23S RNA. RNA. 1996;2:146–52.PubMedPubMedCentralGoogle Scholar
  149. 149.
    Stark H, Rodnina MV, Wieden HJ, Zemlin F, Wintermeyer W, van Heel M. Ribosome interactions of aminoacyl-tRNA and elongation factor Tu in the codon-recognition complex. Nat. Struct Biol. 2002;9:849–54.PubMedGoogle Scholar
  150. 150.
    Hoang L, Fredrick K, Noller HF. Creating ribosomes with an all-RNA 30S subunit P site. Proc Natl Acad Sci USA. 2004;101:12439–43.CrossRefPubMedPubMedCentralGoogle Scholar
  151. 151.
    Fox GE, Woese CR. 5S rRNA secondary structure. Nature. 1975;256:505–7.CrossRefPubMedGoogle Scholar
  152. 152.
    Fox GE, Woese CR. The architecture of 5S rRNA and its relation to function. J Mol Evol. 1975;6:61–76.CrossRefPubMedGoogle Scholar
  153. 153.
    Nishikawa K, Takemura S. Nucleotide sequence of 5 S RNA from Torulopsis utilis. FEBS Lett. 1974;40:106–9.CrossRefPubMedGoogle Scholar
  154. 154.
    Luehrsen KR, Fox GE. The secondary structure of eucaryotic cytoplasmic 5S ribosomal RNA. Proc Natl Acad Sci USA. 1981;78:2150–4.CrossRefPubMedPubMedCentralGoogle Scholar
  155. 155.
    Fox GE. The structure and evolution of archaebacterial RNA. In: Gunzalus IC, editor. The Bacteria, vol 8. New York: Academic Press; 1985. p. 267–310.Google Scholar
  156. 156.
    Correll CC, Freeborn B, Moore PB, Steitz TA. Metals, motif, and recognition in the crystal structure of a 5S rRNA domain. Cell. 1997;91:705–12.CrossRefPubMedGoogle Scholar
  157. 157.
    Wrede P, Erdmann VA. Activities of B. stearothermophilus 50S ribosomes reconstituted with prokaryotic and eukaryotic 5S RNA. FEBS Lett. 1975;33:315–9.CrossRefGoogle Scholar
  158. 158.
    Bellemare G, Vigne R, Jordan B. Interaction between Escherichia coli ribosomal proteins and 5S RNA molecules: recognition of prokaryotic 5S RNAs and rejection of eukaryotic 5S RNAs. Biochimie. 1973;55:29–35.CrossRefPubMedGoogle Scholar
  159. 159.
    Valach M, Burger G, Gray MW, Lang BF. Widespread occurrence of organelle genome-encoded 5S rRNAs including permuted molecules. Nucleic Acids Res. 2014;42:13764–77.CrossRefPubMedPubMedCentralGoogle Scholar
  160. 160.
    Greber BJ, Boehringer D, Leitner A, Bieri P, Voigts-Hoffmann F, Erzberger JP, Leibundgut M, Aebersold R, Ban N. Architecture of the large subunit of the mammalian mitochondrial ribosome. Nature. 2014;515:283–6.PubMedGoogle Scholar
  161. 161.
    Brown A, Amunts A, Bai XC, Sugimoto Y, Edwards PC, Murshudov G, Scheres SH, Ramakrishnan V. Structure of the large ribosomal subunit from human mitochondria. Science. 2014;346:718–22.CrossRefPubMedPubMedCentralGoogle Scholar
  162. 162.
    Amunts A, Brown A, Bai XC, Llácer JL, Hussain T, Emsley P, Long F, Murshudov G, Sjors Scheres SHW, Ramakrishnan V. Structure of the yeast mitochondrial large ribosomal subunit. Science. 2014;2014(43):1485–9.CrossRefGoogle Scholar

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© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Biology and BiochemistryUniversity of HoustonHoustonUSA

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