The Dimeric Proto-Ribosome Within the Modern Ribosome

Chapter
Part of the Cellular Origin, Life in Extreme Habitats and Astrobiology book series (COLE, volume 22)

Abstract

A structural element that could have existed independently in the prebiotic era was identified at the active site of the contemporary ribosome’s large subunit. It is suggested to have functioned as a proto-ribosome, catalyzing noncoded peptide bond formation and primitive elongation. This simple apparatus, constructed from a dimer of small, self-folding, stable RNA molecules, structurally related to tRNA, could have assembled spontaneously under prebiotic conditions. Its structure enabled the catalysis of peptide bond formation in the same manner that the contemporary ribosome exerts positional catalysis by accommodating the two reactants in a stereochemistry favorable for peptide bond formation. This prebiotic entity, which was efficient and stable enough to be retained by evolution as the highly conserved active site of the ribosome, was the matrix from which the modern protein biosynthesis mechanism – common to all living organisms – has evolved.

Keywords

Domain Versus Peptide Bond Formation Symmetrical Region Peptidyl Transferase Center Core Molecule 
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.

Notes

Acknowledgments

Thanks are due to Ada Yonath for initiating the ribosome evolution study and to Amitai Halevi, Noam Adir, Sagi, and Nimrod Agmon for their help. Support was provided by the US National Inst. of Health (GM34360) and the Kimmelman Center for Macromolecular Assemblies.

References

  1. Abramovitz DL, Pyle AM (1997) Remarkable morphological variability of a common RNA folding motif: the GNRA tetraloop-receptor interaction. J Mol Biol 266:493–506PubMedCrossRefGoogle Scholar
  2. Agmon I (2009) The dimeric proto-ribosome: structural details and possible implications on the origin of life. Int J Mol Sci 10:2921–2934PubMedCrossRefGoogle Scholar
  3. Agmon I, Auerbach T, Baram D, Bartels H, Bashan A, Berisio R, Fucini P, Hansen HA, Harms J, Kessler M, Peretz M, Schluenzen F, Yonath A, Zarivach R (2003) On peptide bond formation, translocation, nascent protein progression and the regulatory properties of ribosomes. Eur J Biochem 270:2543–2556PubMedCrossRefGoogle Scholar
  4. Agmon I, Bashan A, Zarivach R, Yonath A (2005) Symmetry at the active site of the ribosome: structural and functional implications. Biol Chem 386:833–844PubMedCrossRefGoogle Scholar
  5. Agmon I, Bashan A, Yonath A (2006) On ribosome conservation and evolution. Isr J Ecol Evol 52:359–374CrossRefGoogle Scholar
  6. Agmon I, Davidovich C, Bashan A, Yonath A (2009) Identification of the prebiotic translation apparatus within the contemporary ribosome. http://precedings.nature.com/documents/-2921/version/1
  7. Ban N, Nissen P, Hansen J, Moore PB, Steitz TA (2000) The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science 289:905–920PubMedCrossRefGoogle Scholar
  8. Bashan A, Agmon I, Zarivach R, Schluenzen F, Harms J, Berisio R, Bartels H, Franceschi F, Auerbach T, Hansen HA, Kossoy E, Kessler M, Yonath A (2003) Structural basis of the ribosomal machinery for peptide bond formation, translocation, and nascent chain progression. Mol Cell 11:91–102PubMedCrossRefGoogle Scholar
  9. Battle DJ, Doudna JA (2002) Specificity of RNA-RNA helix recognition. Proc Natl Acad Sci USA 99:11676–11681PubMedCrossRefGoogle Scholar
  10. 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 38:422–427PubMedCrossRefGoogle Scholar
  11. Bokov K, Steinberg SV (2009) A hierarchical model for evolution of 23S ribosomal RNA. Nature 457:977–980PubMedCrossRefGoogle Scholar
  12. Cannone JJ, Subramanian S, Schnare MN, Collett JR, D’Souza LM, Du Y, Feng B, Lin N, Madabusi LV, Müller KM, Pande N, Shang Z, Yu N, Gutell RR (2002) The comparative RNA Web CRW. Site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics 3:1–31CrossRefGoogle Scholar
  13. Chworos A, Severcan I, Koyfman AY, Weinkam P, Oroudjev E, Hansma HG, Jaeger L (2004) Building programmable jigsaw puzzles with RNA. Science 306:2068–2072PubMedCrossRefGoogle Scholar
  14. Costa M, Michel F (1997) Rules for RNA recognition of GNRA tetraloops deduced by in vitro selection: comparison with in vivo evolution. EMBO J 16:3289–3302PubMedCrossRefGoogle Scholar
  15. Davidovich C, Belousoff M, Bashan A, Yonath A (2009) The evolving ribosome: from non-coded peptide bond formation to sophisticated translation machinery. Res Microbiol 160:487–492PubMedCrossRefGoogle Scholar
  16. Davis JH, Tonelli M, Scott LG, Jaeger L, Williamson JR, Butcher SE (2005) RNA helical packing in solution: NMR structure of a 30 kDa GAAA tetraloop-receptor complex. J Mol Biol 351:371–382. http://www.ncbi.nlm.nih.gov/pubmed/16002091?ordinalpos=3&itool=EntrezSystem2.PEntrez.Pubmed.Pubmed_ResultsPanel.Pubmed_RVDocSum Google Scholar
  17. Di Giulio M (1992) On the origin of the transfer RNA molecule. J Theor Biol 159:199–214PubMedCrossRefGoogle Scholar
  18. Dick TP, Schamel WA (1995) Molecular evolution of transfer RNA from two precursor hairpins: implications for the origin of protein synthesis. J Mol Evol 41:1–9PubMedCrossRefGoogle Scholar
  19. Doshi KJ, Cannone JJ, Cobaugh CW, Gutell RR (2004) Evaluation of the suitability of free energy minimization using nearest-neighbor energy parameters for RNA secondary structure prediction. BMC Bioinformatics 5:105PubMedCrossRefGoogle Scholar
  20. Draper DE (2004) A guide to ions and RNA structure. RNA 10:335–343PubMedCrossRefGoogle Scholar
  21. Eigen M, Lindemann BF, Tietze M, Winkler-Oswatitsch R, Dress A, von Haeseler A (1989) How old is the genetic code? Statistical geometry of tRNA provides an answer. Science 244:673–679PubMedCrossRefGoogle Scholar
  22. Fox GE, Naik AK (2004) The evolutionary history of the ribosome. In: de Pouplana LR (ed) The genetic code and the origin of life. Landes Bioscience, Georgetown, pp 92–105CrossRefGoogle Scholar
  23. Gregory ST, Dahlberg AE (2004) Peptide bond formation is all about proximity. Nat Struct Mol Biol 11:586–587PubMedCrossRefGoogle Scholar
  24. 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 107:679–688PubMedCrossRefGoogle Scholar
  25. Hsiao C, Mohan S, Kalahar BK, Williams LD (2009) Peeling the onion: ribosomes are ancient molecular fossils. Mol Biol Evol 26:2415–2425PubMedCrossRefGoogle Scholar
  26. Jaeger L, Chworos A (2006) The architectonics of programmable RNA and DNA nanostructures. Curr Opin Struct Biol 16:531–543PubMedCrossRefGoogle Scholar
  27. Jaeger L, Michel F, Westhof E (1994) Involvement of a GNRA tetraloop in long-range RNA tertiary interactions. J Mol Biol 236:1271–1276PubMedCrossRefGoogle Scholar
  28. Jaeger L, Westhof E, Leontis NB (2001) TectoRNA: modular assembly units for the construction of RNA nano-objects. Nucleic Acids Res 29:455–463PubMedCrossRefGoogle Scholar
  29. Joshi PC, Aldersley MF, Delano JW, Ferris JP (2009) Mechanism of montmorillonite catalysis in the formation of RNA oligomers. J Am Chem Soc 131:13369–13374PubMedCrossRefGoogle Scholar
  30. Kholod NS (1999) Dimer formation by tRNAs. Biochemistry (Mosc) 64:298–306Google Scholar
  31. Klein DJ, Moore PB, Steitz TA (2004) The roles of ribosomal proteins in the structure assembly, and evolution of the large ribosomal subunit. J Mol Biol 340:141–177PubMedCrossRefGoogle Scholar
  32. Korostelev A, Trakhanov S, Laurberg M, Noller HF (2006) Crystal structure of a 70S ribosome-tRNA complex reveals functional interactions and rearrangements. Cell 126:1065–1077PubMedCrossRefGoogle Scholar
  33. Maizels N, Weiner AM (1994) Phylogeny from function: evidence from the molecular fossil record that tRNA originated in replication, not translation. Proc Natl Acad Sci USA 91:6729–6734PubMedCrossRefGoogle Scholar
  34. Mathews DH, Sabina J, Zuker M, Turner DH (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol 288:911–940PubMedCrossRefGoogle Scholar
  35. Nagaswamy U, Fox GE (2003) RNA ligation and the origin of tRNA. Orig Life Evol Biosph 33:199–209PubMedCrossRefGoogle Scholar
  36. Nissen P, Hansen J, Ban N, Moore PB, Steitz TA (2000) The structural basis of ribosome activity in peptide bond synthesis. Science 289:920–930PubMedCrossRefGoogle Scholar
  37. Nissen P, Ippolito JA, Ban N, Moore PB, Steitz TA (2001) RNA tertiary interactions in the large ribosomal subunit: the A-minor motif. Proc Natl Acad Sci USA 98:4899–4903PubMedCrossRefGoogle Scholar
  38. Pino S, Ciciriello F, Costanzo G, Di Mauro E (2008) Nonenzymatic RNA ligation in water. J Biol Chem 283:36494–36503PubMedCrossRefGoogle Scholar
  39. Pley HW, Flaherty KM, McKay DB (1994) Model for an RNA tertiary interaction from the structure of an intermolecular complex between a GAAA tetraloop and an RNA helix. Nature 372:111–113PubMedCrossRefGoogle Scholar
  40. Pyle AM (2002) Metal ions in the structure and function of RNA. J Biol Inorg Chem 7:679–690PubMedCrossRefGoogle Scholar
  41. Roy MD, Wittenhagen LM, Kelley SO (2005) Structural probing of a pathogenic tRNA dimer. RNA 11:254–260PubMedCrossRefGoogle Scholar
  42. Russell R (2008) RNA misfolding and the action of chaperones. Front Biosci 13:1–20PubMedCrossRefGoogle Scholar
  43. Schuwirth BS, Borovinskaya MA, Hau CW, Zhang W, Vila-Sanjurjo A, Holton JM, Cate JH (2005) Structures of the bacterial ribosome at 3.5 A resolution. Science 310:827–834PubMedCrossRefGoogle Scholar
  44. Selmer M, Dunham CM, Murphy FV 4th, Weixlbaumer A, Petry S, Kelley AC, Weir JR, Ramakrishnan V (2006) Structure of the 70S ribosome complexed with mRNA and tRNA. Science 313:1935–1942PubMedCrossRefGoogle Scholar
  45. Steitz TA, Moore PB (2003) RNA, the first macromolecular catalyst: the ribosome is a ribozyme. Trends Biochem Sci 28:411–418PubMedCrossRefGoogle Scholar
  46. Sun X, Li JM, Wartell RM (2007) Conversion of stable RNA hairpin to a metastable dimer in frozen solution. RNA 13:2277–2286PubMedCrossRefGoogle Scholar
  47. Thirumoorthy K, Nandi N (2007) Homochiral preference in peptide synthesis in ribosome: role of amino terminal, peptidyl terminal, and U2620. J Phys Chem B 111:9999–10004PubMedCrossRefGoogle Scholar
  48. Voorhees RM, Weixlbaumer A, Loakes D, Kelley AC, Ramakrishnan V (2009) Insights into substrate stabilization from snapshots of the peptidyl transferase center of the intact 70S ribosome. Nat Struct Mol Biol 16:528–533PubMedCrossRefGoogle Scholar
  49. Voytek SB, Joyce GF (2007) Emergence of a fast-reacting ribozyme that is capable of undergoing continuous evolution. Proc Natl Acad Sci USA 104:15288–15293PubMedCrossRefGoogle Scholar
  50. Weiner AM, Maizels N (1987) TRNA-like structures tag the 3′ ends of genomic RNA molecules for replication: implications for the origin of protein synthesis. Proc Natl Acad Sci USA 84:7383–7387PubMedCrossRefGoogle Scholar
  51. Woese CR (2001) Translation: in retrospect and prospect. RNA 7:1055–1067PubMedCrossRefGoogle Scholar
  52. Yonath A (2003) Ribosomal tolerance and peptide bond formation. Biol Chem 384:1411–1419PubMedCrossRefGoogle Scholar
  53. Zarivach R, Bashan A, Berisio R, Harms J, Auerbach T, Schluenzen F, Bartels H, Baram D, Pyetan E, Sittner A, Amit M, Hansen HSA, Kessler M, Liebe C, Wolff A, Agmon I, Yonath A (2004) Functional aspects of ribosomal architecture: symmetry, chirality and regulation. J Phys Org Chem 17:901–912CrossRefGoogle Scholar
  54. Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Schulich Faculty of Chemistry, Institute for Advanced Studies in Theoretical ChemistryTechnion–Israel Institute of TechnologyHaifaIsrael
  2. 2.Fritz Haber Research Center for Molecular DynamicsHebrew UniversityJerusalemIsrael

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