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.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abramovitz DL, Pyle AM (1997) Remarkable morphological variability of a common RNA folding motif: the GNRA tetraloop-receptor interaction. J Mol Biol 266:493–506
Agmon I (2009) The dimeric proto-ribosome: structural details and possible implications on the origin of life. Int J Mol Sci 10:2921–2934
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 270:2543–2556
Agmon I, Bashan A, Zarivach R, Yonath A (2005) Symmetry at the active site of the ribosome: structural and functional implications. Biol Chem 386:833–844
Agmon I, Bashan A, Yonath A (2006) On ribosome conservation and evolution. Isr J Ecol Evol 52:359–374
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
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 289:905–920
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 11:91–102
Battle DJ, Doudna JA (2002) Specificity of RNA-RNA helix recognition. Proc Natl Acad Sci USA 99:11676–11681
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
Bokov K, Steinberg SV (2009) A hierarchical model for evolution of 23S ribosomal RNA. Nature 457:977–980
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 3:1–31
Chworos A, Severcan I, Koyfman AY, Weinkam P, Oroudjev E, Hansma HG, Jaeger L (2004) Building programmable jigsaw puzzles with RNA. Science 306:2068–2072
Costa M, Michel F (1997) Rules for RNA recognition of GNRA tetraloops deduced by in vitro selection: comparison with in vivo evolution. EMBO J 16:3289–3302
Davidovich C, Belousoff M, Bashan A, Yonath A (2009) The evolving ribosome: from non-coded peptide bond formation to sophisticated translation machinery. Res Microbiol 160:487–492
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
Di Giulio M (1992) On the origin of the transfer RNA molecule. J Theor Biol 159:199–214
Dick TP, Schamel WA (1995) Molecular evolution of transfer RNA from two precursor hairpins: implications for the origin of protein synthesis. J Mol Evol 41:1–9
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 5:105
Draper DE (2004) A guide to ions and RNA structure. RNA 10:335–343
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 244:673–679
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 92–105
Gregory ST, Dahlberg AE (2004) Peptide bond formation is all about proximity. Nat Struct Mol Biol 11:586–587
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
Hsiao C, Mohan S, Kalahar BK, Williams LD (2009) Peeling the onion: ribosomes are ancient molecular fossils. Mol Biol Evol 26:2415–2425
Jaeger L, Chworos A (2006) The architectonics of programmable RNA and DNA nanostructures. Curr Opin Struct Biol 16:531–543
Jaeger L, Michel F, Westhof E (1994) Involvement of a GNRA tetraloop in long-range RNA tertiary interactions. J Mol Biol 236:1271–1276
Jaeger L, Westhof E, Leontis NB (2001) TectoRNA: modular assembly units for the construction of RNA nano-objects. Nucleic Acids Res 29:455–463
Joshi PC, Aldersley MF, Delano JW, Ferris JP (2009) Mechanism of montmorillonite catalysis in the formation of RNA oligomers. J Am Chem Soc 131:13369–13374
Kholod NS (1999) Dimer formation by tRNAs. Biochemistry (Mosc) 64:298–306
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 340:141–177
Korostelev A, Trakhanov S, Laurberg M, Noller HF (2006) Crystal structure of a 70S ribosome-tRNA complex reveals functional interactions and rearrangements. Cell 126:1065–1077
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 91:6729–6734
Mathews DH, Sabina J, Zuker M, Turner DH (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol 288:911–940
Nagaswamy U, Fox GE (2003) RNA ligation and the origin of tRNA. Orig Life Evol Biosph 33:199–209
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
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 98:4899–4903
Pino S, Ciciriello F, Costanzo G, Di Mauro E (2008) Nonenzymatic RNA ligation in water. J Biol Chem 283:36494–36503
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 372:111–113
Pyle AM (2002) Metal ions in the structure and function of RNA. J Biol Inorg Chem 7:679–690
Roy MD, Wittenhagen LM, Kelley SO (2005) Structural probing of a pathogenic tRNA dimer. RNA 11:254–260
Russell R (2008) RNA misfolding and the action of chaperones. Front Biosci 13:1–20
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 310:827–834
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 313:1935–1942
Steitz TA, Moore PB (2003) RNA, the first macromolecular catalyst: the ribosome is a ribozyme. Trends Biochem Sci 28:411–418
Sun X, Li JM, Wartell RM (2007) Conversion of stable RNA hairpin to a metastable dimer in frozen solution. RNA 13:2277–2286
Thirumoorthy K, Nandi N (2007) Homochiral preference in peptide synthesis in ribosome: role of amino terminal, peptidyl terminal, and U2620. J Phys Chem B 111:9999–10004
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 16:528–533
Voytek SB, Joyce GF (2007) Emergence of a fast-reacting ribozyme that is capable of undergoing continuous evolution. Proc Natl Acad Sci USA 104:15288–15293
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 84:7383–7387
Woese CR (2001) Translation: in retrospect and prospect. RNA 7:1055–1067
Yonath A (2003) Ribosomal tolerance and peptide bond formation. Biol Chem 384:1411–1419
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 17:901–912
Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415
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.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2012 Springer Science+Business Media B.V.
About this chapter
Cite this chapter
Agmon, I. (2012). The Dimeric Proto-Ribosome Within the Modern Ribosome. In: Seckbach, J. (eds) Genesis - In The Beginning. Cellular Origin, Life in Extreme Habitats and Astrobiology, vol 22. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-2941-4_32
Download citation
DOI: https://doi.org/10.1007/978-94-007-2941-4_32
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-2940-7
Online ISBN: 978-94-007-2941-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)