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Cited by 45RNA and protein synthesis mechanismsOrigins and Evolution of LifeGenomics and Phylogenetic Studies

Molecular paleontology: a biochemical model of the ancestral ribosome

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Hsiao, Chiaolong, Lenz, Timothy K., Peters, Jessica K., Fang, Po-Yu, Schneider, Dana M., Anderson, Eric J., Preeprem, Thanawadee, Bowman, Jessica C. +11 more·2013·Nucleic Acids Research
DOI 10.1093/nar/gkt023PMC PMC3597689
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Abstract

Ancient components of the ribosome, inferred from a consensus of previous work, were constructed in silico, in vitro and in vivo. The resulting model of the ancestral ribosome presented here incorporates ∼20% of the extant 23S rRNA and fragments of five ribosomal proteins. We test hypotheses that ancestral rRNA can: (i) assume canonical 23S rRNA-like secondary structure, (ii) assume canonical tertiary structure and (iii) form native complexes with ribosomal protein fragments. Footprinting experiments support formation of predicted secondary and tertiary structure. Gel shift, spectroscopic and yeast three-hybrid assays show specific interactions between ancestral rRNA and ribosomal protein fragments, independent of other, more recent, components of the ribosome. This robustness suggests that the catalytic core of the ribosome is an ancient construct that has survived billions of years of evolution without major changes in structure. Collectively, the data here support a model in which ancestors of the large and small subunits originated and evolved independently of each other, with autonomous functionalities.

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References 70 · Cited by 45

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  1. [1]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 321 215 234 12144780
  2. [2]Woese CR Interpreting the universal phylogenetic tree Proc. Natl. Acad. Sci. USA 2000 97 8392 8396 10900003 PMC26958
  3. [3]Woese CR Translation: in retrospect and prospect RNA 2001 7 1055 1067 11497425 PMC1370154
  4. [4]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 5 e9437 20208990 PMC2830423
  5. [5]Williams D Fournier GP Lapierre P Swithers KS Green AG Andam CP Gogarten JP A rooted net of life Biol. Direct 2011 6 45 21936906 PMC3189188
  6. [9]Hsiao C Mohan S Kalahar BK Williams LD Peeling the onion: ribosomes are ancient molecular fossils Mol. Biol. Evol. 2009 26 2415 2425 19628620
  7. [10]Belousoff MJ Davidovich C Zimmerman E Caspi Y Wekselman I Rozenszajn L Shapira T Sade-Falk O Taha L Bashan A Ancient machinery embedded in the contemporary ribosome Biochem. Soc. Trans. 2010 38 422 427 20298195
  8. [11]Hury J Nagaswamy U Larios-Sanz M Fox GE Ribosome origins: the relative age of 23S rRNA domains Orig. Life Evol. Biosph. 2006 36 421 429 16972151
  9. [12]Noller HF Evolution of protein synthesis from an RNA world Cold Spring Harb. Perspect. Biol. 2010 7 7 PMC3312679 20610545
  10. [16]Crick FH The origin of the genetic code J. Mol. Biol. 1968 38 367 379 4887876
  11. [17]Orgel LE Evolution of the genetic apparatus J. Mol. Biol. 1968 38 381 393 5718557
  12. [18]Crick F Central dogma of molecular biology Nature 1970 226 561 563 4913914
  13. [19]Rost B Protein structures sustain evolutionary drift Fold Des. 1997 2 S19 S24 9218962
  14. [20]Heinz DW Baase WA Zhang XJ Blaber M Dahlquist FW Matthews BW Accommodation of amino acid insertions in an alpha-helix of T4 lysozyme. structural and thermodynamic analysis J. Mol. Biol. 1994 236 869 886 8114100
  15. [21]Selmer M Dunham CM Murphy FV Weixlbaumer A Petry S Kelley AC Weir JR Ramakrishnan V Structure of the 70S ribosome complexed with mRNA and tRNA Science 2006 313 1935 1942 16959973
  16. [22]Hsiao C Williams LD A recurrent magnesium-binding motif provides a framework for the ribosomal peptidyl transferase center Nucleic Acids Res. 2009 37 3134 3142 19279186 PMC2691814
  17. [23]Ban N Nissen P Hansen J Moore PB Steitz TA The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution Science 2000 289 905 920 10937989
  18. [24]Noller HF Hoffarth V Zimniak L Unusual resistance of peptidyl transferase to protein extraction procedures Science 1992 256 1416 1419 1604315
  19. [25]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 340 141 177 15184028
  20. [26]Ben-Shem A Jenner L Yusupova G Yusupov M Crystal structure of the eukaryotic ribosome Science 2010 330 1203 1209 21109664
  21. [27]Petrov A Bernier C Hsiao C Okafor CD Tannenbaum E Stern J Gaucher E Schneider DM Harvey SC Williams LD RNA-magnesium-protein interactions in large ribosomal subunit J. Phys. Chem. B 2012 116 8113 8120 22712611
  22. [28]Mohan S Hsiao C Bowman JC Wartell R Williams LD RNA tetraloop folding reveals tension between backbone restraints and molecular interactions J. Am. Chem. Soc. 2010 132 12679 12689 20726568
  23. [29]Phillips JC Braun R Wang W Gumbart J Tajkhorshid E Villa E Chipot C Skeel RD Kale L Schulten K Scalable molecular dynamics with NAMD J. Comput. Chem. 2005 26 1781 1802 16222654 PMC2486339
  24. [30]Brooks BR Brooks CL 3rd Mackerell AD Jr Nilsson L Petrella RJ Roux B Won Y Archontis G Bartels C Boresch S CHARMM: the biomolecular simulation program J. Comput. Chem. 2009 30 1545 1614 19444816 PMC2810661
  25. [31]Bowman JC Azizi B Lenz TK Roy P Williams LD Conn GL Preparation of long templates for RNA in vitro transcription by recursive PCR Recombinant and In Vitro RNA Synthesis: Methods and Protocols, Methods in Molecular Biology 2012 Vol. 941 Springer Science LLC, pp. 19–41 23065551
  26. [32]Wilkinson KA Merino EJ Weeks KM Selective 2'-hydroxyl acylation analyzed by primer extension (SHAPE): quantitative RNA structure analysis at single nucleotide resolution Nat. Protoc. 2006 1 1610 1616 17406453
  27. [33]Athavale SS Gossett JJ Hsiao C Bowman JC O'Neill E Hershkovitz E Preeprem T Hud NV Wartell RM Harvey SC Domain III of the T. thermophilus 23S rRNA folds independently to a near-native state RNA 2012 18 752 758 22334759 PMC3312562
  28. [35]Cantor C Schimmel P Biophysical Chemistry (I-III) 1984 New York Academic Press
  29. [36]Shcherbakov D Piendl W A novel view of gel-shifts: analysis of RNA-protein complexes using a two-color fluorescence dye procedure Electrophoresis 2007 28 749 755 17315147
  30. [37]Stumpf CR Opperman L Wickens M Analysis of RNA-protein interactions using a yeast three-hybrid system Methods Enzymol. 2008 449 295 315 19215764
  31. [38]Wurster SE Bida JP Her YF Maher LJ 3rd Characterization of anti-Nf-Κb RNA aptamer-binding specificity in vitro and in the yeast three-hybrid system Nucleic Acids Res. 2009 37 6214 6224 19696077 PMC2764441
  32. [39]Cassiday LA Maher LJ 3rd In vivo recognition of an RNA aptamer by its transcription factor target Biochemistry 2001 40 2433 2438 11327864
  33. [40]Hook B Bernstein D Zhang B Wickens M RNA-protein interactions in the yeast three-hybrid system: affinity, sensitivity, and enhanced library screening RNA 2005 11 227 233 15613539 PMC1370711
  34. [41]Bernstein DS Buter N Stumpf C Wickens M Analyzing mRNA-protein complexes using a yeast three-hybrid system Methods 2002 26 123 141 12054889
  35. [42]Nikolcheva T Association of a group 1 intron with its splice junction in 50S ribosomes: implications for intron toxicity RNA 1997 3 1016 1027 9292500 PMC1369547
  36. [43]Kauffmann AD Campagna RJ Bartels CB Childs-Disney JL Improvement of RNA secondary structure prediction using Rnase H cleavage and randomized oligonucleotides Nucleic Acids Res. 2009 37 e121 19596816 PMC2764423
  37. [44]Donis-Keller H Site specific enzymatic cleavage of RNA Nucleic Acids Res. 1979 7 179 192 386279 PMC328004
  38. [45]Hofacker IL Fekete M Flamm C Huynen MA Rauscher S Stolorz PE Stadler PF Automatic detection of conserved RNA structure elements in complete RNA virus genomes Nucleic Acids Res. 1998 26 3825 3836 9685502 PMC147758
  39. [46]Wu P Nakano S Sugimoto N Temperature dependence of thermodynamic properties for DNA/DNA and RNA/DNA duplex formation Eur. J. Biochem. 2002 269 2821 2830 12071944
  40. [47]Merino EJ Wilkinson KA Coughlan JL Weeks KM RNA structure analysis at single nucleotide resolution by selective 2'-hydroxyl acylation and primer extension (SHAPE) J. Am. Chem. Soc. 2005 127 4223 4231 15783204
  41. [48]Deigan KE Li TW Mathews DH Weeks KM Accurate SHAPE-directed RNA structure determination Proc. Natl. Acad. Sci. USA 2009 106 97 102 19109441 PMC2629221
  42. [49]Brion P Westhof E Hierarchy and dynamics of RNA folding Annu. Rev. Biophys. Biomol. Struct. 1997 26 113 137 9241415
  43. [50]Tinoco I Jr Bustamante C How RNA folds J. Mol. Biol. 1999 293 271 281 10550208
  44. [51]Bowman JC Lenz TK Hud NV Williams LD Cations in charge: magnesium ions in RNA folding and catalysis Curr. Opin. Struct. Biol. 2012 22 262 272 22595008
  45. [52]Butcher SE Dieckmann T Feigon J Solution structure of a GAAA tetraloop receptor RNA EMBO J. 1997 16 7490 7499 9405377 PMC1170348
  46. [53]Klein DJ Moore PB Steitz TA The contribution of metal ions to the structural stability of the large ribosomal subunit RNA 2004 10 1366 1379 15317974 PMC1370624
  47. [54]Mortimer SA Weeks KM Time-resolved RNA SHAPE chemistry J. Am. Chem. Soc. 2008 130 16178 16180 18998638
  48. [55]Athavale SS Petrov AS Hsiao C Watkins D Prickett CD Gossett JJ Lie L Bowman JC O'Neill E Bernier CR RNA folding and catalysis mediated by iron (II) PLoS ONE 2012 7 e38024 22701543 PMC3365117
  49. [56]Ryder SP Recht MI Williamson JR Quantitative analysis of protein-RNA interactions by gel mobility shift Methods Mol. Biol. 2008 488 99 115 18982286 PMC2928675
  50. [57]Hayashi T Tahara M Iwasaki K Kouzuma Y Kimura M Requirement for C-terminal extension to the RNA binding domain for efficient RNA binding by ribosomal protein L2 Biosci. Biotechnol. Biochem. 2002 66 682 684 12005072
  51. [58]Uchiumi T Sato N Wada A Hachimori A Interaction of the Sarcin/Ricin domain of 23 S ribosomal RNA with proteins L3 and L6 J. Biol. Chem. 1999 274 681 686 9873002
  52. [59]Marquardt O Roth HE Wystup G Nierhaus KH Binding of Escherichia Coli ribosomal proteins to 23S RNA under reconstitution conditions for the 50S subunit Nucleic Acids Res. 1979 6 3641 3650 386275 PMC327962
  53. [60]Cech TR Crawling out of the RNA World Cell 2009 136 599 602 19239881
  54. [61]Anderson RM Kwon M Strobel SA Toward ribosomal RNA catalytic activity in the absence of protein J Mol Evol. 2007 64 472 483 17417708
  55. [62]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 9874776 PMC15097
  56. [63]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. Trans. R. Soc. Lond. B Biol. Sci. 2011 366 2972 2978 21930590 PMC3158926
  57. [64]Ostergaard P Phan H Johansen LB Egebjerg J Ostergaard L Porse BT Garrett RA Assembly of proteins and 5S rRNA to transcripts of the major structural domains of 23S rRNA J. Mol. Biol. 1998 284 227 240 9813114
  58. [67]Yang H Jossinet F Leontis N Chen L Westbrook J Berman H Westhof E Tools for the automatic identification and classification of RNA base pairs Nucleic Acids Res. 2003 31 3450 3460 12824344 PMC168936
  59. [68]Leontis NB Westhof E Geometric nomenclature and classification of RNA base pairs RNA 2001 7 499 512 11345429 PMC1370104
  60. [69]Leontis NB Stombaugh J Westhof E The non-watson-crick base pairs and their associated isostericity matrices Nucleic Acids Res. 2002 30 3497 3531 12177293 PMC134247
  61. [70]Studier FW Protein production by auto-induction in high density shaking cultures Protein Expr. Purif. 2005 41 207 234 15915565

Authors
Hsiao, C., Lenz, T. K., Peters, J. K., Fang, P.-Y., Schneider, D. M., Anderson, E. J., Preeprem, T., Bowman, J. C., O'Neill, E. B., Lie, L., Athavale, S. S., Gossett, J. J., Trippe, C., Murray, J., Petrov, A. S., Wartell, R. M., Harvey, S. C., Hud, N. V., & Dean Williams, L.
Affiliations
Georgia Institute of Technology (US)
ORCID
Venue
Nucleic Acids Research
Publisher
Oxford University Press (OUP)
Published
2013-01-25
Volume
41
Issue
5
Pages
3373-3385
ISSN
  • 0305-1048 (ISSN-L)
  • 1362-4962
DOI
10.1093/nar/gkt023
PMC
PMC3597689
OpenAlex
W2007410732
Cited by
45
References
70
Citations by year
2026: 1 · 2024: 2 · 2023: 2 · 2022: 4 · 2021: 5 · 2020: 4 · 2019: 5 · 2018: 3 · 2017: 5 · 2016: 4 · 2015: 4 · 2014: 3 · 2013: 3
FWCI
2.09
Type
journal article
Language
en
Open access
Licence
Locations
  • Nucleic Acids Research (publishedVersion, cc-by-nc)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
  • Physical Sciences › Physics and Astronomy › Astronomy and Astrophysics › Origins and Evolution of Life
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Keywords
23S rRNA, ribosomal proteins, ribosome evolution, rRNA secondary structure, rRNA tertiary structure, molecular paleontology
MeSH terms
Magnesium, Models, Genetic, Models, Molecular, Nucleic Acid Conformation, Peptide Fragments, Protein Binding, Ribosomal Proteins, Ribosomes, RNA, Bacterial, RNA, Ribosomal, 23S, Ribonuclease H, Thermus thermophilus, Evolution, Molecular, RNA Cleavage

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