Advertisement

Journal of Molecular Evolution

, Volume 69, Issue 5, pp 430–443 | Cite as

The Evolutionary History of the Structure of 5S Ribosomal RNA

  • Feng-Jie Sun
  • Gustavo Caetano-Anollés
Article

Abstract

5S rRNA is the smallest nucleic acid component of the large ribosomal subunit, contributing to ribosomal assembly, stability, and function. Despite being a model for the study of RNA structure and RNA–protein interactions, the evolution of this universally conserved molecule remains unclear. Here, we explore the history of the three-domain structure of 5S rRNA using phylogenetic trees that are reconstructed directly from molecular structure. A total of 46 structural characters describing the geometry of 666 5S rRNAs were used to derive intrinsically rooted trees of molecules and molecular substructures. Trees of molecules revealed the tripartite nature of life. In these trees, superkingdom Archaea formed a paraphyletic basal group, while Bacteria and Eukarya were monophyletic and derived. Trees of molecular substructures supported an origin of the molecule in a segment that is homologous to helix I (α domain), its initial enhancement with helix III (β domain), and the early formation of the three-domain structure typical of modern 5S rRNA in Archaea. The delayed formation of the branched structure in Bacteria and Eukarya lends further support to the archaeal rooting of the tree of life. Remarkably, the evolution of molecular interactions between 5S rRNA and associated ribosomal proteins inferred from a census of domain structure in hundreds of genomes established a tight relationship between the age of 5S rRNA helices and the age of ribosomal proteins. Results suggest 5S rRNA originated relatively quickly but quite late in evolution, at a time when primordial metabolic enzymes and translation machinery were already in place. The molecule therefore represents a late evolutionary addition to the ribosomal ensemble that occurred prior to the early diversification of Archaea.

Keywords

Ribosome 5S rRNA Secondary structure Molecular evolution Cladistic analysis 

Notes

Acknowledgments

We thank Ajith Harish for help with 3D mappings, Minglei Wang for calculating nd values, and Hee Shin Kim, Ajith Harish, Minglei Wang, Liudmila Yafremava, Kyung Mo Kim, and Jay Mittenthal for helpful discussions. This study was supported by National Science Foundation Grants MCB-0343126 and MCB-0749836, the Critical Research Initiative of the University of Illinois, and the United Soybean Board. Any opinions, findings, and conclusions and recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the funding agencies. Both authors designed and performed the experiments, analyzed the data, and wrote the article.

Supplementary material

239_2009_9264_MOESM1_ESM.pdf (2.2 mb)
Supplementary material 1 (PDF 2288 kb)

References

  1. Ammons D, Rampersad J, Fox GE (1999) 5S rRNA gene deletions cause an unexpectedly high fitness loss in Escherichia coli. Nucleic Acids Res 27:637–642CrossRefPubMedGoogle Scholar
  2. Azad AA, Failla P, Hanna PJ (1998) Inhibition of ribosomal subunit association and protein synthesis by oligonucleotides corresponding to defined regions of 18S rRNA and 5S rRNA. Biochem Biophys Res Commun 248:51–56CrossRefPubMedGoogle Scholar
  3. 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 289:905–920CrossRefPubMedGoogle Scholar
  4. Barciszewska MZ, Szymanski M, Erdmann VA, Barciszewski J (2000) 5S ribosomal RNA. Biomacromolecules 1:297–302CrossRefPubMedGoogle Scholar
  5. Barciszewska MZ, Szymanski M, Erdmann VA, Barciszewski J (2001) Structure and functions of 5S rRNA. Acta Biochim Pol 48:191–198PubMedGoogle Scholar
  6. Betzel C, Lorenz S, Furste JP, Bald R, Zhang M, Schneider TR, Wilson KS, Erdmann VA (1994) Crystal structure of domain A of Thermus flavus 5S rRNA and the contribution of water molecules to its structure. FEBS Lett 351:159–164CrossRefPubMedGoogle Scholar
  7. Bloch DP, McArthur B, Mirrop S (1985) tRNA–rRNA sequence homologies: evidence for an ancient modular format shared by tRNAs and rRNAs. Biosystems 17:209–225CrossRefPubMedGoogle Scholar
  8. Bogdanov AA, Dontsova OA, Dokudovskaya SS, Lavrik IN (1995) Structure and function of 5S rRNA in the ribosome. Biochem Cell Biol 73:869–876PubMedCrossRefGoogle Scholar
  9. Brodersen DE, Clemons WM Jr, Carter AP, Wimberly BT, Ramakrishnan V (2002) Crystal structure of the 30S ribosomal subunit from Thermus thermophilus: structure of the proteins and their interactions with 16S RNA. J Mol Biol 316:725–768CrossRefPubMedGoogle Scholar
  10. Brown J, Doolittle W (1995) Root of the universal tree of life based on ancient aminoacyl-tRNA synthetase gene duplications. Proc Natl Acad Sci USA 92:2441–2445CrossRefPubMedGoogle Scholar
  11. Caetano-Anollés G (2001) Novel strategies to study the role of mutation and nucleic acid structure in evolution. Plant Cell Tissue Org Cult 67:115–132CrossRefGoogle Scholar
  12. Caetano-Anollés G (2002a) Evolved RNA secondary structure and the rooting of the universal tree of life. J Mol Evol 54:333–345PubMedGoogle Scholar
  13. Caetano-Anollés G (2002b) Tracing the evolution of RNA structure in ribosomes. Nucleic Acids Res 30:2575–2587CrossRefPubMedGoogle Scholar
  14. Caetano-Anollés G (2005) Grass evolution inferred from chromosomal rearrangements and geometrical and statistical features in RNA structure. J Mol Evol 60:635–652CrossRefPubMedGoogle Scholar
  15. Caetano-Anollés G, Caetano-Anollés D (2003) An evolutionarily structured universe of protein architecture. Genome Res 13:1563–1571CrossRefPubMedGoogle Scholar
  16. Caetano-Anollés G, Kim HS, Mittenthal JE (2007) The origin of modern metabolic networks inferred from phylogenomic analysis of protein architecture. Proc Natl Acad Sci USA 104:9358–9363CrossRefPubMedGoogle Scholar
  17. Caetano-Anollés G, Wang M, Caetano-Anollés D, Mittenthal JE (2009) The origin, evolution and structure of the protein world. Biochem J 417:621–637CrossRefPubMedGoogle Scholar
  18. Carson M (1997) Ribbons. Methods Enzymol 277:493–505CrossRefPubMedGoogle Scholar
  19. Christiansen J, Garrett RA (1986) How do protein L18 and 5S RNA interact? In: Hardesty B, Kramer G (eds) Structure functions and genetics of ribosomes. Springer, New York, pp 253–269Google Scholar
  20. Deshmukh M, Tsay Y-F, Paulovich A, Woolford JL Jr (1993) Yeast ribosomal protein L1 required for the stability of newly synthesized 5S rRNA and the assembly of 60S ribosomal subunits. Mol Cell Biol 13:2835–2845PubMedGoogle Scholar
  21. Di Giulio M (1992) On the origin of the transfer RNA molecule. J Theor Biol 159:199–214CrossRefPubMedGoogle Scholar
  22. Di Giulio M (2007) The tree of life might be rooted in the branch leading to Nanoarchaeota. Gene 401:108–113CrossRefPubMedGoogle Scholar
  23. Dick TP, Schamel WWA (1995) Molecular evolution of transfer RNA from two precursor hairpins: implications for the origin of protein synthesis. J Mol Evol 41:1–9CrossRefPubMedGoogle Scholar
  24. Ding Y, Lawrence CE (1999) A Bayesian statistical algorithm for secondary structure prediction. Comput Chem 23:387–400CrossRefPubMedGoogle Scholar
  25. Dokudovskaya S, Dontsova O, Shpanchenko O, Bogdanov A, Brimacombe R (1996) Loop IV of 5 S ribosomal RNA has contacts both to domain II and to domain V of the 23 S RNA. RNA 2:146–152PubMedGoogle Scholar
  26. Doolittle RF (2005) Evolutionary aspects of whole-genome biology. Curr Opin Struct Biol 15:248–253CrossRefPubMedGoogle Scholar
  27. Eigen M, Winkler-Oswatitsch R (1981) Transfer-RNA, an early gene? Naturwissenschaften 68:282–292CrossRefPubMedGoogle Scholar
  28. Erdmann VA, Pieler T, Wolters J, Digweed M, Vogel D, Hartmann R (1986) Comparative structural and functional studies on small ribosomal RNAs. In: Hardesty B, Kramer G (eds) Structure function and genetics of ribosomes. Spring, New York, pp 164–183Google Scholar
  29. Fanning TG, Traut RR (1981) Topography of the E. coli 5S RNA-protein complex as determined by crosslinking with dimethyl suberimidate and dimethyl-3, 3′-dithiobispropionimidate. Nucleic Acids Res 9:993–1004CrossRefPubMedGoogle Scholar
  30. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  31. Forterre P (2009) The universal tree of life and the Last Universal Cellular Ancestor (LUCA): revolution and counter-revolutions. In: Caetano-Anollés G (ed), Evolutionary genomics and systems biology. Wiley, Hoboken (in press)Google Scholar
  32. Fox GE, Woese CR (1975) 5S RNA secondary structure. Nature 256:505–507CrossRefPubMedGoogle Scholar
  33. Frank J, Agrawal RK (2000) A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature 406:318–322CrossRefPubMedGoogle Scholar
  34. Gabashvili IS, Whirl-Carrillo M, Bada M, Banatao DR, Altman RB (2003) Ribosomal dynamics inferred from variations in experimental measurements. RNA 9:1301–1307CrossRefPubMedGoogle Scholar
  35. Gautheret RR, Konings D, Gutell R (1995) Pairing motifs in ribosomal RNA. RNA 1:807–814PubMedGoogle Scholar
  36. Glansdorff N, Xu Y, Labedan B (2008) The Last Universal Common Ancestor: emergence, constitution and genetic legacy of an elusive forerunner. Biol Direct 3:29CrossRefPubMedGoogle Scholar
  37. Gribaldo S, Cammarano P (1998) The root of the universal tree of life inferred from anciently duplicated genes encoding components of the protein-targeting machinery. J Mol Evol 47:508–516CrossRefPubMedGoogle Scholar
  38. Hamilton TB, Turner J, Barilla K, Romaniuk PJ (2001) Contribution of individual amino acids to the nucleic acid binding activities of Xenopus zinc finger proteins TFIIIA and p43. Biochemistry 40:6093–6101CrossRefPubMedGoogle Scholar
  39. Hannock J, Wagner R (1982) A structural model of 5S RNA from E. coli based on intramolecular crosslinking evidence. Nucleic Acids Res 10:1257–1269CrossRefGoogle Scholar
  40. Hillis DM, Huelsenbeck JP (1992) Signal, noise, and reliability in molecular phylogenetic analyses. J Hered 83:189–195PubMedGoogle Scholar
  41. Hofacker IL (2003) Vienna RNA secondary structure server. Nucleic Acids Res 31:3429–3431CrossRefPubMedGoogle Scholar
  42. Holmberg L, Nygard O (2000) Release of ribosome-bound 5 S rRNA upon cleavage of the phosphodiester bond between nucleotides A54 and A55 in 5 S rRNA. Biol Chem 381:1041–1046CrossRefPubMedGoogle Scholar
  43. Hopfield JJ (1978) Origin of the genetic code: a testable hypothesis based on tRNA structure, sequence, and kinetic proofreading. Proc Natl Acad Sci USA 75:4334–4338CrossRefPubMedGoogle Scholar
  44. Hori H, Osawa S (1987) Origin and evolution of organisms as deduced from 5S ribosomal RNA sequences. Mol Biol Evol 4:445–472PubMedGoogle Scholar
  45. Hori H, Lim B-L, Osawa S (1985) Evolution of green plants as deduced from 5S rRNA sequences. Proc Natl Acad Sci USA 82:820–823CrossRefPubMedGoogle Scholar
  46. Hunt LT, George DG, Yeh L-S, Dayhoff MO (1984) Evolution of prokaryote and eukaryote lines inferred from sequence evidence. Orig Life 14:657–664CrossRefPubMedGoogle Scholar
  47. Jeanmougin F, Thompson JD, Gouy M, Higgins DG, Gibson TJ (1998) Multiple sequence alignment with Clustal X. Trends Biochem Sci 23:403–405CrossRefPubMedGoogle Scholar
  48. Joachimiak A, Nalaskowska N, Barciszewska M, Barciszewski J, Mashkova T (1990) Higher plant 5S rRNAs share common secondary and tertiary structure. A new three domains model. Int J Macromol 12:321–327CrossRefGoogle Scholar
  49. Kapitonov VV, Jurka J (2003) A novel class of SINE elements derived from 5S rRNA. Mol Biol Evol 20:694–702CrossRefPubMedGoogle Scholar
  50. Kluge AG (1989) A concern for evidence and a phylogenetic hypothesis of relationships among Epicrates (Boidae, Serpentes). Syst Zool 38:7–25CrossRefGoogle Scholar
  51. Kluge AG, Wolf AJ (1993) Cladistics: what’s in a word? Cladistics 9:183–199CrossRefGoogle Scholar
  52. Kouvela E, Gerbanas GV, Xaplanteri MA, Petropoulos AD, Dinos GP, Kalpaxis DL (2007) Changes in the conformation of 5S rRNA cause alternations in principal functions of the ribosomal nanomachine. Nucleic Acids Res 35:5108–5119CrossRefPubMedGoogle Scholar
  53. Küntzel H, Heidrich M, Piechulla B (1981) Phylogenetic tree derived from bacterial, cytosol and organelle 5S rRNA sequences. Nucleic Acids Res 9:1451–1461CrossRefPubMedGoogle Scholar
  54. Küntzel H, Piechulla B, Hahn U (1983) Consensus structure and evolution of 5S rRNA. Nucleic Acids Res 11:893–900CrossRefPubMedGoogle Scholar
  55. Lodmell JS, Dahlberg AE (1997) A conformational switch in Escherichia coli 16S ribosomal RNA during decoding of messenger RNA. Science 277:1262–1267CrossRefPubMedGoogle Scholar
  56. Luehrsen KR, Fox GE (1981) Secondary structure of eukaryotic cytoplasmic 5S ribosomal RNA. Proc Natl Acad Sci USA 78:2150–2154CrossRefPubMedGoogle Scholar
  57. 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 91:6729–6734CrossRefPubMedGoogle Scholar
  58. Mathews DH, Sabina J, Zuker M, Turner DH (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J Mol Biol 288:911–940CrossRefPubMedGoogle Scholar
  59. McDougall J, Wittmann-Liebold B (1994) Comparative analysis of the protein components from 5S rRNA—protein complexes of halophilic archaebacteria. Eur J Biochem 221:779–785CrossRefPubMedGoogle Scholar
  60. Murzin AG, Brenner SE, Hubbard T, Chothia C (1995) SCOP: a structural classification of proteins database for the investigation of sequences and structures. J Mol Biol 247:536–540PubMedGoogle Scholar
  61. Nearhos SP, Fuerst JA (1987) Reanalysis of 5S rRNA sequence data for the Vibrionaceae with the clustan program suite. Curr Microbiol 15:329–335CrossRefGoogle Scholar
  62. Nixon KC, Carpenter JM (1996) On simultaneous analysis. Cladistics 12:221–241CrossRefGoogle Scholar
  63. Okada S, Okada T, Aimi T, Morinaga T, Itoh T (2000) HSP70 and ribosomal protein L2: novel 5S rRNA binding proteins in Escherichia coli. FEBS Lett 485:153–156CrossRefPubMedGoogle Scholar
  64. Penny D, Poole A (1999) The nature of the last universal common ancestor. Curr Opin Genet Dev 9:672–677CrossRefPubMedGoogle Scholar
  65. Pollock D (2003) The Zuckerkandl Prize: structure and evolution. J Mol Evol 56:375–376Google Scholar
  66. Ramakrishnan V (2002) Ribosome structure and the mechanism of translation. Cell 108:557–572CrossRefPubMedGoogle Scholar
  67. Sergiev PV, Bogdanov AA, Dahlberg AE, Dontsova O (2000) Mutations at position A960 of E. coli 23S ribosomal RNA influence the structure of 5S ribosomal RNA and the peptidyltransferase region of 23 S ribosomal RNA. J Mol Biol 299:379–389CrossRefPubMedGoogle Scholar
  68. Smirnov AV, Entelis NS, Krasheninnikov IA, Martin R, Tarassov IA (2008) Specific features of 5S rRNA structure–Its interactions with macromolecules and possible functions. Biochemistry 73:1418–1437PubMedGoogle Scholar
  69. Smith N, Matheson AT, Yaguchi M, Willick GE, Nazar RN (1978) The 5S rRNA—protein complex from an extreme halophile Halobacterium cutirubrum: purification and characterization. Eur J Biochem 89:501–509CrossRefPubMedGoogle Scholar
  70. Steel M, Penny D (2000) Parsimony, likelihood, and the role of models in molecular phylogenetics. Mol Biol Evol 17:839–850PubMedGoogle Scholar
  71. Sun F-J, Caetano-Anollés G (2008a) The origin and evolution of tRNA inferred from phylogenetic analysis of structure. J Mol Evol 66:21–35CrossRefPubMedGoogle Scholar
  72. Sun F-J, Caetano-Anollés G (2008b) Evolutionary patterns in the sequence and structure of transfer RNA: early origins of Archaea and viruses. PLoS Comput Biol 4:e1000018CrossRefPubMedGoogle Scholar
  73. Sun F-J, Caetano-Anollés G (2008c) Evolutionary patterns in the sequence and structure of transfer RNA: a window into early translation and the genetic code. PLoS ONE 3:e2799CrossRefPubMedGoogle Scholar
  74. Sun F-J, Fleurdépine S, Bousquet-Antonelli C, Caetano-Anollés G, Deragon J-M (2007) Common evolutionary trends for SINE RNA structures. Trends Genet 23:26–33CrossRefPubMedGoogle Scholar
  75. Sun F-J, Harish A, Caetano-Anollés G (2009) Phylogenetic utility of RNA structure: evolution’s arrow and emergence of early biochemistry and diversified life. In: Caetano-Anollés G (ed), Evolutionary genomics and systems biology, Wiley, Hoboken (in press)Google Scholar
  76. Swofford DL (2003) PAUP*: phylogenetic analysis using parsimony (*and other methods), Version 4.0b10. Sinauer Associates, SunderlandGoogle Scholar
  77. Szymanski M, Barciszewska MZ, Erdmann VA, Barciszewski J (2002) 5S ribosomal RNA database. Nucleic Acids Res 30:176–178CrossRefPubMedGoogle Scholar
  78. Szymanski M, Barciszewska MZ, Erdmann VA, Barciszewski J (2003) 5 S rRNA: structure and interactions. Biochem J 371:641–651CrossRefPubMedGoogle Scholar
  79. Tanaka T, Kikuchi Y (2001) Origin of the cloverleaf shape of transfer RNA—the double-hairpin model: implication for the role of tRNA intron and the long extra loop. Viva Origino 29:134–142Google Scholar
  80. Teixido J, Altamura S, Londei P, Amils R (1989) Structural and functional exchangeability of 5S RNA species from the eubacterium E. coli and the thermoacidophilic archaebacterium Sulfolobus solfataricus. Nucleic Acids Res 17:845–851CrossRefPubMedGoogle Scholar
  81. Villanueva E, Luehrsen KR, Gibson J, Delihas N, Fox GE (1985) Phylogenetic origins of the plant mitochondrion based on a comparative analysis of 5S ribosomal RNA sequences. J Mol Evol 22:46–52CrossRefPubMedGoogle Scholar
  82. Wang M, Caetano-Anollés G (2006) Global phylogeny determined by the combination of protein domains in proteomes. Mol Biol Evol 23:2444–2454CrossRefPubMedGoogle Scholar
  83. Wang M, Caetano-Anollés G (2009) The evolutionary mechanics of domain organization in proteomes and the rise of modularity in the protein world. Structure 17:66–78CrossRefPubMedGoogle Scholar
  84. Wang M, Yafremava LS, Caetano-Anollés D, Mittenthal JE, Caetano-Anollés G (2007) Reductive evolution of architectural repertoires in proteomes and the birth of the tripartite world. Genome Res 17:1572–1585CrossRefPubMedGoogle Scholar
  85. 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 84:7383–7387CrossRefPubMedGoogle Scholar
  86. Widmann J, Di Giulio M, Yarus M, Knight R (2005) tRNA creation by hairpin duplication. J Mol Evol 61:24–535CrossRefGoogle Scholar
  87. Woese CR (1969) The biological significance of the genetic code. Prog Mol Subcell Biol 1:5–46Google Scholar
  88. Woese CR (1998) The universal ancestor. Proc Natl Acad Sci USA 95:6854–6859CrossRefPubMedGoogle Scholar
  89. Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for domains Archaea, Bacteria and Eucarya. Proc Natl Acad Sci USA 95:6854–6859CrossRefGoogle Scholar
  90. Wong JT-F, Chen J, Mat W-K, Ng S-K, Xue H (2007) Polyphasic evidence delineating the root of life and roots of biological domains. Gene 403:39–52CrossRefPubMedGoogle Scholar
  91. Wool IG (1986) Studies of the structure of eukaryotic (mammalian) ribosomes. In: Hardesty B, Kramer G (eds) Structure function and genetics of ribosomes. Springer, New York, pp 391–411Google Scholar
  92. Xue H, Tong K-L, Marck C, Grosjean H, Wong JT-F (2003) Transfer RNA paralogs: evidence for genetic code-amino acid biosynthesis coevolution and an archaeal root of life. Gene 310:59–66CrossRefPubMedGoogle Scholar
  93. Xue H, Ng S-K, Tong K-L, Wong JT-F (2005) Congruence of evidence for a Methanopyrus-proximal root of life based on transfer RNA and aminoacyl-tRNA synthetase genes. Gene 360:120–130CrossRefPubMedGoogle Scholar
  94. Yonath A (2002) The search and its outcome: high-resolution structures of ribosomal particles from mesophilic, thermophilic, and halophilic bacteria at various functional states. Annu Rev Biophys Biomol Struct 31:257–273CrossRefPubMedGoogle Scholar
  95. Yusupov MM, Yusupov GZ, Baucom A, Lieberman K, Earnest TN, Cate JHD, Noller HF (2001) Crystal structure of the ribosome at 5.5 Å resolution. Science 292:883–896CrossRefPubMedGoogle Scholar
  96. Zhaxybayeva O, Lapierre P, Gogarten JP (2005) Ancient gene duplications and the root(s) of the tree of life. Protoplasma 227:53–64CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Department of Crop SciencesUniversity of Illinois at Urbana-ChampaignUrbanaUSA
  2. 2.Laboratory of Molecular Epigenetics of the Ministry of Education, School of Life SciencesNortheast Normal UniversityChangchunPeople’s Republic of China
  3. 3.W.M. Keck Center for Comparative and Functional Genomics, Roy J. Carver Biotechnology CenterUniversity of IllinoisUrbanaUSA

Personalised recommendations