Abstract
The modern ribosome and its component RNAs are quite large and it is likely that at an earlier time they were much smaller. Hence, not all regions of the modern ribosomal RNAs (rRNA) are likely to be equally old. In the work described here, it is hypothesized that the oldest regions of the RNAs will usually be highly integrated into the machinery. When this is the case, an examination of the interconnectivity between local RNA regions can provide insight to the relative age of the various regions. Herein, we describe an analysis of all known long-range RNA/RNA interactions within the 23S rRNA and between the 23S rRNA and the 16S rRNA in order to assess the interconnectivity between the usual Domains as defined by secondary structure. Domain V, which contains the peptidyl transferase center is centrally located, extensively connected, and therefore likely to be the oldest region. Domain IV and Domain II are extensively interconnected with both themselves and Domain V. A portion of Domain IV is also extensively connected with the 30S subunit and hence Domain IV may be older than Domain II. These results are consistent with other evidence relating to the relative age of RNA regions. Although the relative time of addition of the GTPase center can not be reliably deduced it is pointed out that the development of this may have dramatically affected the progenotes that preceded the last common ancestor.
Article PDF
Similar content being viewed by others
References
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.
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 (2002) The Comparative RNA Web (CRW) Site: An online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics 3:2.
Clark CG (1987) On the evolution of ribosomal RNA. J Molec Evol 25:343–350.
Fox GE, Naik AK (2004) The Evolutionary History of the Ribosome. IN: Ribas de Poplana, L. (Ed.). The Genetic Code and the Origin of Life. Landes Bioscience, Georgetown and New York, pp. 92–105.
Gavrilova LP, Spirin AS (1971) Stimulation of “non-enzymic” translocation in ribosomes by p-chloromercuribenzoate. FEBS Lett 17:324–326.
Gavrilova LP, Kostiashkina OE, Koteliansky VE, Rutkevich NM, Spirin AS (1976) Factor-free (“Non-enzymic”) and factor-dependent systems of translation of polyuridylic acid by Escherichia coli ribosomes. J Mol Biol 101:537–552.
Guex N, Peitsch MC (1997) SWISS_MODEL and the Swiss-Pdb Viewer: An environment for comparative protein modeling. Electrophoresis 18:2714–2723.
Gonzalo P, Reboud JP (2003) The puzzling lateral flexible stalk of the ribosome. Biol Cell 95:179–193.
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.
Mears JA, Cannone JJ, Stagg SM, Gutell RR, Agrawal RK, Harvey SC (2002) Modeling a minimal ribosome based on comparative sequence analysis. J Mol Biol 321:215–234.
Mushegian A (2005) Protein content of minimal and ancestral ribosome. RNA 11:1400–1406.
Nierhaus KH (1991) The assembly of prokaryotic ribosomes. Biochimie 73:739–755.
Nissen P, Hansen J, Moore PB, Steitz TA (2000) The structural basis of ribosomal activity in peptide bond synthesis. Science 289:920–930.
Olsen GJ, Woese CR (1997) Archaeal genomics: An overview. Cell 89:991–994.
Sloof P, Van den Burg J, Voogd A, Benne R, Agostinelli M, Borst P, Gutell R, Noller H (1985) Further characterization of the extremely small mitochondrial ribosomal RNAs from trypanosomes: A detailed comparison of the 9S and 12S RNAs from Crithidia fasciculata and Trypanosoma brucei with rRNAs from other organisms. Nucleic Acids Res 13:4171–4190.
Sopori ML, Lengyel P (1972) Components of the 50S ribosomal subunit involved in GTP cleavage. Biochem Biophys Res Commun 46:238–244.
Spahn CM, Nierhaus KH (1998) Models of the elongation cycle: An evaluation. Biol Chem 379:753–772.
Spirin AS (2002) Ribosome as a molecular machine. FEBS Lett 514:2–10.
Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: The primary kingdoms. Proc Natl Acad Sci USA 74:5088–5090.
Wilson KS, Noller HF (1998) Mapping the position of translational elongation factor EF-G in the ribosome by directed hydroxyl radical probing. Cell 92:131–139.
Wimberly BT, Guymon R, McCutcheon JP, White SW, Ramakrishnan V (1999) A detailed view of a ribosomal active site: The structure of the L11-RNA complex. Cell 97:491–502.
Wuyts J, Van de Peer Y, De Watcher R (2001) Distribution of substitution rates and location of insertion sites in the tertiary structure of ribosomal RNA. Nucleic Acids Res 29:5017–5028.
Yusupov MM, Yusupova GZ, Baucom A, Leiberman K, Earnest TN, Cate JH, Noller HK (2001) Crystal structure of the ribsome at 5.5 A resolution. Science 292:883–896.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hury, J., Nagaswamy, U., Larios-Sanz, M. et al. Ribosome origins: The relative age of 23S rRNA Domains. Orig Life Evol Biosph 36, 421–429 (2006). https://doi.org/10.1007/s11084-006-9011-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11084-006-9011-z