Skip to main content
Download PDF

Structural diversity of eukaryotic 18S rRNA and its impact on alignment and phylogenetic reconstruction

Protein & Cell volume 2, pages 161–170 (2011)Cite this article

Abstract

Ribosomal RNAs are important because they catalyze the synthesis of peptides and proteins. Comparative studies of the secondary structure of 18S rRNA have revealed the basic locations of its many length-conserved and length-variable regions. In recent years, many more sequences of 18S rDNA with unusual lengths have been documented in GenBank. These data make it possible to recognize the diversity of the secondary and tertiary structures of 18S rRNAs and to identify the length-conserved parts of 18S rDNAs. The longest 18S rDNA sequences of almost every known eukaryotic phylum were included in this study. We illustrated the bioinformatics-based structure to show that, the regions that are more length-variable, regions that are less length-variable, the splicing sites for introns, and the sites of A-minor interactions are mostly distributed in different parts of the 18S rRNA. Additionally, this study revealed that some length-variable regions or insertion positions could be quite close to the functional part of the 18S rRNA of Foraminifera organisms. The tertiary structure as well as the secondary structure of 18S rRNA can be more diverse than what was previously supposed. Besides revealing how this interesting gene evolves, it can help to remove ambiguity from the alignment of eukaryotic 18S rDNAs and to improve the performance of 18S rDNA in phylogenetic reconstruction. Six nucleotides shared by Archaea and Eukaryota but rarely by Bacteria are also reported here for the first time, which might further support the supposed origin of eukaryote from archaeans.

References

  • Baldauf, S.L., Roger, A.J., Wenk-Siefert, I., and Doolittle, W.F. (2000). A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290, 972–977.

    Article  Google Scholar 

  • Ban, N., Nissen, P., Hansen, J., Moore, P.B., and Steitz, T.A. (2000). The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science 289, 905–920.

    Article  Google Scholar 

  • Burki, F., Berney, C., and Pawlowski, J. (2002). Phylogenetic position of Gromia oviformis Dujardin inferred from nuclear-encoded small subunit ribosomal DNA. Protist 153, 251–260.

    Article  Google Scholar 

  • Burki, F., and Pawlowski, J. (2006). Monophyly of Rhizaria and multigene phylogeny of unicellular bikonts. Mol Biol Evol 23, 1922–1930.

    Article  Google Scholar 

  • Burki, F., Shalchian-Tabrizi, K., Minge, M., Skjaeveland, Å., Nikolaev, S.I., Jakobsen, K.S., and Pawlowski, J. (2007). Phylogenomics reshuffles the eukaryotic supergroups. PLoS One 2, e790.

    Article  Google Scholar 

  • Busse, I., and Preisfeld, A. (2003). Systematics of primary osmotrophic euglenids: a molecular approach to the phylogeny of Distigma and Astasia (Euglenozoa). Int J Syst Evol Microbiol 53, 617–624.

    Article  Google Scholar 

  • Cannone, J.J., Subramanian, S., Schnare, M.N., Collett, J.R., D’souza, L.M., Du, Y., Feng, B., Lin, N., Madabusi, L.V., Müller, K.M., et al. (2002). The comparative RNA web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. [Correction: BMC Bioinformatics 3, 15.] BMC Bioinformatics 3, 2.

    Article  Google Scholar 

  • Cavalier-Smith, T., and Chao, E.E. (1996). Molecular phylogeny of the free-living archezoan Trepomonas agilis and the nature of the first eukaryote. J Mol Evol 43, 551–562.

    Article  Google Scholar 

  • Chandramouli, P., Topf, M., Ménétret, J.F., Eswar, N., Cannone, J.J., Gutell, R.R., Sali, A., and Akey, C.W. (2008). Structure of the mammalian 80S ribosome at 8.7 A resolution. Structure 16, 535–548.

    Article  Google Scholar 

  • Crease, T.J., and Colbourne, J.K. (1998). The unusually long small-subunit ribosomal RNA of the crustacean, Daphnia pulex: sequence and predicted secondary structure. J Mol Evol 46, 307–313.

    Article  Google Scholar 

  • Cunningham, C.O., Aliesky, H., and Collins, C.M. (2000). Sequence and secondary structure variation in the Gyrodactylus (Platyhelminthes: Monogenea) ribosomal RNA gene array. J Parasitol 86, 567–576.

    Article  Google Scholar 

  • Giribet, G., and Wheeler, W.C. (2001). Some unusual small-subunit ribosomal RNA sequences of Metazoans. Am Mus Novit 3337, 1–16.

    Article  Google Scholar 

  • Green, R., and Noller, H.F. (1997). Ribosomes and translation. Annu Rev Biochem 66, 679–716.

    Article  Google Scholar 

  • Hackett, J.D., Yoon, H.S., Li, S., Reyes-Prieto, A., Rümmele, S.E., and Bhattacharya, D. (2007). Phylogenomic analysis supports the monophyly of cryptophytes and haptophytes and the association of rhizaria with chromalveolates. Mol Biol Evol 24, 1702–1713.

    Article  Google Scholar 

  • Harms, J., Schluenzen, F., Zarivach, R., Bashan, A., Gat, S., Agmon, I., Bartels, H., Franceschi, F., and Yonath, A. (2001). High resolution structure of the large ribosomal subunit from a mesophilic eubacterium. Cell 107, 679–688.

    Article  Google Scholar 

  • Harper, J.T., Waanders, E., and Keeling, P.J. (2005). On the monophyly of chromalveolates using a six-protein phylogeny of eukaryotes. Int J Syst Evol Microbiol 55, 487–496.

    Article  Google Scholar 

  • Hudelot, C., Gowri-Shankar, V., Jow, H., Rattray, M., and Higgs, P.G. (2003). RNA-based phylogenetic methods: application to mammalian mitochondrial RNA sequences. Mol Phylogenet Evol 28, 241–252.

    Article  Google Scholar 

  • Huelsenbeck, J.P., and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.

    Article  Google Scholar 

  • Jackson, S.A., Cannone, J.J., Lee, J.C., Gutell, R.R., and Woodson, S.A. (2002). Distribution of rRNA introns in the three-dimensional structure of the ribosome. J Mol Biol 323, 35–52.

    Article  Google Scholar 

  • Jobb, G., von Haeseler, A., and Strimmer, K. (2004). TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol 4, 18.

    Article  Google Scholar 

  • Jow, H., Hudelot, C., Rattray, M., and Higgs, P.G. (2002). Bayesian phylogenetics using an RNA substitution model applied to early mammalian evolution. Mol Biol Evol 19, 1591–1601.

    Article  Google Scholar 

  • Keeling, P.J., Burger, G., Durnford, D.G., Lang, B.F., Lee, R.W., Pearlman, R.E., Roger, A.J., and Gray, M.W. (2005). The tree of eukaryotes. Trends Ecol Evol 20, 670–676.

    Article  Google Scholar 

  • Keller, A., Förster, F., Müller, T., Dandekar, T., Schultz, J., and Wolf, M. (2010). Including RNA secondary structures improves accuracy and robustness in reconstruction of phylogenetic trees. Biol Direct 5, 4.

    Article  Google Scholar 

  • Kim, E., and Graham, L.E. (2008). EEF2 analysis challenges the monophyly of Archaeplastida and Chromalveolata. PLoS One 3, e2621.

    Article  Google Scholar 

  • Kostka, M., Hampl, V., Cepicka, I., and Flegr, J. (2004). Phylogenetic position of Protoopalina intestinalis based on SSU rRNA gene sequence. Mol Phylogenet Evol 33, 220–224.

    Article  Google Scholar 

  • Kumar, S., and Rzhetsky, A. (1996). Evolutionary relationships of eukaryotic kingdoms. J Mol Evol 42, 183–193.

    Article  Google Scholar 

  • Margulis, L. (1970). Origin of Eukaryotic Cells. New Haven, Connecticut: Yale University Press.

    Google Scholar 

  • Mathews, D.H., Disney, M.D., Childs, J.L., Schroeder, S.J., Zuker, M., and Turner, D.H. (2004). Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. Proc Natl Acad Sci U S A 101, 7287–7292.

    Article  Google Scholar 

  • Neefs, J.M., Van de Peer, Y., De Rijk, P., Goris, A., and De Wachter, R. (1991). Compilation of small ribosomal subunit RNA sequences. Nucleic Acids Res 19, 1987–2015.

    Article  Google Scholar 

  • Nikolaev, S.I., Berney, C., Fahrni, J.F., Bolivar, I., Polet, S., Mylnikov, A.P., Aleshin, V.V., Petrov, N.B., and Pawlowski, J. (2004). The twilight of Heliozoa and rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes. Proc Natl Acad Sci U S A 101, 8066–8071.

    Article  Google Scholar 

  • Nissen, P., Hansen, J., Ban, N., Moore, P.B., and Steitz, T.A. (2000). The structural basis of ribosome activity in peptide bond synthesis. Science 289, 920–930.

    Article  Google Scholar 

  • Noller, H.F. (1991). Ribosomal RNA and translation. Annu Rev Biochem 60, 191–227.

    Article  Google Scholar 

  • Noller, H.F. (2005). RNA structure: reading the ribosome. Science 309, 1508–1514.

    Article  Google Scholar 

  • Parallel Mrbayes@BioHPC. (2011). http://cbsuapps.tc.cornell.edu/mrbayes.aspx

  • Parfrey, L.W., Barbero, E., Lasser, E., Dunthorn, M., Bhattacharya, D., Patterson, D.J., and Katz, L.A. (2006). Evaluating support for the current classification of eukaryotic diversity. PLoS Genet 2, e220.

    Article  Google Scholar 

  • Patron, N.J., Inagaki, Y., and Keeling, P.J. (2007). Multiple gene phylogenies support the monophyly of cryptomonad and haptophyte host lineages. Curr Biol 17, 887–891.

    Article  Google Scholar 

  • Pawlowski, J., Holzmann, M., Berney, C., Fahrni, J., Gooday, A.J., Cedhagen, T., Habura, A., and Bowser, S.S. (2003). The evolution of early Foraminifera. Proc Natl Acad Sci U S A 100, 11494–11498.

    Article  Google Scholar 

  • Philippe, H., Snell, E.A., Bapteste, E., Lopez, P., Holland, P.W., and Casane, D. (2004). Phylogenomics of eukaryotes: impact of missing data on large alignments. Mol Biol Evol 21, 1740–1752.

    Article  Google Scholar 

  • Polet, S., Berney, C., Fahrni, J., and Pawlowski, J. (2004). Small-subunit ribosomal RNA gene sequences of Phaeodarea challenge the monophyly of Haeckel’s Radiolaria. Protist 155, 53–63.

    Article  Google Scholar 

  • Ramakrishnan, V. (2002). Ribosome structure and the mechanism of translation. Cell 108, 557–572.

    Article  Google Scholar 

  • Rodríguez-Ezpeleta, N., Brinkmann, H., Burey, S.C., Roure, B., Burger, G., Löffelhardt, W., Bohnert, H.J., Philippe, H., and Lang, B. F. (2005). Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr Biol 15, 1325–1330.

    Article  Google Scholar 

  • Ronquist, F., and Huelsenbeck, J.P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.

    Article  Google Scholar 

  • Schluenzen, F., Tocilj, A., Zarivach, R., Harms, J., Gluehmann, M., Janell, D., Bashan, A., Bartels, H., Agmon, I., Franceschi, F., et al. (2000). Structure of functionally activated small ribosomal subunit at 3.3 angstroms resolution. Cell 102, 615–623.

    Article  Google Scholar 

  • Schöniger, M., and von Haeseler, A. (1994). A stochastic model for the evolution of autocorrelated DNA sequences. Mol Phylogenet Evol 3, 240–247.

    Article  Google Scholar 

  • Schultz, J., and Wolf, M. (2009). ITS2 sequence-structure analysis in phylogenetics: a how-to manual for molecular systematics. Mol Phylogenet Evol 52, 520–523.

    Article  Google Scholar 

  • Seibel, P.N., Müller, T., Dandekar, T., Schultz, J., and Wolf, M. (2006). 4SALE—a tool for synchronous RNA sequence and secondary structure alignment and editing. BMC Bioinformatics 7, 498.

    Article  Google Scholar 

  • Shalchian-Tabrizi, K., Eikrem, W., Klaveness, D., Vaulot, D., Minge, M.A., Le Gall, F., Romari, K., Throndsen, J., Botnen, A., Massana, R., et al. (2006). Telonemia, a new protist phylum with affinity to chromist lineages. Proc Biol Sci 273, 1833–1842.

    Article  Google Scholar 

  • Shalchian-Tabrizi, K., Kauserud, H., Massana, R., Klaveness, D., and Jakobsen, K.S. (2007). Analysis of environmental 18S ribosomal RNA sequences reveals unknown diversity of the cosmopolitan phylum Telonemia. Protist 158, 173–180.

    Article  Google Scholar 

  • Siebert, S., and Backofen, R. (2005). MARNA: multiple alignment and consensus structure prediction of RNAs based on sequence structure comparisons. Bioinformatics 21, 3352–3359.

    Article  Google Scholar 

  • Spahn, C.M.T., Beckmann, R., Eswar, N., Penczek, P.A., Sali, A., Blobel, G., and Frank, J. (2001). Structure of the 80S ribosome from Saccharomyces cerevisiae—tRNA-ribosome and subunitsubunit interactions. Cell 107, 373–386.

    Article  Google Scholar 

  • Stocsits, R.R., Letsch, H., Hertel, J., Misof, B., and Stadler, P.F. (2009). Accurate and efficient reconstruction of deep phylogenies from structured RNAs. Nucleic Acids Res 37, 6184–6193.

    Article  Google Scholar 

  • Sweeney, R., Chen, L., and Yao, M.C. (1994). An rRNA variable region has an evolutionarily conserved essential role despite sequence divergence. Mol Cell Biol 14, 4203–4215.

    Article  Google Scholar 

  • Telford, M.J., Wise, M.J., and Gowri-Shankar, V. (2005). Consideration of RNA secondary structure significantly improves likelihood-based estimates of phylogeny: examples from the bilateria. Mol Biol Evol 22, 1129–1136.

    Article  Google Scholar 

  • Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. (1997). The ClustalX windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24, 4876–4882.

    Article  Google Scholar 

  • Van de Peer, Y., and De Wachter, R. (1997). Evolutionary relationships among the eukaryotic crown taxa taking into account site-to-site rate variation in 18S rRNA. J Mol Evol 45, 619–630.

    Article  Google Scholar 

  • Wimberly, B.T., Brodersen, D.E., Clemons, W.M. Jr, Morgan-Warren, R.J., Carter, A.P., Vonrhein, C., Hartsch, T., and Ramakrishnan, V. (2000). Structure of the 30S ribosomal subunit. Nature 407, 327–339.

    Article  Google Scholar 

  • Wolf, M., Ruderisch, B., Dandekar, T., Schultz, J., and Müller, T. (2008). ProfDistS: (profile-) distance based phylogeny on sequence—structure alignments. Bioinformatics 24, 2401–2402.

    Article  Google Scholar 

  • Wuyts, J., Perrière, G., and Van De Peer, Y. (2004). The European ribosomal RNA database. Nucleic Acids Res 32, D101–D103.

    Article  Google Scholar 

  • Wuyts, J., Van de Peer, Y., and De Wachter, R. (2001). Distribution of substitution rates and location of insertion sites in the tertiary structure of ribosomal RNA. Nucleic Acids Res 29, 5017–5028.

    Article  Google Scholar 

  • Xie, Q., Tian, X., Qin, Y., and Bu, W. (2009). Phylogenetic comparison of local length plasticity of the small subunit of nuclear rDNAs among all Hexapoda orders and the impact of hyper-length-variation on alignment. Mol Phylogenet Evol 50, 310–316.

    Article  Google Scholar 

  • Xie, Q., Tian, Y., Zheng, L., and Bu, W. (2008). 18S rRNA hyperelongation and the phylogeny of Euhemiptera (Insecta: Hemiptera). Mol Phylogenet Evol 47, 463–471.

    Article  Google Scholar 

  • Yusupov, M.M., Yusupova, G.Z.H., Baucom, A., Lieberman, K., Earnest, T.N., Cate, J.H.D., and Noller, H.F. (2001). Crystal structure of the ribosome at 5.5 A resolution. Science 292, 883–896.

    Article  Google Scholar 

Download references

Author information

Affiliations

  1. Department of Zoology and Developmental Biology, College of Life Sciences, Nankai University, Tianjin, 300071, China

    Qiang Xie & Wenjun Bu

  2. National Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101, China

    Jinzhong Lin & Yan Qin

  3. College of Information Technical Science, Nankai University, 94 Weijin Road, Tianjin, 300071, China

    Jianfu Zhou

Authors
  1. Qiang Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jinzhong Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yan Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jianfu Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wenjun Bu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Qiang Xie or Wenjun Bu.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Xie, Q., Lin, J., Qin, Y. et al. Structural diversity of eukaryotic 18S rRNA and its impact on alignment and phylogenetic reconstruction. Protein Cell 2, 161–170 (2011). https://doi.org/10.1007/s13238-011-1017-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13238-011-1017-2

Keywords

  • secondary structure diversity
  • tertiary structure diversity
  • 18S rRNA
  • Foraminifera
  • Euglenida