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.
Keywords: secondary structure diversity, tertiary structure diversity, 18S rRNA, Foraminifera, Euglenida
Contributor Information
Qiang Xie, Email: qiangxie@nankai.edu.cn.
Wenjun Bu, Email: wenjunbu@nankai.edu.cn.
References
- Baldauf S.L., Roger A.J., Wenk-Siefert I., Doolittle W.F. A kingdom-level phylogeny of eukaryotes based on combined protein data. Science. 2000;290:972–977. doi: 10.1126/science.290.5493.972. [DOI] [PubMed] [Google Scholar]
- Ban N., Nissen P., Hansen J., Moore P.B., Steitz T.A. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science. 2000;289:905–920. doi: 10.1126/science.289.5481.905. [DOI] [PubMed] [Google Scholar]
- Burki F., Berney C., Pawlowski J. Phylogenetic position of Gromia oviformis Dujardin inferred from nuclear-encoded small subunit ribosomal DNA. Protist. 2002;153:251–260. doi: 10.1078/1434-4610-00102. [DOI] [PubMed] [Google Scholar]
- Burki F., Pawlowski J. Monophyly of Rhizaria and multigene phylogeny of unicellular bikonts. Mol Biol Evol. 2006;23:1922–1930. doi: 10.1093/molbev/msl055. [DOI] [PubMed] [Google Scholar]
- Burki F., Shalchian-Tabrizi K., Minge M., Skjaeveland, Nikolaev S.I., Jakobsen K.S., Pawlowski J. Phylogenomics reshuffles the eukaryotic supergroups. PLoS One. 2007;2:e790. doi: 10.1371/journal.pone.0000790. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Busse I., Preisfeld A. Systematics of primary osmotrophic euglenids: a molecular approach to the phylogeny of Distigma and Astasia (Euglenozoa) Int J Syst Evol Microbiol. 2003;53:617–624. doi: 10.1099/ijs.0.02295-0. [DOI] [PubMed] [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. 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. 2002;3:2. doi: 10.1186/1471-2105-3-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cavalier-Smith T., Chao E.E. Molecular phylogeny of the free-living archezoan Trepomonas agilis and the nature of the first eukaryote. J Mol Evol. 1996;43:551–562. doi: 10.1007/BF02202103. [DOI] [PubMed] [Google Scholar]
- Chandramouli P., Topf M., Ménétret J.F., Eswar N., Cannone J.J., Gutell R.R., Sali A., Akey C.W. Structure of the mammalian 80S ribosome at 8.7 A resolution. Structure. 2008;16:535–548. doi: 10.1016/j.str.2008.01.007. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Crease T.J., Colbourne J.K. The unusually long small-subunit ribosomal RNA of the crustacean, Daphnia pulex: sequence and predicted secondary structure. J Mol Evol. 1998;46:307–313. doi: 10.1007/PL00006307. [DOI] [PubMed] [Google Scholar]
- Cunningham C.O., Aliesky H., Collins C.M. Sequence and secondary structure variation in the Gyrodactylus (Platyhelminthes: Monogenea) ribosomal RNA gene array. J Parasitol. 2000;86:567–576. doi: 10.1645/0022-3395(2000)086[0567:SASSVI]2.0.CO;2. [DOI] [PubMed] [Google Scholar]
- Giribet G., Wheeler W.C. Some unusual small-subunit ribosomal RNA sequences of Metazoans. Am Mus Novit. 2001;3337:1–16. doi: 10.1206/0003-0082(2001)337<0001:SUSSRR>2.0.CO;2. [DOI] [Google Scholar]
- Green R., Noller H.F. Ribosomes and translation. Annu Rev Biochem. 1997;66:679–716. doi: 10.1146/annurev.biochem.66.1.679. [DOI] [PubMed] [Google Scholar]
- Hackett J.D., Yoon H.S., Li S., Reyes-Prieto A., Rümmele S.E., Bhattacharya D. Phylogenomic analysis supports the monophyly of cryptophytes and haptophytes and the association of rhizaria with chromalveolates. Mol Biol Evol. 2007;24:1702–1713. doi: 10.1093/molbev/msm089. [DOI] [PubMed] [Google Scholar]
- Harms J., Schluenzen F., Zarivach R., Bashan A., Gat S., Agmon I., Bartels H., Franceschi F., Yonath A. High resolution structure of the large ribosomal subunit from a mesophilic eubacterium. Cell. 2001;107:679–688. doi: 10.1016/S0092-8674(01)00546-3. [DOI] [PubMed] [Google Scholar]
- Harper J.T., Waanders E., Keeling P.J. On the monophyly of chromalveolates using a six-protein phylogeny of eukaryotes. Int J Syst Evol Microbiol. 2005;55:487–496. doi: 10.1099/ijs.0.63216-0. [DOI] [PubMed] [Google Scholar]
- Hudelot C., Gowri-Shankar V., Jow H., Rattray M., Higgs P.G. RNA-based phylogenetic methods: application to mammalian mitochondrial RNA sequences. Mol Phylogenet Evol. 2003;28:241–252. doi: 10.1016/S1055-7903(03)00061-7. [DOI] [PubMed] [Google Scholar]
- Huelsenbeck J.P., Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17:754–755. doi: 10.1093/bioinformatics/17.8.754. [DOI] [PubMed] [Google Scholar]
- Jackson S.A., Cannone J.J., Lee J.C., Gutell R.R., Woodson S.A. Distribution of rRNA introns in the three-dimensional structure of the ribosome. J Mol Biol. 2002;323:35–52. doi: 10.1016/S0022-2836(02)00895-1. [DOI] [PubMed] [Google Scholar]
- Jobb G., von Haeseler A., Strimmer K. TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol. 2004;4:18. doi: 10.1186/1471-2148-4-18. [DOI] [PMC free article] [PubMed] [Google Scholar] [Retracted]
- Jow H., Hudelot C., Rattray M., Higgs P.G. Bayesian phylogenetics using an RNA substitution model applied to early mammalian evolution. Mol Biol Evol. 2002;19:1591–1601. doi: 10.1093/oxfordjournals.molbev.a004221. [DOI] [PubMed] [Google Scholar]
- Keeling P.J., Burger G., Durnford D.G., Lang B.F., Lee R.W., Pearlman R.E., Roger A.J., Gray M.W. The tree of eukaryotes. Trends Ecol Evol. 2005;20:670–676. doi: 10.1016/j.tree.2005.09.005. [DOI] [PubMed] [Google Scholar]
- Keller A., Förster F., Müller T., Dandekar T., Schultz J., Wolf M. Including RNA secondary structures improves accuracy and robustness in reconstruction of phylogenetic trees. Biol Direct. 2010;5:4. doi: 10.1186/1745-6150-5-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kim E., Graham L.E. EEF2 analysis challenges the monophyly of Archaeplastida and Chromalveolata. PLoS One. 2008;3:e2621. doi: 10.1371/journal.pone.0002621. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kostka M., Hampl V., Cepicka I., Flegr J. Phylogenetic position of Protoopalina intestinalis based on SSU rRNA gene sequence. Mol Phylogenet Evol. 2004;33:220–224. doi: 10.1016/j.ympev.2004.05.009. [DOI] [PubMed] [Google Scholar]
- Kumar S., Rzhetsky A. Evolutionary relationships of eukaryotic kingdoms. J Mol Evol. 1996;42:183–193. doi: 10.1007/BF02198844. [DOI] [PubMed] [Google Scholar]
- Margulis L. Origin of Eukaryotic Cells. New Haven, Connecticut: Yale University Press; 1970. [Google Scholar]
- Mathews D.H., Disney M.D., Childs J.L., Schroeder S.J., Zuker M., Turner D.H. Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. Proc Natl Acad Sci U S A. 2004;101:7287–7292. doi: 10.1073/pnas.0401799101. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Neefs J.M., Van de Peer Y., De Rijk P., Goris A., De Wachter R. Compilation of small ribosomal subunit RNA sequences. Nucleic Acids Res. 1991;19:1987–2015. doi: 10.1093/nar/19.suppl.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nikolaev S.I., Berney C., Fahrni J.F., Bolivar I., Polet S., Mylnikov A.P., Aleshin V.V., Petrov N.B., Pawlowski J. The twilight of Heliozoa and rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes. Proc Natl Acad Sci U S A. 2004;101:8066–8071. doi: 10.1073/pnas.0308602101. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nissen P., Hansen J., Ban N., Moore P.B., Steitz T.A. The structural basis of ribosome activity in peptide bond synthesis. Science. 2000;289:920–930. doi: 10.1126/science.289.5481.920. [DOI] [PubMed] [Google Scholar]
- Noller H.F. Ribosomal RNA and translation. Annu Rev Biochem. 1991;60:191–227. doi: 10.1146/annurev.bi.60.070191.001203. [DOI] [PubMed] [Google Scholar]
- Noller H.F. RNA structure: reading the ribosome. Science. 2005;309:1508–1514. doi: 10.1126/science.1111771. [DOI] [PubMed] [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., Katz L.A. Evaluating support for the current classification of eukaryotic diversity. PLoS Genet. 2006;2:e220. doi: 10.1371/journal.pgen.0020220. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Patron N.J., Inagaki Y., Keeling P.J. Multiple gene phylogenies support the monophyly of cryptomonad and haptophyte host lineages. Curr Biol. 2007;17:887–891. doi: 10.1016/j.cub.2007.03.069. [DOI] [PubMed] [Google Scholar]
- Pawlowski J., Holzmann M., Berney C., Fahrni J., Gooday A.J., Cedhagen T., Habura A., Bowser S.S. The evolution of early Foraminifera. Proc Natl Acad Sci U S A. 2003;100:11494–11498. doi: 10.1073/pnas.2035132100. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Philippe H., Snell E.A., Bapteste E., Lopez P., Holland P.W., Casane D. Phylogenomics of eukaryotes: impact of missing data on large alignments. Mol Biol Evol. 2004;21:1740–1752. doi: 10.1093/molbev/msh182. [DOI] [PubMed] [Google Scholar]
- Polet S., Berney C., Fahrni J., Pawlowski J. Small-subunit ribosomal RNA gene sequences of Phaeodarea challenge the monophyly of Haeckel’s Radiolaria. Protist. 2004;155:53–63. doi: 10.1078/1434461000164. [DOI] [PubMed] [Google Scholar]
- Ramakrishnan V. Ribosome structure and the mechanism of translation. Cell. 2002;108:557–572. doi: 10.1016/S0092-8674(02)00619-0. [DOI] [PubMed] [Google Scholar]
- Rodríguez-Ezpeleta N., Brinkmann H., Burey S.C., Roure B., Burger G., Löffelhardt W., Bohnert H.J., Philippe H., Lang B. F. Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr Biol. 2005;15:1325–1330. doi: 10.1016/j.cub.2005.06.040. [DOI] [PubMed] [Google Scholar]
- Ronquist F., Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19:1572–1574. doi: 10.1093/bioinformatics/btg180. [DOI] [PubMed] [Google Scholar]
- Schluenzen F., Tocilj A., Zarivach R., Harms J., Gluehmann M., Janell D., Bashan A., Bartels H., Agmon I., Franceschi F., et al. Structure of functionally activated small ribosomal subunit at 3.3 angstroms resolution. Cell. 2000;102:615–623. doi: 10.1016/S0092-8674(00)00084-2. [DOI] [PubMed] [Google Scholar]
- Schöniger M., von Haeseler A. A stochastic model for the evolution of autocorrelated DNA sequences. Mol Phylogenet Evol. 1994;3:240–247. doi: 10.1006/mpev.1994.1026. [DOI] [PubMed] [Google Scholar]
- Schultz J., Wolf M. ITS2 sequence-structure analysis in phylogenetics: a how-to manual for molecular systematics. Mol Phylogenet Evol. 2009;52:520–523. doi: 10.1016/j.ympev.2009.01.008. [DOI] [PubMed] [Google Scholar]
- Seibel P.N., Müller T., Dandekar T., Schultz J., Wolf M. 4SALE—a tool for synchronous RNA sequence and secondary structure alignment and editing. BMC Bioinformatics. 2006;7:498. doi: 10.1186/1471-2105-7-498. [DOI] [PMC free article] [PubMed] [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. Telonemia, a new protist phylum with affinity to chromist lineages. Proc Biol Sci. 2006;273:1833–1842. doi: 10.1098/rspb.2006.3515. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shalchian-Tabrizi K., Kauserud H., Massana R., Klaveness D., Jakobsen K.S. Analysis of environmental 18S ribosomal RNA sequences reveals unknown diversity of the cosmopolitan phylum Telonemia. Protist. 2007;158:173–180. doi: 10.1016/j.protis.2006.10.003. [DOI] [PubMed] [Google Scholar]
- Siebert S., Backofen R. MARNA: multiple alignment and consensus structure prediction of RNAs based on sequence structure comparisons. Bioinformatics. 2005;21:3352–3359. doi: 10.1093/bioinformatics/bti550. [DOI] [PubMed] [Google Scholar]
- Spahn C.M.T., Beckmann R., Eswar N., Penczek P.A., Sali A., Blobel G., Frank J. Structure of the 80S ribosome from Saccharomyces cerevisiae—tRNA-ribosome and subunitsubunit interactions. Cell. 2001;107:373–386. doi: 10.1016/S0092-8674(01)00539-6. [DOI] [PubMed] [Google Scholar]
- Stocsits R.R., Letsch H., Hertel J., Misof B., Stadler P.F. Accurate and efficient reconstruction of deep phylogenies from structured RNAs. Nucleic Acids Res. 2009;37:6184–6193. doi: 10.1093/nar/gkp600. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sweeney R., Chen L., Yao M.C. An rRNA variable region has an evolutionarily conserved essential role despite sequence divergence. Mol Cell Biol. 1994;14:4203–4215. doi: 10.1128/MCB.14.6.4203. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Telford M.J., Wise M.J., Gowri-Shankar V. Consideration of RNA secondary structure significantly improves likelihood-based estimates of phylogeny: examples from the bilateria. Mol Biol Evol. 2005;22:1129–1136. doi: 10.1093/molbev/msi099. [DOI] [PubMed] [Google Scholar]
- Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The ClustalX windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997;24:4876–4882. doi: 10.1093/nar/25.24.4876. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Van de Peer Y., De Wachter R. Evolutionary relationships among the eukaryotic crown taxa taking into account site-to-site rate variation in 18S rRNA. J Mol Evol. 1997;45:619–630. doi: 10.1007/PL00006266. [DOI] [PubMed] [Google Scholar]
- Wimberly B.T., Brodersen D.E., Clemons W.M., Jr, Morgan-Warren R.J., Carter A.P., Vonrhein C., Hartsch T., Ramakrishnan V. Structure of the 30S ribosomal subunit. Nature. 2000;407:327–339. doi: 10.1038/35030006. [DOI] [PubMed] [Google Scholar]
- Wolf M., Ruderisch B., Dandekar T., Schultz J., Müller T. ProfDistS: (profile-) distance based phylogeny on sequence—structure alignments. Bioinformatics. 2008;24:2401–2402. doi: 10.1093/bioinformatics/btn453. [DOI] [PubMed] [Google Scholar]
- Wuyts J., Perrière G., Van De Peer Y. The European ribosomal RNA database. Nucleic Acids Res. 2004;32:D101–D103. doi: 10.1093/nar/gkh065. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wuyts J., Van de Peer Y., De Wachter R. Distribution of substitution rates and location of insertion sites in the tertiary structure of ribosomal RNA. Nucleic Acids Res. 2001;29:5017–5028. doi: 10.1093/nar/29.24.5017. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Xie Q., Tian X., Qin Y., Bu W. 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. 2009;50:310–316. doi: 10.1016/j.ympev.2008.10.025. [DOI] [PubMed] [Google Scholar]
- Xie Q., Tian Y., Zheng L., Bu W. 18S rRNA hyperelongation and the phylogeny of Euhemiptera (Insecta: Hemiptera) Mol Phylogenet Evol. 2008;47:463–471. doi: 10.1016/j.ympev.2008.01.024. [DOI] [PubMed] [Google Scholar]
- Yusupov M.M., Yusupova G.Z.H., Baucom A., Lieberman K., Earnest T.N., Cate J.H.D., Noller H.F. Crystal structure of the ribosome at 5.5 A resolution. Science. 2001;292:883–896. doi: 10.1126/science.1060089. [DOI] [PubMed] [Google Scholar]