Gutell 030.nar.1993.21.03051


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Gutell 030.nar.1993.21.03051

  1. 1. Nucleic Acids Research, 1993, Vol. 21, No. 13 3051-3054Collection of small subunit (16S- and 16S-like) ribosomalRNA structuresRobin Ray GutellMCB Biology, Campus Box 347, University of Colorado, Boulder, CO 80309-0347, USAINTRODUCTIONInferring higher-order structure for complex RNA molecules,such as the ribosomal RNAs has relied primarily on comparativemethods. Underlying these methods is the premise that moleculeswith different primary structure and similar functionalcharacteristics have similar secondary and tertiary structure[Reviewed in: 1]. For these methods to be effective, the RNAmolecules under study need to be sufficiently similar at theprimary structure level to obtain good sequence alignments,however these same sequences also need to be proportionatelydifferent for positional covariance to occur, the indicatorsuggesting the existence of a basepair.The higher-order structure models for 16S rRNA have evolvedin stages. Initially, with a small number of 16S rRNA sequencesin hand, a minimal secondary structure was proposed. Increasesin the number and diversity of available 16S rRNA sequencesand paralleled with improvements in correlation analysisalgorithms has lead to the continual refinement of this structuremodel. In the earlier stages only secondary structure pairings wereidentified. In contrast during the latter stages only minorrefinements in these pairings occurred while several novel tertaryand non-canonical pairing constraints were proposed [reviewedin: 2-3]. And now with over 2,200 16S and 16S-like rRNAavailable sequences spanning the three phylogenetic domains andthe two organelles (Mitochondria and Chloroplast), detailedphylogenetic, structural, and structural evolution information isnow being deciphered in great detail, although the resultinganalysis from different groups is not always congruent.Over the years several groups have developed 16S rRNAsecondary structure models. The current versions for each arefairly analogous with one another[2, 4-7], although this has notalways been the case. And while the current differences are small,some are significant for the Escherichia coli and other Bacterial,Archaea, Eucarya, and mitochondrial structure models. Theseversions should also not be considered final as these models areexpected to undergo minor revisions as the number and diversityof 16S and 16S-like sequences increases and is paralleled withcontinued improvements and alternative correlation analysisinterpretations [8, unpublished work].Over the next few years this collection, and the accompanying23S rRNA (see Gutell, Gray, Schnare, this issue) will grow insize and detail. The complexity of structure and the evolutionarydimension of these structures presents us with a wonderfulopportunity to investigate RNA structural motifs and map withsome precision, the evolution ofthese RNAs and underlying RNAstructural characteristics associated with different phylogeneticassemblages. This collection of structures should also be ofvalueto the experimentalist studying rRNA structure and function. Andequally valuable to those studying rRNA based phylogeny.OBJECTIVESThe objectives for this annual collection are:1. Present our most current comparative interpretation of theEscherichia coli 16S rRNA secondary structure [withgeneral agreement between C.R.Woese, H.F.Noller, andmyselfl. While this secondary structure model is stable,minor adjustments are expected in some of the helicalpairings.2. Present other significant correlations that suggest tertiaryand other complex structure in the Escherichia coli model.The numbers for such structural interactions should increaseover the next few years.3. Present a sampling of different 16S and 16S-like rRNAhigher-order structure models. Starting with a broadsampling of phylogenetically and structurally distinctmodels, additional examples will be developed to fill in thisbroad phylogenetic and structure matrix. A parallel effortwill refine all previously proposed models as newcomparative structure information is obtained. To bediscussed elsewhere and in more detail, this collection ofstructures will serve as the database for detailed analysisof RNA evolution and RNA structural motifs.The first 16S and 16Slike structure release is set forsummer/fall- 1993, and will include major representativesfrom the three phylogenetic domains and organelles. Theapproximate numbers will be: 25 (eu)bacteria, 10 archaea,15 eucarya, 2 chloroplast, and 10 mitochondria. Readersare encouraged to contact the author with suggestions foradditional higherorder structure models not currentlyavailable.4. Illustrated in this article are three divergent 16S and 16S-like rRNAs structure models for: Escherichia coli, amember of the (eu)bacteria phylogenetic domain; nuclearencoded Saccharomyces cerevisiae, a member of theeucarya domain; and Caenorhabditis elegans mitochondria,one of the smallest known 16S-like rRNAs.This work is an adjunct to the monumental effort of the RDP(Ribosomal Database Project, see this issue); Their mandate beingto generate and make various tpes of ribosomal RNA data andinterpretation generally available. On-line access to these 16SrRNA secondary structure files is available from the RDPk.l 1993 Oxford University Press
  2. 2. 3052 Nucleic Acids Research, 1993, Vol. 21, No. 13aOU °AaU A0A 0 OAA A0cc Q.%AAUOC AUCUOOGAUOUC 0Aa II I. 11111-0 1l C II AUOC0A oUGOACACUUA0AU a COO0-oc--C0-co-CO-CO-C-C-O-0 a0U-A0-C-C--0U-UU-A0-C-isGA - UAAC %UA AkAACCUOOO UOCAUCUOA CUOOCAAOC-C to-IIl ..lI1IlIIt --IIl-1 /c0UCOOOCCC OUOUAOACU OA UUOUUUO /ICUCAC A I A I C .UAA GO IO0UUA CU-AA00U I I * I I1UUCC00 UAUCI AA0AA440AOaCCUOaA 0CAOV"l(0A%AII -1111 0cCOCGOU ACOUAU %A-SOA?0-cU-AO:CAco A-UA 0350 C-0UCd,,OAIOCAO-CACU UUO A, C-OeAa^ CA-a CA OUC ACSW A allII I -1 110~A0UCAA00UC coo UGoAoo GA% 0aA(A,AU C AAU lPUI U aCO AA*CcAUOACOCh^ au C COOAC05.U (1 A:C-aAO-C0-C-UC-0U-AAC-0- 11UA~~~~~~AG I A AUAALQ3A0aAAA-cGocucA a CAO --W c AAA-C0-C-A 0ACA5,AAOU CAOOAAGOII I lII - I I ICA OUCUUUCLa 0 I0oOOOAOUACOOCC 4--.11uAA-u uO-Ca - C 1100o-C, IU * OC CAAA 0 C u aAGuU ACOAOC CCUUA UCCUUUOU CC COOuCO I I I I I I I -I1 I I I I I I I 1011 1 1 1 CU . O UOCUCO AOOOU AOOAAAC A 00 aCCOOA-U I A U 0 0 I UC AIA-U C O% AC 1150-A 0 . . AU o-cAA UGU O-C .....OOUc-o 0 0-U U 0 CO-C AA C-U-AU C C-o0U 0 O - UC-1200 aAc-o A -A AC-0 0-CU A UO OA AU-AaAUOAOAAU OU A111.11 C 00C UU0A S ° G O-CIuU. OA.eC UAC-AU%CUU 1000 CUe0 AC 0 A UC-OCC A CeU/U-ZAw COU 95~A0X: XU^0 0-CCU.% ~ A0-CA~0eso A C-0A 0U ~~~~~0C 0oA U IACCU aA UU-A a 0aAA-~~~00~aU UOClla %O~~~~C UIAAU ~ 15 A~U-A CaAaA A10C- 5AA a0cu~ ~ ~ AU A CUC AAA -0A AGAC 0-C CAaA-Ua, OAACUCA UUO3AAAA I AAAAItI U UO ACOOOOCCCOCACAACOOUACU I I I I** III* * AC UOU UCCOGOCLOUUu aA C A CIA C10 C U1400-C---- I -UUo-C 0 C0C Aul I U A A CUAACCOUAGOOOU U * IlII I I*ICA-GA UUOOCOUCCAC oAA-A-U- UC-0 CC-0 AA O O CU*0 C0-U U0-C CO AA CA O o U-0-U U-U-A- AO-C IAAOC 0-U 3U ° - UUI U-Auuco u * a0-UC-oA-UA-U-A-U-A C0 AAA CO-CU-AA-U0-U0-CU* 0AO-C-C-0U-0AU -0A AC-0C -01450-U 0UCFigure 1. Higher-order structure diagram for Escherichia coil 16S rRNA [2-3]. For secondary structure basepairings, short lines connect canonical pairs (C:G,U:A), G:U pairs are denoted with dots, A:G pairings with larger open circles, and other non-canonical pairings with closed circles. Terdary interactions are connectedwith thicker and longer solid lines. Every 10th nucleotide position is marked with a tic mark, while every 50th posiion is numbered [Sequence Accession number is J01695]._u .- A 1
  3. 3. Nucleic Acids Research, 1993, Vol. 21, No. 13 3053U U0uuLAAACUU0UOAAUUAAAAAAOUUUCAU U U UOUo,ocucuuo0c 0 A A CCAOoAC 0u 1,111 I I 1111-1 AUCCU0A0UUCC A A u C OOUCUU Ac cuu0 A CUQO MCAAC0000OCC ty Uuuuco AGuoUc^coocuu II 1111 IIII 11111. UUUAGCc UoOCC ooUU0acccooo00AAAAUA c CA^ ac c ua u0 U o-U A 0AA AAGUCSoU C UAAUAICAAUOU! AOUi. Hg1 UCO UCA AA u0A 00UUUCCOUAOOU.11I I I I I I I (IOAAOOC0UCCAAUCAuU3.Figure 2. Higher-order structure diagram for Saccharomyces cerevisiae nucleocytoplasmic 16S-like rRNA. Higher-order structure interactions illustrated and notedas in Fig. 1. [Sequence is slighdy modified from acccession number J01353].A;U Aoao UAuuAAAAle uauAae AcAUUCC
  4. 4. 3054 Nucleic Acids Research, 1993, Vol. 21, No. 13AAUUU O OAUUUAUAUUAOU oa ...... ...I . I I .uoou U C UAOAUUUUCuuu AuAuuICAcuaAU UO-cu uu uAUA-4C -0AAuu-AAUUACCU AAAA c0oa. AAA *UoOU AA UU A^u0 Aa AOAC OLUAuuucuAU AA AUUUUuUAU UAAAA Au 11t1 1 uA- UUAUUUU uO-C ua .U A AA AuU AAU0*uUA^u-AO0* uAU - AAu UUO -cu cU-CUC-0AAc-AuUUuuuC_uC0UU - AUA-UCUU-AA AU..uAC-0uuUAQAUUUAO0G0,1111 1II AA UCUA A UC CAAu0Au u3.FIgr 3. Higher-order structure diagram for Caenorhabditis elegans mitochondrial 16S-like rRNA. Higher-order structre interactions illustrated and noted as inFig. 1. [Sequence Accession number is X54252].anonymous ftp site ( Currently, thesePostScript files are maintained in the/pub/RDP/SSU rRNA/sec_struct directory. Additionalinformation about this server and access to the RibosomalDatabase Project is described in their article in this issue. Readersunable to access this on-line information, can obtain a set of 16SrRNA hardcopy diagrams from the author.The interactive graphics program XRNA (developed by BrynWeiser, UC Santa Cruz) facilitated the generation ofthe higher-order structure models displayed here and the PostScript filesavailable at the RDP anonymous ftp site. Manual alignment ofthese 16S and 16S-like rRNA sequences was facilitated with theinteractive sequence alignment editor AE2 (developed by TomMacke, Scripps Clinic).ACKNOWLEDGMENTSRefining and interpreting these rRNA structure models is an on-going and long term collaboration with Drs Carl Woese andHarry Noller. Bryn Weiser and Tom Macke are greatfullyacknowleged for developing the wonderful programs that makemuch of this analysis and presentation possible. I also wish totank the W.M.Keck Foundation for their generous support ofRNA science on the Boulder campus, and SUN Microsystemsfor their timely donation of computer equipment. The author isan Associate in the Program in Evolutionary Biology of theCanadian Institute of Advanced Research. This work wassupported by the NIH (GM 48207).REFERENCES1. Gutell R.R. (1993a) Curr. Opin. Struct. Biol. 3, in press.2. Gutell R.R., Larsen N., and Woese C.R. (1993). In Zimmernmann R.A, andDahlberg A.E.(eds). Ribosomal RNA: Stucue, Evolution, Gene Expressionand Function in Protein Synthesis. CRC Press, Boca Raton, FL. in press.3. Gutell R.R. (1993b). In Nierhaus K.H., Subramanian A.R., Erdiann V.A.,Franceschi F., and Wittman-Liebold B. (eds). The Translational Apparatus.Plenum Publishing Corporation, NY, NY in press.4. Brimacombe R., Greuer B., Mitchell P., Osswald M., Rinke-Appel J.,Schuler D., and Stade K. (1990). In Hill W.E., Dahlberg A., Garrett R.A.,Moore P.B., Schlessinger D., and Warner J.R. (eds). The Ribosome:Structure, Function, and Evolution. American Society for Microbiology,Washington D.C. pp93-106.5. Ehresnann B., E C., Romby P., Mougel M., Baudin F., WesthofE., and Ebel J-P. (1990). In Hill W.E., Dahlberg A., Garrett R.A., MooreP.B., Schlessinger D., and Warner J.R. (eds). The Ribosome: Structure,Function, and Evolution. American Society for Microbiology, WashingtonD.C. ppl48-159.6. Noller H.F., Moazed D., Stern S., Powers T., Allen P.N., Robertson J.M.,Weiser B., and Triman K. (1990). In Hill W.E., Dahlberg A., Garrett R.A.,Moore P.B., Schlessinger D., and Warner J.R. (eds). The Ribosome:Structure, Function, and Evolution. American Society for Microbiology,Washington D.C. pp73-92.7. De Rijk P., Neefs J-M., Van de Peer Y., De Wachter R., (1992). NucleicAcids Res. 20,Supplement 2075 -2089.8. Gutell R.R., Power A., Hertz G.J., Putz E.J., and Stormo G.D. (1992).Nucleic Acids Res. 20, 5785-5795.