or have become accessible in sequence libraries, since the last compilation (271), plus 8 ...... in both libraries but there can be a delay before a sequence submitted to one library arrives in the other one. ...... DmU*~A1P3O. CU. AA. GAC C.
.::j 1990 Oxford University Press
Nucleic Acids Research, Vol. 18, Supplement 2237
Compilation of small ribosomal subunit RNA
sequences
Jean-Marc Neefs, Yves Van de Peer, Lydia Hendriks and Rupert De Wachter* Departement Biochemie, Universiteit Antwerpen, UIA, Universiteitsplein 1, B-2610 Antwerp, Belgium
INTRODUCTION Table 1 lists 275 small ribosomal subunit RNA (further abbreviated as srRNA) sequences (references 1-270) that have been published, or submitted to the EMBL or GenBank nucleotide sequence libraries, to our knowledge. The previous compilation (271) listed 106 srRNA sequences. There is a tendency towards publication of partial, rather than complete sequences. This is a consequence of the availability of new techniques for sequencing or DNA amplification, that allow to collect results faster, but do not allow to determine the complete sequence up to the termini. One such method uses reverse transcription of the RNA with primers complementary to universally conserved sequence areas (272), in which case the sequence adjacent to the 3'-terminus cannot be determined. In another approach (27), the rDNA is amplified by the polymerase chain reaction (273) rather than by cloning. Since the primers for the PCR bind to conserved sequences close to the termini but within the boundaries of the srRNA gene, neither of the terminal sequences is comprised in the analysis. Both these methods, however, can yield a continuous sequence spanning more than 90% of the molecule, provided a sufficient number of primers is used. Some authors (e.g. reference 274) use a limited set of primers, in which case a discontinuous set of partial sequences is obtained, which can nevertheless be aligned with complete sequences from other species and used for phylogenetic studies. The set of 270 different srRNA sequences listed in Table 1 comprises complete sequences and continuous partial sequences, but no discontinuous partial sequences. In order to limit the space needed for the alignment, we have restricted it to 60 sequences. This comprises all the complete sequences that were published, or have become accessible in sequence libraries, since the last compilation (271), plus 8 previously listed sequences added as references in order to allow a comparison of the present alignment and secondary structure scheme with the previous one.
SEQUENCE ALIGNMENT The 60 sequences are listed in 5 groups, consisting of eukaryotic (cytoplasmic) -, archaebacterial -, eubacterial -, plastidial -and mitochondrial srRNAs. Each group comprises a sequence already aligned in the previous compilation, viz. Homo sapiens for the eukaryotic cytoplasmic srRNAs, Halobacterium cutirubrum for the archaebacterial srRNAs, Escherichia coli for the eubacterial srRNAs, Zea mays for the plastid srRNAs. Because of the extreme variability in length and secondary structure of mitochondrial srRNA sequences, an animal -, a plant -, a fungal -and a flagellate sequence were added as references in this group. The species chosen are H. sapiens, Glycine max, *
To whom
correspondence
should be addressed
Saccharomyces cerevisiae and Leishmania tarentolae. The sequences are identified on each alignment page by a number corresponding with that in Table 1 and with the literature reference, and by the initials of the species name. Alignment positions are numbered at the top and bottom of each page. In addition, E. coli srRNA nucleotide positions counting from its 5'-terminus are indicated above the eubacterial sequences. Regardless of the analytical method used, all sequences are listed using the ribonucleotide symbols U, C, A, and G. Posttranscriptional modifications are known for few sequences and not indicated in the alignment, but if data are available this is mentioned by a footnote in the last column of Table 1. The symbol X is used for unidentified and the symbols Y (pyrimidine nucleotide) and R (purine nucleotide) for incompletely identified nucleotides. These symbols point to uncertainty in the identification of a nucleotide in the case of analyses performed on cloned or amplified DNA, which examine the structure of a single gene. In the case of sequencing by reverse transcription of srRNA, however, they can point either to analytical uncertainty or to sequence heterogeneity, since the srRNA used as template may be a mixture of different sequences. Gaps introduced in order to optimize the alignment are filled with hyphens. On the contrary, dots are used for an interruption of the sequence due to partial sequencing. Hence, a sequence interrupted by 10 dots means that partial sequences are known to the left and to the right of the interruption, but that the length of the separating stretch is unknown. An interruption by 10 X's means that exactly 10 nucleotides are present, but their identity is unknown. A sequence starting or ending with dots means that sequencing has not reached the terminus. Lower case characters at termini are used to indicate length heterogeneity of the RNA molecules. It should be noted that the alignment of the sequences for optimal similarity is straightforward in areas of relatively conserved primary and secondary structure, but is much more arbitrary in the structurally more variable areas. Alignment rests mostly on the periodic occurrence of conserved sequence motifs and on the observation of compensating substitutions in complementary areas of the secondary structure (see below). In -,
the variable areas, conserved sequence motifs are rarer and at the same time the sequences differ in length. Whether compensating substitutions are seen or not then depends on how the gaps are placed, which makes their observation less
meaningful. Sequence segments presumedly involved in base pairing according to the secondary structure model described below are indicated by shading superimposed on the alignment. Shaded
2238 Nucleic Acids Research, Vol. 18, Supplement
V7 41
40
39 42
V6
P41-3
P35-1
V8
18 P17-1
V3
48
V9
17
vi 121
9
11
V2
10
Fig. 1. Secondary structure model for prokaryotic srRNAs. The 5'-terminus is symbolized by a filled circle and the 3'-terminus by an arrowhead. Helices are numbered in the order of occurrence from 5'- to 3'-terminus. Helices bearing a single number are common to the prokaryotic and eukaryotic (Fig. 2) models. A composite number preceded by P points to a prokaryote-specific helix. Relatively conserved areas are drawn in bold lines, areas of sequence-and length variability in thin lines. Eight variable areas, numbered VI to V9, are distinguished, V4 being absent in prokaryotic srRNAs. Helices drawn in broken lines are present in a small number of known structures only. Archaebacterial sequences follow the prokaryotic pattern except for helix 35, which is unbranched as in eukaryotes.
Nucleic Acids Research, Vol. 18, Supplement 2239 areas corresponding to complementary strands of helices 1 to 48 of the secondary structure model are numbered 1 and 1' to 48 and 48'. Helix numbers are listed twice, the uppermost row applying to the eukaryotic sequences, and the lowermost row to the bacterial -, plastidial -, and mitochondrial sequences. Internal loops and bulges in a helix are indicated by interruption of the shading. Bases suspected to belong to pairs other than the WatsonCrick pairs G * C, A * U, or the wobble pair G * U, because they are intercalated between Watson-Crick and/or wobble pairs, are put in parentheses.
SECONDARY STRUCTURE MODEL The secondary structure models adopted for indication of the double stranded areas in the alignment are shown in Fig. 1 and 2. The prokaryotic model of Fig. 1 applies to archaebacterial, eubacterial, plastidial, and mitochondrial srRNAs. The model of Fig. 2 applies to eukaryotic srRNAs. Helices common to both models, further called universal helices, are numbered 1 to 48, in the order of occurrence of the 5'-proximal strand when the sequence is scanned from 5' to 3'-end. Helix numbers change
V7 40
41
39
35 E21-9 II
E43-1
V5 27
44
E21-7
V8
V4
E21-1 48
V3
V9
E21-4 14
vi 121
11
9
V2 E10-2
E10-1
Fig. 2. Secondary structure model for eukaryotic srRNAs. Symbols are as in Fig. 1. Helices bearing a composite number preceded by E are eukaryote-specific. Variable area V6 is missing in eukaryotic srRNAs.
2240 Nucleic Acids Research, Vol. 18, Supplement at branching points and at pseudoknot loops, not at internal- and bulge loops. Helices specific to the prokaryotic model are numbered Pa-b, where a is the number of the preceding universal helix and b is a serial number. Helices specific to the eukaryotic model are similarly numbered Ea-b. Structurally conserved areas are drawn in bold lines, whereas structurally variable areas, labeled VI to V9, are drawn in thin lines. Helices that are present in a limited number of species are drawn in broken lines. Such is the case for e.g. helices P41-1 to P41-3, specific for plant mitochondrial srRNAs, or helix E10-3, hitherto found only in Euglena gracilis cytoplasmic srRNA. Conversely, helices can be absent in certain srRNAs. As an example, the diplomonad Giardia kamblia misses helices E21-1 to E21-4. Even the 'universal' helices do not occur in all srRNAs, the exceptions being found among the mitochondrial srRNAs. Those from animal mitochondria retain only 36 of the universal helices, with most of the missing ones belonging to variable areas. In flagellate mitochondrial srRNAs the structure retains only 25 universal helices, with the entire area consisting of helices 31 to 45 missing. The Fig. 1 model should therefore be regarded, not so much as a general prokaryotic model, but rather as a model for eubacterial and plastidial srRNA secondary structure, from which mitochondrial srRNA structures can be derived by addition (in the case of plant mitochondria) or subtraction of sets of helices. As for the archaebacterial srRNAs, these differ from the eubacterial ones only by lacking the branching point leading to helices P35-1 and P35-2. The models of Fig. 1 and 2 concur with those proposed by Gutell et al. (275) as far as the conserved areas are concerned, and for a fraction of the variable areas. However, we propose a structure for a long insertion in area V7 found in plant mitochondrial srRNAs, and for area V4 in eukaryotic srRNAs, both left undefined in (275). The latter structure is different from that adopted in the previous compilation (271) and comprises a pseudoknot. In addition, for areas V2 and V3 of the eukaryotic model, we propose a base pairing scheme slightly different from that of Gutell et al. (275). Although most of the structures that we propose in the variable areas are supported by observation of compensating substitutions, (unpublished) they should nevertheless be regarded as tentative in view of the difficulties connected with alignment in these areas explained above.
AVAILABILITY OF THE DATA Of the 270 different srRNA sequences listed in Table 1, 197 were in our computer file at the time of writing, in aligned form and with delimitation of secondary structure elements. The remaining ones, which are not listed in the papers reporting them but have been submitted to GenBank, have only recently become available in the file server of this library. They will be aligned as soon as possible. The sequences will be available on floppy disks, readable on microcomputers operating under MS-DOS, in the following three formats: 1) In the form of an alignment with indication of secondary structure elements. Aligned sequences will be listed on 42 pages each containing 100 alignment positions of all the sequences. This format is most useful for those wishing to produce a hardcopy of the complete alignment, rather than the sample of 60 sequences listed here. From this file, the complete alignment can be printed using a wide carriage printer, condensed print and reduced line spacing. Note, however, that this takes about 252 pages of 15 inch wide printer paper.
2) The sequences, listed one by one, without indication of secondary structure elements, but interspersed with the gaps required for alignment, i.e. with homologous nucleotides in the same position in each sequence. 3) The sequences, listed one by one, written continuously without gaps or secondary structure-describing symbols. The number of formatted floppy disks of different types that should be sent in order to obtain each of these files is listed in Table 2. In addition, all these files can be obtained on a TK50 tape, suitable for a MicroVax computer operating under VMS 5.0 or
higher. ACKNOWLEDGEMENTS Our work was supported in part by the Fund for Medical Scientific Research and in part by the Incentive Program for Fundamental Research in the Life Sciences of the Belgian Office for Science Policy Programming (grant BIO/03). J.N. and Y.V.d.P. are holders of a scholarship from the Institute for Scientific Research in Agriculture and Industry. We thank A. Wilmotte, A. Goris, and R. De Baere for their assistance in the correction of the computer files.
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Table 2. Number of formatted disks to be sent in order to obtain a copy of the database. Disk type Size
Capacity
Format 1
5.25" 5.25"
DSDD (360 Kbytes) DSHD (1.2 Mbytes) DSDD (720 Kbytes) DSHD (1.44 Mbytes)
15 5 8 4
3.5" 3.5"
Database format (see text) Format 3 Format 2 4 2 2 1
2 1 1 1
Footnotes to Table 1 The same number, and the a) This number corresponds with the literature reference and is preceded by an asterisk if the sequence is printed in the alignment. case character, are attributed lower a different followed numbers, Identical each by on the follow or page. alignment sequence initials of the species name, precede and Tetrahymena borealis). canadensis same the that have Tetrahymena same the sequence (e.g. species, to srRNAs from related species, or from different strains of In such cases only one sequence is listed in our computer file. b) This column contains the following data, if specified by the authors: - Strain name for laboratory animals, (cultivated) variety for plants, culture collection and strain number in the case of microorganisms. - Tissue from which the DNA used for cloning or amplification was extracted in the case of differentiated organisms. - Ribosomal RNA operon to which belongs the cloned srRNA gene in the case of bacteria. to 20), 279 c) The taxonomic position is described according to the following references: 277 for the metazoa (No. 1 to 14), 278 for the higher plants (No.to15Wetzel (281) is according described 34-62) of the (No. The taxonomic 28 to protista position 33). for the algae (No. 21 to 27), 280 for the fungi (No. for the species numbered 34-47 and 49-56, but according to Corliss (282) for Prorocentrum micans (No. 48) and for Euglenozoa, Microsporida and Polymastigotes to Stackebrandt et al. (284) for the Proteobacteria, (57-62). The archaebacteria are classified according to Woese (283). The classification of the eubacteria is according no information yet on the taxonomic position We have taxa. the for to Woese remaining and (283) the for al. Firmicuta, et according (285) according to Wayne of species 218-221. Taxon designations corresponding to an established taxonomic level are followed by the abbreviation Ph. (phylum), Sph. (subphylum), Cl. (class), 0. (order). by comparison with structures from d) The srRNA termini are located experimentally (e.g. by Si nuclease mapping) by some authors, but more often deduced denotes uncertainty on the location the length mark following A is listed. variant of the the question longest of related species. In case length heterogeneity length of the sequenced area. No length the length and gives has been determined partially the that means sequence of the termini. A number enclosed in brackets is mentioned for sequences not yet accessible in sequence libraries at the time of writing. The accession number for a sequence is the same in both libraries but there can e) Accession number in the EMBL and Genbank nucleotide sequence libraries.one. other in the arrives to one submitted a library be a delay before sequence f) PCR: the DNA was amplified by the polymerase chain reaction. RT: the srRNA was sequenced by the dideoxynucleotide method using reverse transcriptase. method. In the remaining cases DNA was amplified by cloning and sequencing was performed in most cases by the dideoxynucleotide sequence. this in the be found reporting can modification paper nucleoside on data g) Complete h) Partial data on modified nucleosides are mentioned in this paper or other papers cited therein. and has been corrected in (105). i) Complete data on nucleoside modification can be found in (276), but the sequence listed there misses I innucleotide are interspersed with genes coding for the rDNA j) Chlamydomonas reinhardtii mitochondrial srRNA consists of a set of 4 discontinuous fragments, which with alignment positions 239 to 312, 911 correspond the fragments between The and interruptions RNA subunit proteins. ribosomal fragments, tRNAs, large 2811. to 2643 to 930, and k) In the mature RNA, the nucleotides in alignment positions 431 to 618 are deleted by processing.
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Nucleic Acids Research, Vol. 18,
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2294 Nucleic Acids Research, Vol. 18, Supplement
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Nucleic Acids Research, Vol. 18, Supplement 2309 3680
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Nucleic Acids Research, Vol. 18, Supplement 2317 4160
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I 4150
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Lt 269 Ls 270
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I 4160
