Abstract
The sequences and structures of RNase P RNAs of some Gram-positive bacteria, e.g. Bacillus subtilis, are very different than those of other bacteria. In order to expand our understanding of the structure and evolution of RNase P RNA in Gram-positive bacteria, gene sequences encoding RNase P RNAs from 10 additional species from this evolutionary group have been determined, doubling the number of sequences available for comparative analysis. The enlarged data set allows refinement of the secondary structure model of these unusual RNase P RNAs and the identification of potential tertiary interactions between P10.1 and L12, and between L5.1 and L15.1. The newly-obtained sequences suggest that RNase P RNA underwent an abrupt, dramatic restructuring in the ancestry of the low-G+C Gram-positive bacteria after the divergence of the branches leading to the 'Clostridia and relatives' and the remaining low-G+C Gram-positive species. The unusual structures of the RNase P RNAs of Mycoplasma hyopneumoniae and M.floccularre are apparently derived from RNAs with Bacillus-like structure rather than from intermediate, partially restructured ancestral RNAs. The structure of the RNase P RNA from the photosynthetic Heliobacillus mobilis supports the relationship of this specie with Bacillus and Staphylococcus rather than the 'Clostridia and relatives' as suggested by the sequences of their small-subunit ribosomal RNAs.
Full Text
The Full Text of this article is available as a PDF (243.5 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Altman S., Kirsebom L., Talbot S. Recent studies of ribonuclease P. FASEB J. 1993 Jan;7(1):7–14. doi: 10.1096/fasebj.7.1.7916700. [DOI] [PubMed] [Google Scholar]
- Bothwell A. L., Garber R. L., Altman S. Nucleotide sequence and in vitro processing of a precursor molecule to Escherichia coli 4.5 S RNA. J Biol Chem. 1976 Dec 10;251(23):7709–7716. [PubMed] [Google Scholar]
- Brown J. W., Haas E. S., James B. D., Hunt D. A., Liu J. S., Pace N. R. Phylogenetic analysis and evolution of RNase P RNA in proteobacteria. J Bacteriol. 1991 Jun;173(12):3855–3863. doi: 10.1128/jb.173.12.3855-3863.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown J. W., Haas E. S., Pace N. R. Characterization of ribonuclease P RNAs from thermophilic bacteria. Nucleic Acids Res. 1993 Feb 11;21(3):671–679. doi: 10.1093/nar/21.3.671. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown J. W., Nolan J. M., Haas E. S., Rubio M. A., Major F., Pace N. R. Comparative analysis of ribonuclease P RNA using gene sequences from natural microbial populations reveals tertiary structural elements. Proc Natl Acad Sci U S A. 1996 Apr 2;93(7):3001–3006. doi: 10.1073/pnas.93.7.3001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown J. W. Phylogenetic comparative analysis of RNA structure on Macintosh computers. Comput Appl Biosci. 1991 Jul;7(3):391–393. doi: 10.1093/bioinformatics/7.3.391. [DOI] [PubMed] [Google Scholar]
- Brown J. W. The Ribonuclease P Database. Nucleic Acids Res. 1996 Jan 1;24(1):236–237. doi: 10.1093/nar/24.1.236. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Costa M., Michel F. Frequent use of the same tertiary motif by self-folding RNAs. EMBO J. 1995 Mar 15;14(6):1276–1285. doi: 10.1002/j.1460-2075.1995.tb07111.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Darr S. C., Zito K., Smith D., Pace N. R. Contributions of phylogenetically variable structural elements to the function of the ribozyme ribonuclease P. Biochemistry. 1992 Jan 21;31(2):328–333. doi: 10.1021/bi00117a003. [DOI] [PubMed] [Google Scholar]
- Fleischmann R. D., Adams M. D., White O., Clayton R. A., Kirkness E. F., Kerlavage A. R., Bult C. J., Tomb J. F., Dougherty B. A., Merrick J. M. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science. 1995 Jul 28;269(5223):496–512. doi: 10.1126/science.7542800. [DOI] [PubMed] [Google Scholar]
- Fraser C. M., Gocayne J. D., White O., Adams M. D., Clayton R. A., Fleischmann R. D., Bult C. J., Kerlavage A. R., Sutton G., Kelley J. M. The minimal gene complement of Mycoplasma genitalium. Science. 1995 Oct 20;270(5235):397–403. doi: 10.1126/science.270.5235.397. [DOI] [PubMed] [Google Scholar]
- Gutell R. R., Power A., Hertz G. Z., Putz E. J., Stormo G. D. Identifying constraints on the higher-order structure of RNA: continued development and application of comparative sequence analysis methods. Nucleic Acids Res. 1992 Nov 11;20(21):5785–5795. doi: 10.1093/nar/20.21.5785. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Haas E. S., Morse D. P., Brown J. W., Schmidt F. J., Pace N. R. Long-range structure in ribonuclease P RNA. Science. 1991 Nov 8;254(5033):853–856. doi: 10.1126/science.1719634. [DOI] [PubMed] [Google Scholar]
- Harris M. E., Nolan J. M., Malhotra A., Brown J. W., Harvey S. C., Pace N. R. Use of photoaffinity crosslinking and molecular modeling to analyze the global architecture of ribonuclease P RNA. EMBO J. 1994 Sep 1;13(17):3953–3963. doi: 10.1002/j.1460-2075.1994.tb06711.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- James B. D., Olsen G. J., Liu J. S., Pace N. R. The secondary structure of ribonuclease P RNA, the catalytic element of a ribonucleoprotein enzyme. Cell. 1988 Jan 15;52(1):19–26. doi: 10.1016/0092-8674(88)90527-2. [DOI] [PubMed] [Google Scholar]
- Kirsebom L. A., Svärd S. G. Base pairing between Escherichia coli RNase P RNA and its substrate. EMBO J. 1994 Oct 17;13(20):4870–4876. doi: 10.1002/j.1460-2075.1994.tb06814.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Larsen N., Zwieb C. The Signal Recognition Particle Database (SRPDB). Nucleic Acids Res. 1996 Jan 1;24(1):80–81. doi: 10.1093/nar/24.1.80. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maidak B. L., Larsen N., McCaughey M. J., Overbeek R., Olsen G. J., Fogel K., Blandy J., Woese C. R. The Ribosomal Database Project. Nucleic Acids Res. 1994 Sep;22(17):3485–3487. doi: 10.1093/nar/22.17.3485. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Murphy F. L., Cech T. R. GAAA tetraloop and conserved bulge stabilize tertiary structure of a group I intron domain. J Mol Biol. 1994 Feb 11;236(1):49–63. doi: 10.1006/jmbi.1994.1117. [DOI] [PubMed] [Google Scholar]
- Nakamura K., Minemura M., Nishiguchi M., Honda K., Nakamura A., Yamane K. Conserved residues and secondary structure found in small cytoplasmic RNAs from thirteen Bacillus species. Nucleic Acids Res. 1992 Oct 11;20(19):5227–5228. doi: 10.1093/nar/20.19.5227. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Oh B. K., Pace N. R. Interaction of the 3'-end of tRNA with ribonuclease P RNA. Nucleic Acids Res. 1994 Oct 11;22(20):4087–4094. doi: 10.1093/nar/22.20.4087. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pace N. R., Brown J. W. Evolutionary perspective on the structure and function of ribonuclease P, a ribozyme. J Bacteriol. 1995 Apr;177(8):1919–1928. doi: 10.1128/jb.177.8.1919-1928.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pace N. R., Smith D. K., Olsen G. J., James B. D. Phylogenetic comparative analysis and the secondary structure of ribonuclease P RNA--a review. Gene. 1989 Oct 15;82(1):65–75. doi: 10.1016/0378-1119(89)90031-0. [DOI] [PubMed] [Google Scholar]
- Poritz M. A., Strub K., Walter P. Human SRP RNA and E. coli 4.5S RNA contain a highly homologous structural domain. Cell. 1988 Oct 7;55(1):4–6. doi: 10.1016/0092-8674(88)90003-7. [DOI] [PubMed] [Google Scholar]
- Reed R. E., Baer M. F., Guerrier-Takada C., Donis-Keller H., Altman S. Nucleotide sequence of the gene encoding the RNA subunit (M1 RNA) of ribonuclease P from Escherichia coli. Cell. 1982 Sep;30(2):627–636. doi: 10.1016/0092-8674(82)90259-8. [DOI] [PubMed] [Google Scholar]
- Reich C., Gardiner K. J., Olsen G. J., Pace B., Marsh T. L., Pace N. R. The RNA component of the Bacillus subtilis RNase P. Sequence, activity, and partial secondary structure. J Biol Chem. 1986 Jun 15;261(17):7888–7893. [PubMed] [Google Scholar]
- Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
- Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Seidman J. G., McClain W. H. Three steps in conversion of large precursor RNA into serine and proline transfer RNAs. Proc Natl Acad Sci U S A. 1975 Apr;72(4):1491–1495. doi: 10.1073/pnas.72.4.1491. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Siegel R. W., Banta A. B., Haas E. S., Brown J. W., Pace N. R. Mycoplasma fermentans simplifies our view of the catalytic core of ribonuclease P RNA. RNA. 1996 May;2(5):452–462. [PMC free article] [PubMed] [Google Scholar]
- Struck J. C., Hartmann R. K., Toschka H. Y., Erdmann V. A. Transcription and processing of Bacillus subtilis small cytoplasmic RNA. Mol Gen Genet. 1989 Feb;215(3):478–482. doi: 10.1007/BF00427046. [DOI] [PubMed] [Google Scholar]
- Svärd S. G., Mattsson J. G., Johansson K. E., Kirsebom L. A. Cloning and characterization of the RNase P RNA genes from two porcine mycoplasmas. Mol Microbiol. 1994 Mar;11(5):849–859. doi: 10.1111/j.1365-2958.1994.tb00363.x. [DOI] [PubMed] [Google Scholar]
- Tanner M. A., Cech T. R. An important RNA tertiary interaction of group I and group II introns is implicated in gram-positive RNase P RNAs. RNA. 1995 Jun;1(4):349–350. [PMC free article] [PubMed] [Google Scholar]
- Wang M. J., Davis N. W., Gegenheimer P. Novel mechanisms for maturation of chloroplast transfer RNA precursors. EMBO J. 1988 Jun;7(6):1567–1574. doi: 10.1002/j.1460-2075.1988.tb02981.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Westhof E., Altman S. Three-dimensional working model of M1 RNA, the catalytic RNA subunit of ribonuclease P from Escherichia coli. Proc Natl Acad Sci U S A. 1994 May 24;91(11):5133–5137. doi: 10.1073/pnas.91.11.5133. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Woese C. R. Bacterial evolution. Microbiol Rev. 1987 Jun;51(2):221–271. doi: 10.1128/mr.51.2.221-271.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]