Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1989 Sep;171(9):5025–5030. doi: 10.1128/jb.171.9.5025-5030.1989

Evidence for unlinked rrn operons in the Planctomycete Pirellula marina.

W Liesack 1, E Stackebrandt 1
PMCID: PMC210313  PMID: 2768196

Abstract

Southern hybridization of rRNAs to chromosomal BamHI-digested DNA of the eubacterium Pirellula marina revealed the presence of two sets of 16S and 23S rRNA genes. The two copies of the 23S rRNA genes, located on 11- and about 13-kilobase (kb) inserts, were isolated from a lambda bacteriophage Charon 35 library. The 11-kb fragment was cloned directly into pBR322, while a 5.4-kb BamHI-PstI rDNA subfragment of the approximately 13-kb insert was cloned into pUC18. Both recombinant plasmids, pPI1100 and pPI540, were characterized by restriction enzyme mapping and Southern hybridization with the large rRNA species. Restriction fragments from both inserts were subcloned into phage M13 mp18 and mp19. Correlation of genomic hybridization data with physical characterization of recombinant plasmids showed that, in contrast to the general organization of rrn operons in eubacteria, the 16S rRNA genes of P. marina are separated by at least 8.5 (pPI540) and 4.4 (pPI1100) kb, respectively, from the closely linked 23S-5S rRNA genes. Comparison of the flanking regions from both 23S-5S rRNA genes with published consensus sequences of structural elements indicates the presence of putative transcription signals, i.e., a single Pribnow box, discriminator, antitermination boxes A, B, and C, and a Rho-independent terminator.

Full text

PDF
5025

Images in this article

5026Image
on p.5026
5027Image
on p.5027
5027Image
on p.5027

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baylis H. A., Bibb M. J. Organisation of the ribosomal RNA genes in Streptomyces coelicolor A3(2). Mol Gen Genet. 1988 Feb;211(2):191–196. doi: 10.1007/BF00330593. [DOI] [PubMed] [Google Scholar]
  2. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bomar D., Giovannoni S., Stackebrandt E. A unique type of eubacterial 5S rRNA in members of the order Planctomycetales. J Mol Evol. 1988;27(2):121–125. doi: 10.1007/BF02138371. [DOI] [PubMed] [Google Scholar]
  4. Boyer H. W., Roulland-Dussoix D. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J Mol Biol. 1969 May 14;41(3):459–472. doi: 10.1016/0022-2836(69)90288-5. [DOI] [PubMed] [Google Scholar]
  5. Brosius J., Dull T. J., Sleeter D. D., Noller H. F. Gene organization and primary structure of a ribosomal RNA operon from Escherichia coli. J Mol Biol. 1981 May 15;148(2):107–127. doi: 10.1016/0022-2836(81)90508-8. [DOI] [PubMed] [Google Scholar]
  6. Harley C. B., Reynolds R. P. Analysis of E. coli promoter sequences. Nucleic Acids Res. 1987 Mar 11;15(5):2343–2361. doi: 10.1093/nar/15.5.2343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hartmann R. K., Toschka H. Y., Ulbrich N., Erdmann V. A. Genomic organization of rDNA in Pseudomonas aeruginosa. FEBS Lett. 1986 Jan 20;195(1-2):187–193. doi: 10.1016/0014-5793(86)80158-2. [DOI] [PubMed] [Google Scholar]
  8. Hartmann R. K., Ulbrich N., Erdmann V. A. An unusual rRNA operon constellation: in Thermus thermophilus HB8 the 23S/5S rRNA operon is a separate entity from the 16S rRNA operon. Biochimie. 1987 Oct;69(10):1097–1104. doi: 10.1016/0300-9084(87)90009-5. [DOI] [PubMed] [Google Scholar]
  9. Lamfrom H., Sarabhai A., Abelson J. Cloning of Beneckea genes in Escherichia coli. J Bacteriol. 1978 Jan;133(1):354–363. doi: 10.1128/jb.133.1.354-363.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Lamond A. I., Travers A. A. Requirement for an upstream element for optimal transcription of a bacterial tRNA gene. Nature. 1983 Sep 15;305(5931):248–250. doi: 10.1038/305248a0. [DOI] [PubMed] [Google Scholar]
  11. Lane D. J., Pace B., Olsen G. J., Stahl D. A., Sogin M. L., Pace N. R. Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc Natl Acad Sci U S A. 1985 Oct;82(20):6955–6959. doi: 10.1073/pnas.82.20.6955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Li S. C., Squires C. L., Squires C. Antitermination of E. coli rRNA transcription is caused by a control region segment containing lambda nut-like sequences. Cell. 1984 Oct;38(3):851–860. doi: 10.1016/0092-8674(84)90280-0. [DOI] [PubMed] [Google Scholar]
  13. Liesack W., Höpfl P., Stackebrandt E. Complete nucleotide sequence of a 23S ribosomal RNA gene from Pirellula marina. Nucleic Acids Res. 1988 Jun 10;16(11):5194–5194. doi: 10.1093/nar/16.11.5194. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Loenen W. A., Blattner F. R. Lambda Charon vectors (Ch32, 33, 34 and 35) adapted for DNA cloning in recombination-deficient hosts. Gene. 1983 Dec;26(2-3):171–179. doi: 10.1016/0378-1119(83)90187-7. [DOI] [PubMed] [Google Scholar]
  15. Messing J., Crea R., Seeburg P. H. A system for shotgun DNA sequencing. Nucleic Acids Res. 1981 Jan 24;9(2):309–321. doi: 10.1093/nar/9.2.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Morgan E. A. Antitermination mechanisms in rRNA operons of Escherichia coli. J Bacteriol. 1986 Oct;168(1):1–5. doi: 10.1128/jb.168.1.1-5.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Nomura M., Gourse R., Baughman G. Regulation of the synthesis of ribosomes and ribosomal components. Annu Rev Biochem. 1984;53:75–117. doi: 10.1146/annurev.bi.53.070184.000451. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Schleifer K. H., Kandler O. Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev. 1972 Dec;36(4):407–477. doi: 10.1128/br.36.4.407-477.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  21. Stackebrandt E., Ludwig W., Schleifer K. H., Gross H. J. Rapid cataloging of ribonuclease T1 resistant oligonucleotides from ribosomal RNAs for phylogenetic studies. J Mol Evol. 1981;17(4):227–236. doi: 10.1007/BF01732760. [DOI] [PubMed] [Google Scholar]
  22. Stackebrandt E., Ludwig W., Schubert W., Klink F., Schlesner H., Roggentin T., Hirsch P. Molecular genetic evidence for early evolutionary origin of budding peptidoglycan-less eubacteria. Nature. 1984 Feb 23;307(5953):735–737. doi: 10.1038/307735a0. [DOI] [PubMed] [Google Scholar]
  23. Tabor S., Richardson C. C. DNA sequence analysis with a modified bacteriophage T7 DNA polymerase. Proc Natl Acad Sci U S A. 1987 Jul;84(14):4767–4771. doi: 10.1073/pnas.84.14.4767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Taschke C., Klinkert M. Q., Wolters J., Herrmann R. Organization of the ribosomal RNA genes in Mycoplasma hyopneumoniae: the 5S rRNA gene is separated from the 16S and 23S rRNA genes. Mol Gen Genet. 1986 Dec;205(3):428–433. doi: 10.1007/BF00338078. [DOI] [PubMed] [Google Scholar]
  25. Travers A. A. Conserved features of coordinately regulated E. coli promoters. Nucleic Acids Res. 1984 Mar 26;12(6):2605–2618. doi: 10.1093/nar/12.6.2605. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Travers A. A. Promoter sequence for stringent control of bacterial ribonucleic acid synthesis. J Bacteriol. 1980 Feb;141(2):973–976. doi: 10.1128/jb.141.2.973-976.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Tu J., Zillig W. Organization of rRNA structural genes in the archaebacterium Thermoplasma acidophilum. Nucleic Acids Res. 1982 Nov 25;10(22):7231–7245. doi: 10.1093/nar/10.22.7231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ulbrich N., Kumagai I., Erdmann V. A. The number of ribosomal RNA genes in Thermus thermophilus HB8. Nucleic Acids Res. 1984 Feb 24;12(4):2055–2060. doi: 10.1093/nar/12.4.2055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Weisburg W. G., Oyaizu Y., Oyaizu H., Woese C. R. Natural relationship between bacteroides and flavobacteria. J Bacteriol. 1985 Oct;164(1):230–236. doi: 10.1128/jb.164.1.230-236.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Woese C. R., Stackebrandt E., Macke T. J., Fox G. E. A phylogenetic definition of the major eubacterial taxa. Syst Appl Microbiol. 1985;6:143–151. doi: 10.1016/s0723-2020(85)80047-3. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES