Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1997 May;179(10):3270–3276. doi: 10.1128/jb.179.10.3270-3276.1997

The actinomycete Thermobispora bispora contains two distinct types of transcriptionally active 16S rRNA genes.

Y Wang 1, Z Zhang 1, N Ramanan 1
PMCID: PMC179106  PMID: 9150223

Abstract

Here we present the first description of the presence of two distinct types of 16S rRNA genes in the genome of a (eu)bacterium, Thermobispora bispora. We cloned and determined the nucleotide sequences of all four rRNA operons of T. bispora. Sequence comparisons revealed that the genome of T. bispora contains two distinct types of 16S rRNA genes, each type consisting of two identical or nearly identical copies, and three identical copies of the 23S RNA gene. The nucleotide sequences of the two types of 16S rRNA genes differ at 98 nucleotide positions (6.4% of total nucleotides) together with six regions of deletion-insertions. None of the base substitutions or insertion-deletions corresponds to any of the approximately 600 evolutionarily invariable or rarely variable nucleotides, indicating that both genes are functional. Both types of 16S rRNA genes are transcribed and processed as determined by Northern (RNA) hybridization and reverse transcriptase-mediated PCR.

Full Text

The Full Text of this article is available as a PDF (628.5 KB).

Selected References

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

  1. Amann R. I., Ludwig W., Schleifer K. H. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev. 1995 Mar;59(1):143–169. doi: 10.1128/mr.59.1.143-169.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arnheim N., Krystal M., Schmickel R., Wilson G., Ryder O., Zimmer E. Molecular evidence for genetic exchanges among ribosomal genes on nonhomologous chromosomes in man and apes. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7323–7327. doi: 10.1073/pnas.77.12.7323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bourn W. R., Babb B. Computer assisted identification and classification of streptomycete promoters. Nucleic Acids Res. 1995 Sep 25;23(18):3696–3703. doi: 10.1093/nar/23.18.3696. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brosius J., Palmer M. L., Kennedy P. J., Noller H. F. Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sci U S A. 1978 Oct;75(10):4801–4805. doi: 10.1073/pnas.75.10.4801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Carranza S., Giribet G., Ribera C., Baguñ, Riutort M. Evidence that two types of 18S rDNA coexist in the genome of Dugesia (Schmidtea) mediterranea (Platyhelminthes, Turbellaria, Tricladida). Mol Biol Evol. 1996 Jul;13(6):824–832. doi: 10.1093/oxfordjournals.molbev.a025643. [DOI] [PubMed] [Google Scholar]
  6. Clayton R. A., Sutton G., Hinkle P. S., Jr, Bult C., Fields C. Intraspecific variation in small-subunit rRNA sequences in GenBank: why single sequences may not adequately represent prokaryotic taxa. Int J Syst Bacteriol. 1995 Jul;45(3):595–599. doi: 10.1099/00207713-45-3-595. [DOI] [PubMed] [Google Scholar]
  7. Condon C., Philips J., Fu Z. Y., Squires C., Squires C. L. Comparison of the expression of the seven ribosomal RNA operons in Escherichia coli. EMBO J. 1992 Nov;11(11):4175–4185. doi: 10.1002/j.1460-2075.1992.tb05511.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. East A. K., Thompson D. E., Collins M. D. Analysis of operons encoding 23S rRNA of Clostridium botulinum type A. J Bacteriol. 1992 Dec;174(24):8158–8162. doi: 10.1128/jb.174.24.8158-8162.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Groisman E. A., Saier M. H., Jr, Ochman H. Horizontal transfer of a phosphatase gene as evidence for mosaic structure of the Salmonella genome. EMBO J. 1992 Apr;11(4):1309–1316. doi: 10.1002/j.1460-2075.1992.tb05175.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Groisman E. A., Sturmoski M. A., Solomon F. R., Lin R., Ochman H. Molecular, functional, and evolutionary analysis of sequences specific to Salmonella. Proc Natl Acad Sci U S A. 1993 Feb 1;90(3):1033–1037. doi: 10.1073/pnas.90.3.1033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gunderson J. H., Sogin M. L., Wollett G., Hollingdale M., de la Cruz V. F., Waters A. P., McCutchan T. F. Structurally distinct, stage-specific ribosomes occur in Plasmodium. Science. 1987 Nov 13;238(4829):933–937. doi: 10.1126/science.3672135. [DOI] [PubMed] [Google Scholar]
  12. Heinonen T. Y., Schnare M. N., Gray M. W. Sequence heterogeneity in the duplicate large subunit ribosomal RNA genes of Tetrahymena pyriformis mitochondrial DNA. J Biol Chem. 1990 Dec 25;265(36):22336–22341. [PubMed] [Google Scholar]
  13. Hillis D. M., Moritz C., Porter C. A., Baker R. J. Evidence for biased gene conversion in concerted evolution of ribosomal DNA. Science. 1991 Jan 18;251(4991):308–310. doi: 10.1126/science.1987647. [DOI] [PubMed] [Google Scholar]
  14. Huang Z., Fasco M. J., Kaminsky L. S. Optimization of Dnase I removal of contaminating DNA from RNA for use in quantitative RNA-PCR. Biotechniques. 1996 Jun;20(6):1012-4, 1016, 1018-20. doi: 10.2144/96206st02. [DOI] [PubMed] [Google Scholar]
  15. King T. C., Sirdeskmukh R., Schlessinger D. Nucleolytic processing of ribonucleic acid transcripts in procaryotes. Microbiol Rev. 1986 Dec;50(4):428–451. doi: 10.1128/mr.50.4.428-451.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Long E. O., Dawid I. B. Repeated genes in eukaryotes. Annu Rev Biochem. 1980;49:727–764. doi: 10.1146/annurev.bi.49.070180.003455. [DOI] [PubMed] [Google Scholar]
  18. Maden B. E., Dent C. L., Farrell T. E., Garde J., McCallum F. S., Wakeman J. A. Clones of human ribosomal DNA containing the complete 18 S-rRNA and 28 S-rRNA genes. Characterization, a detailed map of the human ribosomal transcription unit and diversity among clones. Biochem J. 1987 Sep 1;246(2):519–527. doi: 10.1042/bj2460519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Mashkova T. D., Serenkova T. I., Mazo A. M., Avdonina T. A., Timofeyeva MYa, Kisselev L. L. The primary structure of oocyte and somatic 5S rRNAs from the loach Misgurnus fossilis. Nucleic Acids Res. 1981 May 11;9(9):2141–2151. doi: 10.1093/nar/9.9.2141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. McClure W. R. Mechanism and control of transcription initiation in prokaryotes. Annu Rev Biochem. 1985;54:171–204. doi: 10.1146/annurev.bi.54.070185.001131. [DOI] [PubMed] [Google Scholar]
  21. McCutchan T. F. The ribosomal genes of Plasmodium. Int Rev Cytol. 1986;99:295–309. doi: 10.1016/s0074-7696(08)61429-1. [DOI] [PubMed] [Google Scholar]
  22. Mevarech M., Hirsch-Twizer S., Goldman S., Yakobson E., Eisenberg H., Dennis P. P. Isolation and characterization of the rRNA gene clusters of Halobacterium marismortui. J Bacteriol. 1989 Jun;171(6):3479–3485. doi: 10.1128/jb.171.6.3479-3485.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mylvaganam S., Dennis P. P. Sequence heterogeneity between the two genes encoding 16S rRNA from the halophilic archaebacterium Haloarcula marismortui. Genetics. 1992 Mar;130(3):399–410. doi: 10.1093/genetics/130.3.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nübel U., Engelen B., Felske A., Snaidr J., Wieshuber A., Amann R. I., Ludwig W., Backhaus H. Sequence heterogeneities of genes encoding 16S rRNAs in Paenibacillus polymyxa detected by temperature gradient gel electrophoresis. J Bacteriol. 1996 Oct;178(19):5636–5643. doi: 10.1128/jb.178.19.5636-5643.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sollner-Webb B., Reeder R. H. The nucleotide sequence of the initiation and termination sites for ribosomal RNA transcription in X. laevis. Cell. 1979 Oct;18(2):485–499. doi: 10.1016/0092-8674(79)90066-7. [DOI] [PubMed] [Google Scholar]
  26. Stackebrandt E., Liesack W., Witt D. Ribosomal RNA and rDNA sequence analyses. Gene. 1992 Jun 15;115(1-2):255–260. doi: 10.1016/0378-1119(92)90567-9. [DOI] [PubMed] [Google Scholar]
  27. Syvanen M. Horizontal gene transfer: evidence and possible consequences. Annu Rev Genet. 1994;28:237–261. doi: 10.1146/annurev.ge.28.120194.001321. [DOI] [PubMed] [Google Scholar]
  28. Van de Peer Y., Chapelle S., De Wachter R. A quantitative map of nucleotide substitution rates in bacterial rRNA. Nucleic Acids Res. 1996 Sep 1;24(17):3381–3391. doi: 10.1093/nar/24.17.3381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Wang Y., Zhang Z., Ruan J. A proposal to transfer Microbispora bispora (Lechevalier 1965) to a new genus, Thermobispora gen. nov., as Thermobispora bispora comb. nov. Int J Syst Bacteriol. 1996 Oct;46(4):933–938. doi: 10.1099/00207713-46-4-933. [DOI] [PubMed] [Google Scholar]
  30. Waters A. P., Syin C., McCutchan T. F. Developmental regulation of stage-specific ribosome populations in Plasmodium. Nature. 1989 Nov 23;342(6248):438–440. doi: 10.1038/342438a0. [DOI] [PubMed] [Google Scholar]
  31. Wegnez M., Monier R., Denis H. Sequence heterogeneity of 5 S RNA in Xenopus laevis. FEBS Lett. 1972 Sep 1;25(1):13–20. doi: 10.1016/0014-5793(72)80443-5. [DOI] [PubMed] [Google Scholar]
  32. Wellauer P. K., Dawid I. B., Brown D. D., Reeder R. H. The molecular basis for length heterogeneity in ribosomal DNA from Xenopus laevis. J Mol Biol. 1976 Aug 25;105(4):461–486. doi: 10.1016/0022-2836(76)90229-1. [DOI] [PubMed] [Google Scholar]
  33. Wellauer P. K., Reeder R. H., Carroll D., Brown D. D., Deutch A., Higashinakagawa T., Dawid I. B. Amplified ribosomal DNA from Xenopus laevis has heterogeneous spacer lengths. Proc Natl Acad Sci U S A. 1974 Jul;71(7):2823–2827. doi: 10.1073/pnas.71.7.2823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. Woese C. R., Kandler O., Wheelis M. L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4576–4579. doi: 10.1073/pnas.87.12.4576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. van Wezel G. P., Vijgenboom E., Bosch L. A comparative study of the ribosomal RNA operons of Streptomyces coelicolor A3(2) and sequence analysis of rrnA. Nucleic Acids Res. 1991 Aug 25;19(16):4399–4403. doi: 10.1093/nar/19.16.4399. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES