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. 1982 Mar 11;10(5):1607–1624. doi: 10.1093/nar/10.5.1607

tRNA genes are found between 16S and 23S rRNA genes in Bacillus subtilis.

K Loughney, E Lund, J E Dahlberg
PMCID: PMC320553  PMID: 6280153

Abstract

There are at least nine, and probably ten, ribosomal RNA gene sets in the genome of Bacillus subtilis. Each gene set contains sequences complementary to 16S, 23S and 5S rRNAs. We have determined the nucleotide sequences of two DNA fragments which each contain 165 base pairs of the 16S rRNA gene, 191 base pairs of the 23S rRNA gene, and the spacer region between them. The smaller space region is 164 base pairs in length and the larger one includes an additional 180 base pairs. The extra nucleotides could be transcribed in tRNAIIe and tRNA Ala sequences. Evidence is also presented for the existence of a second spacer region which also contains tRNAIIe and tRNA Ala sequences. No other tRNAs appear to be encoded in the spacer regions between the 16S and 23S rRNA genes. Whereas the nucleotide sequences corresponding to the 16S rRNA, 23S rRNA and the spacer tRNAs are very similar to those of E. coli, the sequences between these structural genes are very different.

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Selected References

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  1. Benton W. D., Davis R. W. Screening lambdagt recombinant clones by hybridization to single plaques in situ. Science. 1977 Apr 8;196(4286):180–182. doi: 10.1126/science.322279. [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. Bolivar F., Rodriguez R. L., Greene P. J., Betlach M. C., Heyneker H. L., Boyer H. W., Crosa J. H., Falkow S. Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene. 1977;2(2):95–113. [PubMed] [Google Scholar]
  4. Bram R. J., Young R. A., Steitz J. A. The ribonuclease III site flanking 23S sequences in the 30S ribosomal precursor RNA of E. coli. Cell. 1980 Feb;19(2):393–401. doi: 10.1016/0092-8674(80)90513-9. [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. Brownlee G. G., Sanger F. Nucleotide sequences from the low molecular weight ribosomal RNA of Escherichia coli. J Mol Biol. 1967 Feb 14;23(3):337–353. doi: 10.1016/s0022-2836(67)80109-8. [DOI] [PubMed] [Google Scholar]
  7. Chow L. T., Davidson N. Electron microscope mapping of the distribution of ribosomal genes of the Bacillus subtilis chromosome. J Mol Biol. 1973 Apr 5;75(2):265–279. doi: 10.1016/0022-2836(73)90020-x. [DOI] [PubMed] [Google Scholar]
  8. Clewell D. B., Helinski D. R. Supercoiled circular DNA-protein complex in Escherichia coli: purification and induced conversion to an opern circular DNA form. Proc Natl Acad Sci U S A. 1969 Apr;62(4):1159–1166. doi: 10.1073/pnas.62.4.1159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Colli W., Smith I., Oishi M. Physical linkage between 5 s, 16 s and 23 s ribosomal RNA genes in Bacillus subtilis. J Mol Biol. 1971 Feb 28;56(1):117–127. doi: 10.1016/0022-2836(71)90088-x. [DOI] [PubMed] [Google Scholar]
  10. Delius H., Koller B. Sequence homologies between Escherichia coli and chloroplast ribosomal DNA as seen by heteroduplex analysis. J Mol Biol. 1980 Sep 15;142(2):247–261. doi: 10.1016/0022-2836(80)90048-0. [DOI] [PubMed] [Google Scholar]
  11. Denhardt D. T. A membrane-filter technique for the detection of complementary DNA. Biochem Biophys Res Commun. 1966 Jun 13;23(5):641–646. doi: 10.1016/0006-291x(66)90447-5. [DOI] [PubMed] [Google Scholar]
  12. Fitch W. M. An improved method of testing for evolutionary homology. J Mol Biol. 1966 Mar;16(1):9–16. doi: 10.1016/s0022-2836(66)80258-9. [DOI] [PubMed] [Google Scholar]
  13. Fitch W. M. Further improvements in the method of testing for evolutionary homology among proteins. J Mol Biol. 1970 Apr 14;49(1):1–14. doi: 10.1016/0022-2836(70)90372-4. [DOI] [PubMed] [Google Scholar]
  14. Graf L., Kössel H., Stutz E. Sequencing of 16S--23S spacer in a ribosomal RNA operon of Euglena gracilis chloroplast DNA reveals two tRNA genes. Nature. 1980 Aug 28;286(5776):908–910. doi: 10.1038/286908a0. [DOI] [PubMed] [Google Scholar]
  15. Grunstein M., Hogness D. S. Colony hybridization: a method for the isolation of cloned DNAs that contain a specific gene. Proc Natl Acad Sci U S A. 1975 Oct;72(10):3961–3965. doi: 10.1073/pnas.72.10.3961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Herr W., Noller H. F. A fragment of 23S RNA containing a nucleotide sequence complementary to a region of 5S RNA. FEBS Lett. 1975 May 1;53(2):248–252. doi: 10.1016/0014-5793(75)80030-5. [DOI] [PubMed] [Google Scholar]
  17. Ikemura T., Dahlberg J. E. Small ribonucleic acids of Escherichia coli. I. Characterization by polyacrylamide gel electrophoresis and fingerprint analysis. J Biol Chem. 1973 Jul 25;248(14):5024–5032. [PubMed] [Google Scholar]
  18. Ikemura T., Nomura M. Expression of spacer tRNA genes in ribosomal RNA transcription units carried by hybrid Col E1 plasmids in E. coli. Cell. 1977 Aug;11(4):779–793. doi: 10.1016/0092-8674(77)90291-4. [DOI] [PubMed] [Google Scholar]
  19. Koch W., Edwards K., Kössel H. Sequencing of the 16S-23S spacer in a ribosomal RNA operon of Zea mays chloroplast DNA reveals two split tRNA genes. Cell. 1981 Jul;25(1):203–213. doi: 10.1016/0092-8674(81)90245-2. [DOI] [PubMed] [Google Scholar]
  20. Lund E., Dahlberg J. E., Lindahl L., Jaskunas S. R., Dennis P. P., Nomura M. Transfer RNA genes between 16S and 23S rRNA genes in rRNA transcription units of E. coli. Cell. 1976 Feb;7(2):165–177. doi: 10.1016/0092-8674(76)90016-7. [DOI] [PubMed] [Google Scholar]
  21. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  22. Moran C. P., Jr, Bott K. F. Restriction enzyme analysis of Bacillus subtilis ribosomal ribonucleic acid genes. J Bacteriol. 1979 Oct;140(1):99–105. doi: 10.1128/jb.140.1.99-105.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Morgan E. A., Ikemura T., Nomura M. Identification of spacer tRNA genes in individual ribosomal RNA transcription units of Escherichia coli. Proc Natl Acad Sci U S A. 1977 Jul;74(7):2710–2714. doi: 10.1073/pnas.74.7.2710. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Neidhardt F. C., Bloch P. L., Smith D. F. Culture medium for enterobacteria. J Bacteriol. 1974 Sep;119(3):736–747. doi: 10.1128/jb.119.3.736-747.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nishimura S. Minor components in transfer RNA: their characterization, location, and function. Prog Nucleic Acid Res Mol Biol. 1972;12:49–85. [PubMed] [Google Scholar]
  26. Potter S. S., Bott K. F., Newbold J. E. Two-dimensional restriction analysis of the Bacillus subtilis genome: gene purification and ribosomal ribonucleic acid gene organization. J Bacteriol. 1977 Jan;129(1):492–500. doi: 10.1128/jb.129.1.492-500.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sanger F., Brownlee G. G., Barrell B. G. A two-dimensional fractionation procedure for radioactive nucleotides. J Mol Biol. 1965 Sep;13(2):373–398. doi: 10.1016/s0022-2836(65)80104-8. [DOI] [PubMed] [Google Scholar]
  28. Sharp P. A., Sugden B., Sambrook J. Detection of two restriction endonuclease activities in Haemophilus parainfluenzae using analytical agarose--ethidium bromide electrophoresis. Biochemistry. 1973 Jul 31;12(16):3055–3063. doi: 10.1021/bi00740a018. [DOI] [PubMed] [Google Scholar]
  29. Sogin M. L., Pace N. R. Nucleotide sequence of 5 S ribosomal RNA precursor from Bacillus subtilis. J Biol Chem. 1976 Jun 10;251(11):3480–3488. [PubMed] [Google Scholar]
  30. 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]
  31. Sprague K. U., Steitz J. A., Grenley R. M., Stocking C. E. 3' terminal sequences of 16S rRNA do not explain translational specificity differences between E. coli and B. stearothermophilus ribosomes. Nature. 1977 Jun 2;267(5610):462–465. doi: 10.1038/267462a0. [DOI] [PubMed] [Google Scholar]
  32. Sugiura M., Takanami M. Analysis of the 5'-terminal nucleotide sequences of ribonucleic acids. II. Comparison of the 5'-terminal nucleotide sequences of ribosomal RNA's from different organisms. Proc Natl Acad Sci U S A. 1967 Oct;58(4):1595–1602. doi: 10.1073/pnas.58.4.1595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Taylor W. E., Burgess R. R. Escherichia coli RNA polymerase binding and initiation of transcription on fragments of lambda rifd 18 DNA containing promoters for lambda genes and for rrnB, tufB, rplC,A, rplJ,L, and rpoB,C genes. Gene. 1979 Aug;6(4):331–365. doi: 10.1016/0378-1119(79)90073-8. [DOI] [PubMed] [Google Scholar]
  34. Van Charldorp R., Van Kimmenade A. M., Van Knippenberg P. H. Sequence and secondary structure of the colicin fragment of Bacillus stearothermophilus 16S ribosomal RNA. Nucleic Acids Res. 1981 Oct 10;9(19):4909–4917. doi: 10.1093/nar/9.19.4909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Weiner A. M. An abundant cytoplasmic 7S RNA is complementary to the dominant interspersed middle repetitive DNA sequence family in the human genome. Cell. 1980 Nov;22(1 Pt 1):209–218. doi: 10.1016/0092-8674(80)90169-5. [DOI] [PubMed] [Google Scholar]
  36. Woese C. R., Magrum L. J., Gupta R., Siegel R. B., Stahl D. A., Kop J., Crawford N., Brosius J., Gutell R., Hogan J. J. Secondary structure model for bacterial 16S ribosomal RNA: phylogenetic, enzymatic and chemical evidence. Nucleic Acids Res. 1980 May 24;8(10):2275–2293. doi: 10.1093/nar/8.10.2275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Young R. A., Macklis R., Steitz J. A. Sequence of the 16 S-23 s spacer region in two ribosomal RNA operons of Escherichia coli. J Biol Chem. 1979 May 10;254(9):3264–3271. [PubMed] [Google Scholar]
  38. Young R. A., Steitz J. A. Complementary sequences 1700 nucleotides apart form a ribonuclease III cleavage site in Escherichia coli ribosomal precursor RNA. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3593–3597. doi: 10.1073/pnas.75.8.3593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Zingales B., Colli W. Ribosomal RNA genes in Bacillus subtilis. Evidence for a cotranscription mechanism. Biochim Biophys Acta. 1977 Feb 16;474(4):562–577. doi: 10.1016/0005-2787(77)90076-4. [DOI] [PubMed] [Google Scholar]

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