Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1985 Jul;163(1):155–166. doi: 10.1128/jb.163.1.155-166.1985

Organization and nucleotide sequence analysis of an rRNA and tRNA gene cluster from Caulobacter crescentus.

J Feingold, V Bellofatto, L Shapiro, K Amemiya
PMCID: PMC219093  PMID: 4008439

Abstract

rRNA genes of Caulobacter crescentus CB13 were isolated and shown to be present in two gene clusters in the genome. The organization of each rRNA gene cluster was found to be 5'-16S-tRNA spacer-23S-5S-3'. The DNA sequence of 40% of the 16S rRNA gene, the entire 16S/23S intergenic spacer region, and portions of the 23S rRNA gene were determined. Analysis of the nucleotide sequence in the 16S-23S intergenic spacer region revealed the presence of tRNAIle and tRNAAla genes. Large invert repeat sequences were found surrounding the 16S rRNA gene. These inverted repeat sequences are analogous to the RNase III-processing sites in the E. coli rRNA precursor. Small invert repeat sequences were also found flanking the individual tRNA genes. RNA polymerase-binding studies with restriction fragments of the rRNA gene cluster revealed three regions which bound enzyme, and these regions were shown to contain transcription initiation sites. One of these sites was located within the 16S gene near its 3' end, and the other two were found at the 5' end of the 23S gene.

Full text

PDF
155

Images in this article

156Image
on p.156
158Image
on p.158
159Image
on p.159
161Image
on p.161
161Image
on p.161
162Image
on p.162

Selected References

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

  1. Amemiya K., Shapiro L. Differential template recognition by the Caulobacter crescentus and the escherichia coli RNA polymerases. J Biol Chem. 1983 Jul 25;258(14):8984–8992. [PubMed] [Google Scholar]
  2. Apirion D. Isolation, genetic mapping and some characterization of a mutation in Escherichia coli that affects the processing of ribonuleic acid. Genetics. 1978 Dec;90(4):659–671. doi: 10.1093/genetics/90.4.659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bellofatto V., Amemiya K., Shapiro L. Purification and characterization of an RNA processing enzyme from Caulobacter crescentus. J Biol Chem. 1983 May 10;258(9):5467–5476. [PubMed] [Google Scholar]
  4. 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]
  5. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  6. Blattner F. R., Blechl A. E., Denniston-Thompson K., Faber H. E., Richards J. E., Slightom J. L., Tucker P. W., Smithies O. Cloning human fetal gamma globin and mouse alpha-type globin DNA: preparation and screening of shotgun collections. Science. 1978 Dec 22;202(4374):1279–1284. doi: 10.1126/science.725603. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Clewell D. B., Helinski D. R. Properties of a supercoiled deoxyribonucleic acid-protein relaxation complex and strand specificity of the relaxation event. Biochemistry. 1970 Oct 27;9(22):4428–4440. doi: 10.1021/bi00824a026. [DOI] [PubMed] [Google Scholar]
  9. Contreras I., Shapiro L., Henry S. Membrane phospholipid composition of Caulobacter crescentus. J Bacteriol. 1978 Sep;135(3):1130–1136. doi: 10.1128/jb.135.3.1130-1136.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fox G. E., Stackebrandt E., Hespell R. B., Gibson J., Maniloff J., Dyer T. A., Wolfe R. S., Balch W. E., Tanner R. S., Magrum L. J. The phylogeny of prokaryotes. Science. 1980 Jul 25;209(4455):457–463. doi: 10.1126/science.6771870. [DOI] [PubMed] [Google Scholar]
  11. Gegenheimer P., Apirion D. Processing of procaryotic ribonucleic acid. Microbiol Rev. 1981 Dec;45(4):502–541. doi: 10.1128/mr.45.4.502-541.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Glaser G., Amikam D., Razin S. Physical mapping of the ribosomal RNA genes of Mycoplasma capricolum. Nucleic Acids Res. 1984 Mar 12;12(5):2421–2426. doi: 10.1093/nar/12.5.2421. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hawley D. K., McClure W. R. Compilation and analysis of Escherichia coli promoter DNA sequences. Nucleic Acids Res. 1983 Apr 25;11(8):2237–2255. doi: 10.1093/nar/11.8.2237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hofman J. D., Lau R. H., Doolittle W. F. The number, physical organization and transcription of ribosomal RNA cistrons in an archaebacterium: Halobacterium halobium. Nucleic Acids Res. 1979 Nov 10;7(5):1321–1333. doi: 10.1093/nar/7.5.1321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jinks-Robertson S., Gourse R. L., Nomura M. Expression of rRNA and tRNA genes in Escherichia coli: evidence for feedback regulation by products of rRNA operons. Cell. 1983 Jul;33(3):865–876. doi: 10.1016/0092-8674(83)90029-6. [DOI] [PubMed] [Google Scholar]
  16. Keller M., Burkard G., Bohnert H. J., Mubumbila M., Gordon K., Steinmetz A., Heiser D., Crouse E. J., Weil J. H. Transfer RNA genes associated with the 16S and 23S rRNA genes of Euglena chloroplast DNA. Biochem Biophys Res Commun. 1980 Jul 16;95(1):47–54. doi: 10.1016/0006-291x(80)90702-0. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Loughney K., Lund E., Dahlberg J. E. Ribosomal RNA precursors of Bacillus subtilis. Nucleic Acids Res. 1983 Oct 11;11(19):6709–6721. doi: 10.1093/nar/11.19.6709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Loughney K., Lund E., Dahlberg J. E. tRNA genes are found between 16S and 23S rRNA genes in Bacillus subtilis. Nucleic Acids Res. 1982 Mar 11;10(5):1607–1624. doi: 10.1093/nar/10.5.1607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Maniatis T., Hardison R. C., Lacy E., Lauer J., O'Connell C., Quon D., Sim G. K., Efstratiadis A. The isolation of structural genes from libraries of eucaryotic DNA. Cell. 1978 Oct;15(2):687–701. doi: 10.1016/0092-8674(78)90036-3. [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. 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]
  23. Ohta N., Newton A. Isolation and mapping of ribosomal RNA genes of Caulobacter crescentus. J Mol Biol. 1981 Dec 5;153(2):291–303. doi: 10.1016/0022-2836(81)90279-5. [DOI] [PubMed] [Google Scholar]
  24. POINDEXTER J. S. BIOLOGICAL PROPERTIES AND CLASSIFICATION OF THE CAULOBACTER GROUP. Bacteriol Rev. 1964 Sep;28:231–295. doi: 10.1128/br.28.3.231-295.1964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Peacock A. C., Dingman C. W. Resolution of multiple ribonucleic acid species by polyacrylamide gel electrophoresis. Biochemistry. 1967 Jun;6(6):1818–1827. doi: 10.1021/bi00858a033. [DOI] [PubMed] [Google Scholar]
  26. Pribnow D. Bacteriophage T7 early promoters: nucleotide sequences of two RNA polymerase binding sites. J Mol Biol. 1975 Dec 15;99(3):419–443. doi: 10.1016/s0022-2836(75)80136-7. [DOI] [PubMed] [Google Scholar]
  27. Purucker M., Bryan R., Amemiya K., Ely B., Shapiro L. Isolation of a Caulobacter gene cluster specifying flagellum production by using nonmotile Tn5 insertion mutants. Proc Natl Acad Sci U S A. 1982 Nov;79(22):6797–6801. doi: 10.1073/pnas.79.22.6797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Rosenberg M., Court D. Regulatory sequences involved in the promotion and termination of RNA transcription. Annu Rev Genet. 1979;13:319–353. doi: 10.1146/annurev.ge.13.120179.001535. [DOI] [PubMed] [Google Scholar]
  29. Shine J., Dalgarno L. Determinant of cistron specificity in bacterial ribosomes. Nature. 1975 Mar 6;254(5495):34–38. doi: 10.1038/254034a0. [DOI] [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. Takaiwa F., Sugiura M. Nucleotide sequence of the 16S - 23S spacer region in an rRNA gene cluster from tobacco chloroplast DNA. Nucleic Acids Res. 1982 Apr 24;10(8):2665–2676. doi: 10.1093/nar/10.8.2665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Tinoco I., Jr, Borer P. N., Dengler B., Levin M. D., Uhlenbeck O. C., Crothers D. M., Bralla J. Improved estimation of secondary structure in ribonucleic acids. Nat New Biol. 1973 Nov 14;246(150):40–41. doi: 10.1038/newbio246040a0. [DOI] [PubMed] [Google Scholar]
  33. Woese C. R., Gutell R., Gupta R., Noller H. F. Detailed analysis of the higher-order structure of 16S-like ribosomal ribonucleic acids. Microbiol Rev. 1983 Dec;47(4):621–669. doi: 10.1128/mr.47.4.621-669.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]

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

RESOURCES