Skip to main content
NCBI home page
Biochemical Journal logoLink to Biochemical Journal
. 1971 Apr;122(2):139–148. doi: 10.1042/bj1220139

Ribosomal ribonucleic acid synthesis in Bacillus subtilis

R J Avery 1,2, J E M Midgley 1,2
PMCID: PMC1176757  PMID: 4330148

Abstract

The mode of biosynthesis of the 16S and 23S ribosomal ribonucleic acids (rRNA) was studied in Bacillus subtilis 168thy−. Three criteria were used to define the characteristics of the rRNA species: (i) the time required at 37°C to synthesize 16S and 23S rRNA chains de novo in growing cultures; (ii) the degree of reactivity of the 3′-terminal groups of the rRNA molecules with periodate and [carbonyl-14C]isonicotinic acid hydrazide; and (iii) the reactivity of the 5′-terminal regions of the rRNA molecules with the bacterial exonuclease purified by Riley (1969). The 16S and 23S chains of B. subtilis were synthesized at rates of 22±2 and 21±2 nucleotides added/s. The periodate–[14C]isonicotinic acid hydrazide and the exonuclease techniques for estimating apparent chain lengths of RNA indicated that the chain length of the 23S rRNA was 1.8 times that of the 16S fraction. The apparent chain lengths of each rRNA species were: 16S rRNA, 1650±50 nucleotide residues; 23S rRNA, 3050±90 nucleotide residues. It appears that, the 16S and 23S rRNA molecules in B. subtilis are synthesized in the expected manner, by simple polymerization of the final products on independent cistrons.

Full text

PDF
139

Selected References

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

  1. Attardi G., Huang P. C., Kabat S. Recognition of ribosomal RNA sites in DNA. I. Analysis of the E. coli system. Proc Natl Acad Sci U S A. 1965 Jun;53(6):1490–1498. doi: 10.1073/pnas.53.6.1490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Avery R. J., Midgley J. E. A new approach to the analysis of hybridization of bacterial nucleic acids. Analysis of the ribosomal ribonucleic acids of Bacillus subtilis. Biochem J. 1969 Nov;115(3):383–394. doi: 10.1042/bj1150383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Avery R. J., Midgley J. E., Pigott G. H. An analysis of the ribosomal ribonucleic acids of Escherichia coli by hybridization techniques. Biochem J. 1969 Nov;115(3):395–403. doi: 10.1042/bj1150395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. BOLTON E. T., McCARTHY B. J. A general method for the isolation of RNA complementary to DNA. Proc Natl Acad Sci U S A. 1962 Aug;48:1390–1397. doi: 10.1073/pnas.48.8.1390. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. BUCHWALD M., BRITTEN R. J. Incorporation of ribonucleic acid bases into the metabolic pool and RNA of E. coli. Biophys J. 1963 Mar;3:155–166. doi: 10.1016/s0006-3495(63)86811-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bremer H., Yuan D. RNA chain growth-rate in Escherichia coli. J Mol Biol. 1968 Dec 14;38(2):163–180. doi: 10.1016/0022-2836(68)90404-x. [DOI] [PubMed] [Google Scholar]
  7. Colli W., Oishi M. Ribosomal RNA genes in bacteria: evidence for the nature of the physical linkage between 16S and 23S RNA genes in Bacillus subtilis. Proc Natl Acad Sci U S A. 1969 Oct;64(2):642–649. doi: 10.1073/pnas.64.2.642. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Doi R. H., Igarashi R. T. Heterogeneity of the conserved ribosomal ribonucleic acid sequences of Bacillus subtilis. J Bacteriol. 1966 Jul;92(1):88–96. doi: 10.1128/jb.92.1.88-96.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fellner P., Sanger F. Sequence analysis of specific areas of the 16S and 23S ribosomal RNAs. Nature. 1968 Jul 20;219(5151):236–238. doi: 10.1038/219236a0. [DOI] [PubMed] [Google Scholar]
  10. GESTELAND R. F., BOEDTKER H. SOME PHYSICAL PROPERTIES OF BACTERIOPHAGE R17 AND ITS RIBONUCLEIC ACID. J Mol Biol. 1964 Apr;8:496–507. doi: 10.1016/s0022-2836(64)80007-3. [DOI] [PubMed] [Google Scholar]
  11. HUNT J. A. TERMINAL-SEQUENCE STUDIES OF HIGH-MOLECULAR-WEIGHT RIBONUCLEIC. THE REACTION OF PERIODATE-OXIDIZED RIBONUCLEOSIDES , 5'-RIBONUCLEOTIDES AND RIBONUCLEIC ACID WITH ISONIAZID. Biochem J. 1965 May;95:541–551. doi: 10.1042/bj0950541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hecht N. B., Woese C. R. Separation of bacterial ribosomal ribonucleic acid from its macromolecular precursors by polyacrylamide gel electrophoresis. J Bacteriol. 1968 Mar;95(3):986–990. doi: 10.1128/jb.95.3.986-990.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Loening U. E. Molecular weights of ribosomal RNA in relation to evolution. J Mol Biol. 1968 Dec;38(3):355–365. doi: 10.1016/0022-2836(68)90391-4. [DOI] [PubMed] [Google Scholar]
  14. MANDELL J. D., HERSHEY A. D. A fractionating column for analysis of nucleic acids. Anal Biochem. 1960 Jun;1:66–77. doi: 10.1016/0003-2697(60)90020-8. [DOI] [PubMed] [Google Scholar]
  15. MCCARTHY B. J., BOLTON E. T. INTERACTION OF COMPLEMENTARY RNA AND DNA. J Mol Biol. 1964 Feb;8:184–200. doi: 10.1016/s0022-2836(64)80128-5. [DOI] [PubMed] [Google Scholar]
  16. MIDGLEY J. E. EFFECTS OF DIFFERENT EXTRACTION PROCEDURES ON THE MOLECULAR CHARACTERISTICS OF BACTERIAL RIBOSOMAL RIBONUCLEIC ACID. Biochim Biophys Acta. 1965 Feb 8;95:232–243. doi: 10.1016/0005-2787(65)90488-0. [DOI] [PubMed] [Google Scholar]
  17. Mangiarotti G., Apirion D., Schlessinger D., Silengo L. Biosynthetic precursors of 30S and 50S ribosomal particles in Escherichia coli. Biochemistry. 1968 Jan;7(1):456–472. doi: 10.1021/bi00841a058. [DOI] [PubMed] [Google Scholar]
  18. McCarthy B. J., Britten R. J. The Synthesis of Ribosomes in E. coli: I. The Incorporation of C-Uracil into the Metabolic Pool and RNA. Biophys J. 1962 Jan;2(1):35–47. doi: 10.1016/s0006-3495(62)86839-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. McIlreavy D. J., Midgley J. E. The chemical structure of bacterial ribosomal RNA. I. Terminal nucleotide sequences of Escherichia coli ribosomal RNA. Biochim Biophys Acta. 1967 Jun 20;142(1):47–64. doi: 10.1016/0005-2787(67)90514-x. [DOI] [PubMed] [Google Scholar]
  20. Midgley J. E., McIlreavy D. J. The isonicotinyl hydrazones of Escherichia coli ribosomal ribonucleic acids. Biochim Biophys Acta. 1967 Sep 26;145(2):512–514. doi: 10.1016/0005-2787(67)90071-8. [DOI] [PubMed] [Google Scholar]
  21. Midgley J. E. The estimation of polynucleotide chain length by a chemical method. Biochim Biophys Acta. 1965 Nov 8;108(3):340–347. doi: 10.1016/0005-2787(65)90026-2. [DOI] [PubMed] [Google Scholar]
  22. Midgley J. E. The isonicotinyl hydrazones of nucleosides and their phosphorylated derivatives. Biochim Biophys Acta. 1966 Jul 20;123(1):210–213. doi: 10.1016/0005-2787(66)90177-8. [DOI] [PubMed] [Google Scholar]
  23. Midgley J. E. The messenger ribonucleic acid content of Bacillus subtilis 168. Biochem J. 1969 Nov;115(2):171–181. doi: 10.1042/bj1150171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Oishi M., Sueoka N. Location of genetic loci of ribosomal RNA on Bacillus subtilis chromosome. Proc Natl Acad Sci U S A. 1965 Aug;54(2):483–491. doi: 10.1073/pnas.54.2.483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Pace B., Peterson R. L., Pace N. R. Formation of all stable RNA species in Escherichia coli by posttranscriptional modification. Proc Natl Acad Sci U S A. 1970 Apr;65(4):1097–1104. doi: 10.1073/pnas.65.4.1097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Pettijohn D. E., Stonington O. G., Kossman C. R. Chain termination of ribosomal RNA synthesis in vitro. Nature. 1970 Oct 17;228(5268):235–239. doi: 10.1038/228235a0. [DOI] [PubMed] [Google Scholar]
  27. Pigott G. H., Midgley J. E. Characterization of rapidly labelled ribonucleic acid in Escherichia coli by deoxyribonucleic acid-ribonucleic acid hybridization. Biochem J. 1968 Nov;110(2):251–263. doi: 10.1042/bj1100251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Purdom I., Bishop J. O., Birnstiel M. L. Scattered arrangement of the bacterial ribosomal cistrons. Nature. 1970 Jul 18;227(5255):239–242. doi: 10.1038/227239a0. [DOI] [PubMed] [Google Scholar]
  29. Riley W. T. Polynucleotide chain lengths of rapidly labelled and ribosomal RNA of mammalian cells and E. coli. Nature. 1969 May 3;222(5192):446–452. doi: 10.1038/222446a0. [DOI] [PubMed] [Google Scholar]
  30. Smith I., Dubnau D., Morrell P., Marmur J. Chromosomal location of DNA base sequences complementary to transfer RNA and to 5 s, 16 s and 23 s ribosomal RNA in Bacillus subtilis. J Mol Biol. 1968 Apr 14;33(1):123–140. doi: 10.1016/0022-2836(68)90285-4. [DOI] [PubMed] [Google Scholar]
  31. Stanley W. M., Jr, Bock R. M. Isolation and physical properties of the ribosomal ribonucleic acid of Escherichia coli. Biochemistry. 1965 Jul;4(7):1302–1311. doi: 10.1021/bi00883a014. [DOI] [PubMed] [Google Scholar]
  32. Walker G. J. Metabolism of the reserve polysaccharide of Streptococcus mitis. Some properties of a pullulanase. Biochem J. 1968 Jun;108(1):33–40. doi: 10.1042/bj1080033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. YANKOFSKY S. A., SPIEGELMAN S. Distinct cistrons for the two ribosomal RNA components. Proc Natl Acad Sci U S A. 1963 Apr;49:538–544. doi: 10.1073/pnas.49.4.538. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Zimmermann R. A., Levinthal C. Messenger RNA and RNA transcription time. J Mol Biol. 1967 Dec 14;30(2):349–370. [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES