Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1970 Sep;103(3):560–568. doi: 10.1128/jb.103.3.560-568.1970

Asymmetric Template Function of Microbial Deoxyribonucleic Acids: Transcription of Ribosomal and Soluble Ribonucleic Acids

Lola Margulies 1, Virgilija Remeza 1, Rivka Rudner 1
PMCID: PMC248127  PMID: 4319834

Abstract

In Bacillus subtilis and Escherichia coli, 16 and 23S ribosomal ribonucleic acid (rRNA) hybridize exclusively with the heavy (H) strand of methylated albuminkieselguhr (MAK)-fractionated complementary deoxyribonucleic acid (DNA) strands. All the soluble RNA (4S RNA) in B. subtilis and 66 to 75% of the 4S RNA in E. coli also hybridize with the H strand. Interspecific hybridization shows that E. coli 23S rRNA also binds selectively to the DNA H strand of Salmonella typhimurium. The hybridization peak for all three cellular RNA components is specifically located in the late-eluting region of the absorbance profile of the DNA H strand. The early-eluting region of the light (L) strand preferentially inhibits the hybridization between the peak region of the H strand and 23S rRNA. These regions are considered to represent the transcribing sequences and their complements for 23S rRNA in the separated H and L strands of DNA, respectively.

Full text

PDF
561

Selected References

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

  1. Borst P., Aaij C. Identification of the heavy strand of rat-liver mitochondrial DNA as the messenger strand. Biochem Biophys Res Commun. 1969 Feb 7;34(3):358–364. doi: 10.1016/0006-291x(69)90841-9. [DOI] [PubMed] [Google Scholar]
  2. CORDES S., EPSTEIN H. T., MARMUR J. Some properties of the deoxyribonucleic acid of phage alpha. Nature. 1961 Sep 9;191:1097–1098. doi: 10.1038/1911097b0. [DOI] [PubMed] [Google Scholar]
  3. Colvill A. J., Kanner L. C., Tocchini-Valentini G. P., Sarnat M. T., Geiduschek E. P. Asymmetric RNA synthesis in vitro: heterologous DNA-enzyme systems; E. coli RNA polymerase. Proc Natl Acad Sci U S A. 1965 May;53(5):1140–1147. doi: 10.1073/pnas.53.5.1140. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Corneo G., Ginelli E., Soave C., Bernardi G. Isolation and characterization of mouse and guinea pig satellite deoxyribonucleic acids. Biochemistry. 1968 Dec;7(12):4373–4379. doi: 10.1021/bi00852a033. [DOI] [PubMed] [Google Scholar]
  5. DAVIS B. D., MINGIOLI E. S. Mutants of Escherichia coli requiring methionine or vitamin B12. J Bacteriol. 1950 Jul;60(1):17–28. doi: 10.1128/jb.60.1.17-28.1950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dubnau D., Smith I., Morell P., Marmur J. Gene conservation in Bacillus species. I. Conserved genetic and nucleic acid base sequence homologies. Proc Natl Acad Sci U S A. 1965 Aug;54(2):491–498. doi: 10.1073/pnas.54.2.491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Flamm W. G., McCallum M., Walker P. M. The isolation of complementary strands from a mouse DNA fraction. Proc Natl Acad Sci U S A. 1967 Jun;57(6):1729–1734. doi: 10.1073/pnas.57.6.1729. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. GIACOMONI D., SPIEGELMAN S. Origin and biologic individuality of the genetic dictionary. Science. 1962 Dec 21;138(3547):1328–1331. doi: 10.1126/science.138.3547.1328. [DOI] [PubMed] [Google Scholar]
  9. GOODMAN H. M., RICH A. Formation of a DNA-soluble RNA hybrid and its relation to the origin, evolution, and degeneracy of soluble RNA. Proc Natl Acad Sci U S A. 1962 Dec 15;48:2101–2109. doi: 10.1073/pnas.48.12.2101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gillespie D., Spiegelman S. A quantitative assay for DNA-RNA hybrids with DNA immobilized on a membrane. J Mol Biol. 1965 Jul;12(3):829–842. doi: 10.1016/s0022-2836(65)80331-x. [DOI] [PubMed] [Google Scholar]
  11. Guha A., Szybalski W. Fractionation of the complementary strands of coliphage T4 DNA based on the asymmetric distribution of the poly U and poly U,G binding sites. Virology. 1968 Apr;34(4):608–616. doi: 10.1016/0042-6822(68)90082-2. [DOI] [PubMed] [Google Scholar]
  12. Hogness D. S., Doerfler W., Egan J. B., Black L. W. The position and orientation of genes in lambda and lambda dg DNA. Cold Spring Harb Symp Quant Biol. 1966;31:129–138. doi: 10.1101/sqb.1966.031.01.020. [DOI] [PubMed] [Google Scholar]
  13. Karkas J. D., Rudner R., Chargaff E. Seapration of B. subtilis DNA into complementary strands. II. Template functions and composition as determined by transcription with RNA polymerase. Proc Natl Acad Sci U S A. 1968 Jul;60(3):915–920. doi: 10.1073/pnas.60.3.915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kennell D., Kotoulas A. Titration of the gene sites on DNA by DNA-RNA hybridization. I. Problem of measurement. J Mol Biol. 1968 May 28;34(1):71–84. doi: 10.1016/0022-2836(68)90235-0. [DOI] [PubMed] [Google Scholar]
  15. LEVINTHAL C., KEYNAN A., HIGA A. Messenger RNA turnover and protein synthesis in B. subtilis inhibited by actinomycin D. Proc Natl Acad Sci U S A. 1962 Sep 15;48:1631–1638. doi: 10.1073/pnas.48.9.1631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. MARGOLIN P. BIPOLARITY OF INFORMATION TRANSFER FROM THE SALMONELLA TYPHIMURIUM CHROMOSOME. Science. 1965 Mar 19;147(3664):1456–1458. doi: 10.1126/science.147.3664.1456. [DOI] [PubMed] [Google Scholar]
  17. MARMUR J., GREENSPAN C. M. TRANSCRIPTION IN VIVO OF DNA FROM BACTERIOPHAGE SP8. Science. 1963 Oct 18;142(3590):387–389. doi: 10.1126/science.142.3590.387. [DOI] [PubMed] [Google Scholar]
  18. Morell P., Smith I., Dubnau D., Marmur J. Isolation and characterization of low molecular weight ribonucleic acid species from Bacillus subtilis. Biochemistry. 1967 Jan;6(1):258–265. doi: 10.1021/bi00853a040. [DOI] [PubMed] [Google Scholar]
  19. NYGAARD A. P., HALL B. D. A method for the detection of RNA-DNA complexes. Biochem Biophys Res Commun. 1963 Jul 18;12:98–104. doi: 10.1016/0006-291x(63)90242-0. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Oishi M. The transcribing strands of bacillus subtilis DNA for ribosomal and transfer RNA. Proc Natl Acad Sci U S A. 1969 Jan;62(1):256–262. doi: 10.1073/pnas.62.1.256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Riva S. C. Asymmetric transcription of B. subtilis phage SPP1 DNA in vitro. Biochem Biophys Res Commun. 1969 Mar 31;34(6):824–830. doi: 10.1016/0006-291x(69)90254-x. [DOI] [PubMed] [Google Scholar]
  23. Riva S., Polsinelli M., Falaschi A. A new phage of Bacillus subtilis with infectious DNA having separable strands. J Mol Biol. 1968 Jul 28;35(2):347–356. doi: 10.1016/s0022-2836(68)80029-4. [DOI] [PubMed] [Google Scholar]
  24. Rudner R., Karkas J. D., Chargaff E. Separation of B. subtilis DNA into complementary strands, I. Biological properties. Proc Natl Acad Sci U S A. 1968 Jun;60(2):630–635. doi: 10.1073/pnas.60.2.630. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rudner R., Karkas J. D., Chargaff E. Separation of B. subtilis DNA into complementary strands. 3. Direct analysis. Proc Natl Acad Sci U S A. 1968 Jul;60(3):921–922. doi: 10.1073/pnas.60.3.921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rudner R., Karkas J. D., Chargaff E. Separation of microbial deoxyribonucleic acids into complementary strands. Proc Natl Acad Sci U S A. 1969 May;63(1):152–159. doi: 10.1073/pnas.63.1.152. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rudner R., Lin H. J., Hoffmann E. M., Chargaff E. Studies on the loss and the restoration of the transforming activity of the deoxyribonucleic acid of Bacillus subtilis. Biochim Biophys Acta. 1967 Nov 21;149(1):199–219. doi: 10.1016/0005-2787(67)90702-2. [DOI] [PubMed] [Google Scholar]
  28. Rudner R., Shapiro H. S., Chargaff E. Studies on the nucleotide arrangement in deoxyribonucleic acids. X. Frequency and composition of pyrimidine isostichs in microbial deoxyribonucleic acids and in the DNA of E. coli phage T3. Biochim Biophys Acta. 1966 Oct 24;129(1):85–103. [PubMed] [Google Scholar]
  29. SANDERSON K. E., DEMEREC M. THE LINKAGE MAP OF SALMONELLA TYPHIMURIUM. Genetics. 1965 Jun;51:897–913. doi: 10.1093/genetics/51.6.897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. SUEOKA N., CHENG T. Y. Fractionation of nucleic acids with the methylated albumin column. J Mol Biol. 1962 Mar;4:161–172. doi: 10.1016/s0022-2836(62)80048-5. [DOI] [PubMed] [Google Scholar]
  31. Sanderson K. E. Information transfer in Salmonella typhimurium. Proc Natl Acad Sci U S A. 1965 Jun;53(6):1335–1340. doi: 10.1073/pnas.53.6.1335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sanderson K. E. Revised linkage map of Salmonella typhimurium. Bacteriol Rev. 1967 Dec;31(4):354–372. doi: 10.1128/br.31.4.354-372.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Saunders G. F., Campbell L. L. Properties of the deoxyribonucleic acid of the thermophilic bacteriophage TP-84. Biochemistry. 1965 Dec;4(12):2836–2844. doi: 10.1021/bi00888a039. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Spizizen J. TRANSFORMATION OF BIOCHEMICALLY DEFICIENT STRAINS OF BACILLUS SUBTILIS BY DEOXYRIBONUCLEATE. Proc Natl Acad Sci U S A. 1958 Oct 15;44(10):1072–1078. doi: 10.1073/pnas.44.10.1072. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Streisinger G., Emrich J., Okada Y., Tsugita A., Inouye M. Direction of translation of the lysozyme gene of bacteriophage T4 relative to the linkage map. J Mol Biol. 1968 Feb 14;31(3):607–612. doi: 10.1016/0022-2836(68)90431-2. [DOI] [PubMed] [Google Scholar]
  37. Szybalski W., Kubinski H., Sheldrick P. Pyrimidine clusters on the transcribing strand of DNA and their possible role in the initiation of RNA synthesis. Cold Spring Harb Symp Quant Biol. 1966;31:123–127. doi: 10.1101/sqb.1966.031.01.019. [DOI] [PubMed] [Google Scholar]
  38. TOCCHINI-VALENTINI G. P., STODOLSKY M., AURISICCHIO A., SARNAT M., GRAZIOSI F., WEISS S. B., GEIDUSCHEK E. P. ON THE ASYMMETRY OF RNA SYNTHESIS IN VIVO. Proc Natl Acad Sci U S A. 1963 Nov;50:935–942. doi: 10.1073/pnas.50.5.935. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Taylor A. L., Trotter C. D. Revised linkage map of Escherichia coli. Bacteriol Rev. 1967 Dec;31(4):332–353. doi: 10.1128/br.31.4.332-353.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. YANKOFSKY S. A., SPIEGELMAN S. The identification of the ribosomal RNA cistron by sequence complementarity. II. Saturation of and competitive interaction at the RNA cistron. Proc Natl Acad Sci U S A. 1962 Aug;48:1466–1472. doi: 10.1073/pnas.48.8.1466. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES