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. 1983 May 11;11(9):2599–2616. doi: 10.1093/nar/11.9.2599

The spc ribosomal protein operon of Escherichia coli: sequence and cotranscription of the ribosomal protein genes and a protein export gene.

D P Cerretti, D Dean, G R Davis, D M Bedwell, M Nomura
PMCID: PMC325911  PMID: 6222285

Abstract

The genes encoding the 52 ribosomal proteins (r-proteins) of Escherichia coli are organized into approximately 19 operons scattered throughout the chromosome. One of these, the spc operon, contains the genes for ten ribosomal proteins: L14, L24, L5, S14, S8, L6, L18, S5, L30 and L15 (rp1N, rp1X, rp1E, rpsN, rpsH, rp1F, rp1R, rpsE, rpmD, and rp1O). We now report the entire 5.9 kb nucleotide sequence of the spc operon. DNA sequence analysis has confirmed the genetic organization and refined the amino acid sequence of the ten r-proteins in this operon. It has also revealed the presence of two open reading frames past the last known gene (L15) of the spc operon. One of these corresponds to a gene (pr1A or secY) which recently has been shown by others to be involved in protein export. In addition, S1 mapping experiments indicate that a significant proportion of transcription initiated from the spc operon continues not only into the two putative genes, but also without termination into the downstream alpha r-protein operon.

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Selected References

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  1. Adhya S., Gottesman M. Promoter occlusion: transcription through a promoter may inhibit its activity. Cell. 1982 Jul;29(3):939–944. doi: 10.1016/0092-8674(82)90456-1. [DOI] [PubMed] [Google Scholar]
  2. Allen G., Wittmann-Liebold B. The amino acid sequence of the ribosomal protein S8 of Escherichia coli. Hoppe Seylers Z Physiol Chem. 1978 Nov;359(11):1509–1525. doi: 10.1515/bchm2.1978.359.2.1509. [DOI] [PubMed] [Google Scholar]
  3. Berk A. J., Sharp P. A. Spliced early mRNAs of simian virus 40. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1274–1278. doi: 10.1073/pnas.75.3.1274. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brosius J., Schiltz E., Chen R. The primary structure of the 5S RNA binding protein L18 from Escherichia coli ribosomes. FEBS Lett. 1975 Aug 15;56(2):359–361. doi: 10.1016/0014-5793(75)81127-6. [DOI] [PubMed] [Google Scholar]
  5. Brückner R., Matzura H. In vivo synthesis of a polycistronic messenger RNA for the ribosomal proteins L11, L1, L10 and L7/12 in Escherichia coli. Mol Gen Genet. 1981;183(2):277–282. doi: 10.1007/BF00270629. [DOI] [PubMed] [Google Scholar]
  6. Chen R., Arfsten U., Chen-Schmeisser U. The primary structure of protein L6 from the aminoacyl-tRNA binding site of the Escherichia coli ribosome. Hoppe Seylers Z Physiol Chem. 1977 Apr;358(4):531–535. [PubMed] [Google Scholar]
  7. Chen R., Ehrke G. The primary structure of the 5 S RNA binding protein L5 of Escherichia coli ribosomes. FEBS Lett. 1976 Oct 15;69(1):240–245. doi: 10.1016/0014-5793(76)80695-3. [DOI] [PubMed] [Google Scholar]
  8. Coulondre C., Miller J. H. Genetic studies of the lac repressor. III. Additional correlation of mutational sites with specific amino acid residues. J Mol Biol. 1977 Dec 15;117(3):525–567. doi: 10.1016/0022-2836(77)90056-0. [DOI] [PubMed] [Google Scholar]
  9. Dean D., Yates J. L., Nomura M. Escherichia coli ribosomal protein S8 feedback regulates part of spc operon. Nature. 1981 Jan 1;289(5793):89–91. doi: 10.1038/289089a0. [DOI] [PubMed] [Google Scholar]
  10. Emr S. D., Hanley-Way S., Silhavy T. J. Suppressor mutations that restore export of a protein with a defective signal sequence. Cell. 1981 Jan;23(1):79–88. doi: 10.1016/0092-8674(81)90272-5. [DOI] [PubMed] [Google Scholar]
  11. Fallon A. M., Jinks C. S., Yamamoto M., Nomura M. Expression of ribosomal protein genes cloned in a hybrid plasmid in Escherichia coli: gene dosage effects on synthesis of ribosomal proteins and ribosomal protein messenger ribonucleic acid. J Bacteriol. 1979 May;138(2):383–396. doi: 10.1128/jb.138.2.383-396.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Farabaugh P. J. Sequence of the lacI gene. Nature. 1978 Aug 24;274(5673):765–769. doi: 10.1038/274765a0. [DOI] [PubMed] [Google Scholar]
  13. Garoff H., Ansorge W. Improvements of DNA sequencing gels. Anal Biochem. 1981 Aug;115(2):450–457. doi: 10.1016/0003-2697(81)90031-2. [DOI] [PubMed] [Google Scholar]
  14. Giorginis S., Chen R. The primary structure of protein L15 located at the peptidyltransferase center of Escherichia coli ribosomes. FEBS Lett. 1977 Dec 15;84(2):347–350. doi: 10.1016/0014-5793(77)80722-9. [DOI] [PubMed] [Google Scholar]
  15. Gouy M., Gautier C. Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Res. 1982 Nov 25;10(22):7055–7074. doi: 10.1093/nar/10.22.7055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Grosjean H., Fiers W. Preferential codon usage in prokaryotic genes: the optimal codon-anticodon interaction energy and the selective codon usage in efficiently expressed genes. Gene. 1982 Jun;18(3):199–209. doi: 10.1016/0378-1119(82)90157-3. [DOI] [PubMed] [Google Scholar]
  17. Jaskunas S. R., Fallon A. M., Nomura M. Identification and organization of ribosomal protein genes of Escherichia coli carried by lambdafus2 transducing phage. J Biol Chem. 1977 Oct 25;252(20):7323–7336. [PubMed] [Google Scholar]
  18. Jaskunas S. R., Fallon A. M., Nomura M., Williams B. G., Blattner F. R. Expression of ribosomal protein genes cloned in Charon vector phages and identification of their promoters. J Biol Chem. 1977 Oct 25;252(20):7355–7364. [PubMed] [Google Scholar]
  19. Jaskunas S. R., Lindahl L., Nomura M. Isolation of polar insertion mutants and the direction of transcription of ribosomal protein genes in E. coli. Nature. 1975 Jul 17;256(5514):183–187. doi: 10.1038/256183a0. [DOI] [PubMed] [Google Scholar]
  20. Jaskunas S. R., Lindahl L., Nomura M. Specialized transducing phages for ribosomal protein genes of Escherichia coli. Proc Natl Acad Sci U S A. 1975 Jan;72(1):6–10. doi: 10.1073/pnas.72.1.6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Jaskunas S. R., Nomura M. Organization of ribosomal protein genes of Escherichia coli as analyzed by polar insertion mutations. J Biol Chem. 1977 Oct 25;252(20):7337–7343. [PubMed] [Google Scholar]
  22. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  23. Lindahl L., Post L., Zengel J., Gilbert S. F., Strycharz W. A., Nomura M. Mapping of ribosomal protein genes by in vitro protein synthesis using DNA fragments of lambdafus3 transducing phage DNA as templates. J Biol Chem. 1977 Oct 25;252(20):7365–7383. [PubMed] [Google Scholar]
  24. Lindahl L., Zengel J. M. Expression of ribosomal genes in bacteria. Adv Genet. 1982;21:53–121. doi: 10.1016/s0065-2660(08)60297-7. [DOI] [PubMed] [Google Scholar]
  25. Maxam A. M., Gilbert W. A new method for sequencing DNA. Proc Natl Acad Sci U S A. 1977 Feb;74(2):560–564. doi: 10.1073/pnas.74.2.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Messing J., Crea R., Seeburg P. H. A system for shotgun DNA sequencing. Nucleic Acids Res. 1981 Jan 24;9(2):309–321. doi: 10.1093/nar/9.2.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Messing J., Vieira J. A new pair of M13 vectors for selecting either DNA strand of double-digest restriction fragments. Gene. 1982 Oct;19(3):269–276. doi: 10.1016/0378-1119(82)90016-6. [DOI] [PubMed] [Google Scholar]
  28. Miura A., Krueger J. H., Itoh S., de Boer H. A., Nomura M. Growth-rate-dependent regulation of ribosome synthesis in E. coli: expression of the lacZ and galK genes fused to ribosomal promoters. Cell. 1981 Sep;25(3):773–782. doi: 10.1016/0092-8674(81)90185-9. [DOI] [PubMed] [Google Scholar]
  29. Morinaga T., Funatsu G., Funatsu M. Primary structure of protein L14 isolated from Escherichia coli ribosomes. FEBS Lett. 1978 Jul 1;91(1):74–77. doi: 10.1016/0014-5793(78)80020-9. [DOI] [PubMed] [Google Scholar]
  30. Nomura M., Yates J. L., Dean D., Post L. E. Feedback regulation of ribosomal protein gene expression in Escherichia coli: structural homology of ribosomal RNA and ribosomal protein MRNA. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7084–7088. doi: 10.1073/pnas.77.12.7084. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Olins P. O., Nomura M. Translational regulation by ribosomal protein S8 in Escherichia coli: structural homology between rRNA binding site and feedback target on mRNA. Nucleic Acids Res. 1981 Apr 10;9(7):1757–1764. doi: 10.1093/nar/9.7.1757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Platt T. Termination of transcription and its regulation in the tryptophan operon of E. coli. Cell. 1981 Apr;24(1):10–23. doi: 10.1016/0092-8674(81)90496-7. [DOI] [PubMed] [Google Scholar]
  33. Post L. E., Arfsten A. E., Davis G. R., Nomura M. DNA sequence of the promoter region for the alpha ribosomal protein operon in Escherichia coli. J Biol Chem. 1980 May 25;255(10):4653–4659. [PubMed] [Google Scholar]
  34. Post L. E., Arfsten A. E., Reusser F., Nomura M. DNA sequences of promoter regions for the str and spc ribosomal protein operons in E. coli. Cell. 1978 Sep;15(1):215–229. doi: 10.1016/0092-8674(78)90096-x. [DOI] [PubMed] [Google Scholar]
  35. Post L. E., Nomura M. DNA sequences from the str operon of Escherichia coli. J Biol Chem. 1980 May 25;255(10):4660–4666. [PubMed] [Google Scholar]
  36. Post L. E., Strycharz G. D., Nomura M., Lewis H., Dennis P. P. Nucleotide sequence of the ribosomal protein gene cluster adjacent to the gene for RNA polymerase subunit beta in Escherichia coli. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1697–1701. doi: 10.1073/pnas.76.4.1697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Ritter E., Wittmann-Liebold B. The primary structure of protein L30 from Escherichia coli ribosomes. FEBS Lett. 1975 Dec 1;60(1):153–155. doi: 10.1016/0014-5793(75)80440-6. [DOI] [PubMed] [Google Scholar]
  38. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Shine J., Dalgarno L. The 3'-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1342–1346. doi: 10.1073/pnas.71.4.1342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Shultz J., Silhavy T. J., Berman M. L., Fiil N., Emr S. D. A previously unidentified gene in the spc operon of Escherichia coli K12 specifies a component of the protein export machinery. Cell. 1982 Nov;31(1):227–235. doi: 10.1016/0092-8674(82)90422-6. [DOI] [PubMed] [Google Scholar]
  41. Squires C., Krainer A., Barry G., Shen W. F., Squires C. L. Nucleotide sequence at the end of the gene for the RNA polymerase beta' subunit (rpoC). Nucleic Acids Res. 1981 Dec 21;9(24):6827–6840. doi: 10.1093/nar/9.24.6827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Staden R. A new computer method for the storage and manipulation of DNA gel reading data. Nucleic Acids Res. 1980 Aug 25;8(16):3673–3694. doi: 10.1093/nar/8.16.3673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Vieira J., Messing J. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene. 1982 Oct;19(3):259–268. doi: 10.1016/0378-1119(82)90015-4. [DOI] [PubMed] [Google Scholar]
  44. Walter P., Blobel G. Purification of a membrane-associated protein complex required for protein translocation across the endoplasmic reticulum. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7112–7116. doi: 10.1073/pnas.77.12.7112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Walter P., Blobel G. Signal recognition particle contains a 7S RNA essential for protein translocation across the endoplasmic reticulum. Nature. 1982 Oct 21;299(5885):691–698. doi: 10.1038/299691a0. [DOI] [PubMed] [Google Scholar]
  46. Wittmann-Liebold B., Greuer B. The primary structure of protein S5 from the small subunit of the Escherichia coli ribosome. FEBS Lett. 1978 Nov 1;95(1):91–98. doi: 10.1016/0014-5793(78)80059-3. [DOI] [PubMed] [Google Scholar]
  47. Wittmann-Liebold B. Primary structure of protein L24 from the Escherichia coli ribosome. FEBS Lett. 1979 Dec 1;108(1):75–80. doi: 10.1016/0014-5793(79)81182-5. [DOI] [PubMed] [Google Scholar]
  48. Yanofsky C., Platt T., Crawford I. P., Nichols B. P., Christie G. E., Horowitz H., VanCleemput M., Wu A. M. The complete nucleotide sequence of the tryptophan operon of Escherichia coli. Nucleic Acids Res. 1981 Dec 21;9(24):6647–6668. doi: 10.1093/nar/9.24.6647. [DOI] [PMC free article] [PubMed] [Google Scholar]

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