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. 1996 Sep;178(17):5309–5315. doi: 10.1128/jb.178.17.5309-5315.1996

Genetic control of the resistance to phage C1 of Escherichia coli K-12.

N A Likhacheva 1, V V Samsonov 1, V V Samsonov 1, S P Sineoky 1
PMCID: PMC178332  PMID: 8752353

Abstract

Escherichia coli K-12 lytic phage C1 was earlier isolated in our laboratory. Its adsorption is controlled by at least three bacterial genes: dcrA, dcrB, and btuB. Our results provide evidence that the dcrA gene located at 60 min on the E. coli genetic map is identical to the sdaC gene. This gene product is an inner membrane protein recently identified as a putative specific serine transporter. The dcrB gene, located at 76.5 min, encodes a 20-kDa processed periplasmic protein, as determined by maxicell analysis, and corresponds to a recently determined open reading frame with a previously unknown function. The btuB gene product is known to be an outer membrane receptor protein responsible for adsorption of BF23 phage and vitamin B12 uptake. According to our data the DcrA and DcrB proteins are not involved in these processes. However, the DcrA protein probably participates in some cell division steps.

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Selected References

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  1. Ahmer B. M., Thomas M. G., Larsen R. A., Postle K. Characterization of the exbBD operon of Escherichia coli and the role of ExbB and ExbD in TonB function and stability. J Bacteriol. 1995 Aug;177(16):4742–4747. doi: 10.1128/jb.177.16.4742-4747.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aufrère R., Tempête M., Bohin J. P. Regulation of expression of the gene for vitamin B12 receptor cloned on a multicopy plasmid in Escherichia coli. Mol Gen Genet. 1986 Nov;205(2):358–365. doi: 10.1007/BF00430451. [DOI] [PubMed] [Google Scholar]
  3. Bradbeer C., Woodrow M. L., Khalifah L. I. Transport of vitamin B12 in Escherichia coli: common receptor system for vitamin B12 and bacteriophage BF23 on the outer membrane of the cell envelope. J Bacteriol. 1976 Mar;125(3):1032–1039. doi: 10.1128/jb.125.3.1032-1039.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Braun V., Günter K., Hantke K. Transport of iron across the outer membrane. Biol Met. 1991;4(1):14–22. doi: 10.1007/BF01135552. [DOI] [PubMed] [Google Scholar]
  5. Braun V., Schaller K., Wolff H. A common receptor protein for phage T5 and colicin M in the outer membrane of Escherichia coli B. Biochim Biophys Acta. 1973 Sep 27;323(1):87–97. doi: 10.1016/0005-2736(73)90433-1. [DOI] [PubMed] [Google Scholar]
  6. Bremer E., Middendorf A., Martinussen J., Valentin-Hansen P. Analysis of the tsx gene, which encodes a nucleoside-specific channel-forming protein (Tsx) in the outer membrane of Escherichia coli. Gene. 1990 Nov 30;96(1):59–65. doi: 10.1016/0378-1119(90)90341-n. [DOI] [PubMed] [Google Scholar]
  7. Charbit A., Werts C., Michel V., Klebba P. E., Quillardet P., Hofnung M. A role for residue 151 of LamB in bacteriophage lambda adsorption: possible steric effect of amino acid substitutions. J Bacteriol. 1994 Jun;176(11):3204–3209. doi: 10.1128/jb.176.11.3204-3209.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Close T. J., Rodriguez R. L. Construction and characterization of the chloramphenicol-resistance gene cartridge: a new approach to the transcriptional mapping of extrachromosomal elements. Gene. 1982 Dec;20(2):305–316. doi: 10.1016/0378-1119(82)90048-8. [DOI] [PubMed] [Google Scholar]
  9. Clément J. M., Lepouce E., Marchal C., Hofnung M. Genetic study of a membrane protein: DNA sequence alterations due to 17 lamB point mutations affecting adsorption of phage lambda. EMBO J. 1983;2(1):77–80. doi: 10.1002/j.1460-2075.1983.tb01384.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Di Girolamo P. M., Kadner R. J., Bradbeer C. Isolation of vitamin B 12 transport mutants of Escherichia coli. J Bacteriol. 1971 Jun;106(3):751–757. doi: 10.1128/jb.106.3.751-757.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Di Masi D. R., White J. C., Schnaitman C. A., Bradbeer C. Transport of vitamin B12 in Escherichia coli: common receptor sites for vitamin B12 and the E colicins on the outer membrane of the cell envelope. J Bacteriol. 1973 Aug;115(2):506–513. doi: 10.1128/jb.115.2.506-513.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hancock R. W., Braun V. Nature of the energy requirement for the irreversible adsorption of bacteriophages T1 and phi80 to Escherichia coli. J Bacteriol. 1976 Feb;125(2):409–415. doi: 10.1128/jb.125.2.409-415.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Heller K. J., Kadner R. J., Günther K. Suppression of the btuB451 mutation by mutations in the tonB gene suggests a direct interaction between TonB and TonB-dependent receptor proteins in the outer membrane of Escherichia coli. Gene. 1988 Apr 15;64(1):147–153. doi: 10.1016/0378-1119(88)90488-x. [DOI] [PubMed] [Google Scholar]
  14. Hufton S. E., Ward R. J., Bunce N. A., Armstrong J. T., Fletcher A. J., Glass R. E. Structure-function analysis of the vitamin B12 receptor of Escherichia coli by means of informational suppression. Mol Microbiol. 1995 Jan;15(2):381–393. doi: 10.1111/j.1365-2958.1995.tb02251.x. [DOI] [PubMed] [Google Scholar]
  15. Ito K., Sato T., Yura T. Synthesis and assembly of the membrane proteins in E. coli. Cell. 1977 Jul;11(3):551–559. doi: 10.1016/0092-8674(77)90073-3. [DOI] [PubMed] [Google Scholar]
  16. Jaskula J. C., Letain T. E., Roof S. K., Skare J. T., Postle K. Role of the TonB amino terminus in energy transduction between membranes. J Bacteriol. 1994 Apr;176(8):2326–2338. doi: 10.1128/jb.176.8.2326-2338.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kadner R. J., Heller K. J. Mutual inhibition of cobalamin and siderophore uptake systems suggests their competition for TonB function. J Bacteriol. 1995 Sep;177(17):4829–4835. doi: 10.1128/jb.177.17.4829-4835.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kadner R. J. Repression of synthesis of the vitamin B12 receptor in Escherichia coli. J Bacteriol. 1978 Dec;136(3):1050–1057. doi: 10.1128/jb.136.3.1050-1057.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kadner R. J. Vitamin B12 transport in Escherichia coli: energy coupling between membranes. Mol Microbiol. 1990 Dec;4(12):2027–2033. doi: 10.1111/j.1365-2958.1990.tb00562.x. [DOI] [PubMed] [Google Scholar]
  20. Karlsson M., Hannavy K., Higgins C. F. A sequence-specific function for the N-terminal signal-like sequence of the TonB protein. Mol Microbiol. 1993 Apr;8(2):379–388. doi: 10.1111/j.1365-2958.1993.tb01581.x. [DOI] [PubMed] [Google Scholar]
  21. Kiino D. R., Rothman-Denes L. B. Genetic analysis of bacteriophage N4 adsorption. J Bacteriol. 1989 Sep;171(9):4595–4602. doi: 10.1128/jb.171.9.4595-4602.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Killmann H., Braun V. An aspartate deletion mutation defines a binding site of the multifunctional FhuA outer membrane receptor of Escherichia coli K-12. J Bacteriol. 1992 Jun;174(11):3479–3486. doi: 10.1128/jb.174.11.3479-3486.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Killmann H., Videnov G., Jung G., Schwarz H., Braun V. Identification of receptor binding sites by competitive peptide mapping: phages T1, T5, and phi 80 and colicin M bind to the gating loop of FhuA. J Bacteriol. 1995 Feb;177(3):694–698. doi: 10.1128/jb.177.3.694-698.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kohara Y., Akiyama K., Isono K. The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library. Cell. 1987 Jul 31;50(3):495–508. doi: 10.1016/0092-8674(87)90503-4. [DOI] [PubMed] [Google Scholar]
  25. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  26. Levengood S. K., Beyer W. F., Jr, Webster R. E. TolA: a membrane protein involved in colicin uptake contains an extended helical region. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):5939–5943. doi: 10.1073/pnas.88.14.5939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Likhacheva N. A., Khrenova E. A., Sineokii S. P. Geneticheskii kontrol' rezistentnosti Escherichia coli K12 k fagu C1. Mol Gen Mikrobiol Virusol. 1990 Dec;(12):12–15. [PubMed] [Google Scholar]
  28. Lundrigan M. D., De Veaux L. C., Mann B. J., Kadner R. J. Separate regulatory systems for the repression of metE and btuB by vitamin B12 in Escherichia coli. Mol Gen Genet. 1987 Mar;206(3):401–407. doi: 10.1007/BF00428878. [DOI] [PubMed] [Google Scholar]
  29. Morona R., Henning U. New locus (ttr) in Escherichia coli K-12 affecting sensitivity to bacteriophage T2 and growth on oleate as the sole carbon source. J Bacteriol. 1986 Nov;168(2):534–540. doi: 10.1128/jb.168.2.534-540.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Postle K. TonB protein and energy transduction between membranes. J Bioenerg Biomembr. 1993 Dec;25(6):591–601. doi: 10.1007/BF00770246. [DOI] [PubMed] [Google Scholar]
  31. Reanney D. C., Ackermann H. W. Comparative biology and evolution of bacteriophages. Adv Virus Res. 1982;27:205–280. doi: 10.1016/s0065-3527(08)60436-4. [DOI] [PubMed] [Google Scholar]
  32. Roa M. Interaction of bacteriophage K10 with its receptor, the lamB protein of Escherichia coli. J Bacteriol. 1979 Nov;140(2):680–686. doi: 10.1128/jb.140.2.680-686.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Saigo K. Isolation of high-density mutants and identification of nonessential structural proteins in bacteriophage T5; dispensability of L-shaped tail fibers and a secondary major head protein. Virology. 1978 Apr;85(2):422–433. doi: 10.1016/0042-6822(78)90449-x. [DOI] [PubMed] [Google Scholar]
  34. Sancar A., Hack A. M., Rupp W. D. Simple method for identification of plasmid-coded proteins. J Bacteriol. 1979 Jan;137(1):692–693. doi: 10.1128/jb.137.1.692-693.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. 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]
  36. Shao Z., Lin R. T., Newman E. B. Sequencing and characterization of the sdaC gene and identification of the sdaCB operon in Escherichia coli K12. Eur J Biochem. 1994 Jun 15;222(3):901–907. doi: 10.1111/j.1432-1033.1994.tb18938.x. [DOI] [PubMed] [Google Scholar]
  37. Skare J. T., Ahmer B. M., Seachord C. L., Darveau R. P., Postle K. Energy transduction between membranes. TonB, a cytoplasmic membrane protein, can be chemically cross-linked in vivo to the outer membrane receptor FepA. J Biol Chem. 1993 Aug 5;268(22):16302–16308. [PubMed] [Google Scholar]
  38. Sofia H. J., Burland V., Daniels D. L., Plunkett G., 3rd, Blattner F. R. Analysis of the Escherichia coli genome. V. DNA sequence of the region from 76.0 to 81.5 minutes. Nucleic Acids Res. 1994 Jul 11;22(13):2576–2586. doi: 10.1093/nar/22.13.2576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Traub I., Gaisser S., Braun V. Activity domains of the TonB protein. Mol Microbiol. 1993 Apr;8(2):409–423. doi: 10.1111/j.1365-2958.1993.tb01584.x. [DOI] [PubMed] [Google Scholar]
  40. Vianney A., Lewin T. M., Beyer W. F., Jr, Lazzaroni J. C., Portalier R., Webster R. E. Membrane topology and mutational analysis of the TolQ protein of Escherichia coli required for the uptake of macromolecules and cell envelope integrity. J Bacteriol. 1994 Feb;176(3):822–829. doi: 10.1128/jb.176.3.822-829.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. 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]
  42. Webster R. E. The tol gene products and the import of macromolecules into Escherichia coli. Mol Microbiol. 1991 May;5(5):1005–1011. doi: 10.1111/j.1365-2958.1991.tb01873.x. [DOI] [PubMed] [Google Scholar]
  43. Werts C., Michel V., Hofnung M., Charbit A. Adsorption of bacteriophage lambda on the LamB protein of Escherichia coli K-12: point mutations in gene J of lambda responsible for extended host range. J Bacteriol. 1994 Feb;176(4):941–947. doi: 10.1128/jb.176.4.941-947.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Wilson G. G., Young K. Y., Edlin G. J., Konigsberg W. High-frequency generalised transduction by bacteriophage T4. Nature. 1979 Jul 5;280(5717):80–82. doi: 10.1038/280080a0. [DOI] [PubMed] [Google Scholar]
  45. Winans S. C., Elledge S. J., Krueger J. H., Walker G. C. Site-directed insertion and deletion mutagenesis with cloned fragments in Escherichia coli. J Bacteriol. 1985 Mar;161(3):1219–1221. doi: 10.1128/jb.161.3.1219-1221.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Yankovsky N. K., Fonstein MYu, Lashina SYu, Bukanov N. O., Yakubovich N. V., Ermakova L. M., Rebentish B. A., Janulaitis A. A., Debabov V. G. Phasmids as effective and simple tools for construction and analysis of gene libraries. Gene. 1989 Sep 30;81(2):203–210. doi: 10.1016/0378-1119(89)90180-7. [DOI] [PubMed] [Google Scholar]
  47. Zaror I., Gómez I., Castillo G., Yudelevich A., Venegas A. Molecular cloning and expression in E. coli of a Salmonella typhi porin gene. FEBS Lett. 1988 Feb 29;229(1):77–81. doi: 10.1016/0014-5793(88)80801-9. [DOI] [PubMed] [Google Scholar]

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