Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1979 Nov;140(2):415–423. doi: 10.1128/jb.140.2.415-423.1979

Production and excretion of cloacin DF13 by Escherichia coli harboring plasmid CloDF13.

G J Van Tiel-Menkvled, A Rezee, F K De Graaf
PMCID: PMC216665  PMID: 227839

Abstract

The production and the mechanism of excretion of cloacin DF13 were investigated in noninduced and mitomycin C-induced cell cultures. A mitomycin C concentration was selected which did not cause lysis of cloacinogenic cells, but at the same time induced a maximal production of cloacin DF13. Native cloacin DF13, possessing killing activity, was first released into the cytoplasm. Shortly thereafter, the bacteriocin was transported through the cytoplasmic membrane and accumulated in the periplasm. Finally, cloacin DF13 was excreted into the culture medium. A small amount of cloacin DF13 remained associated with the cell surface. Producing cells did not become permeable for the cytoplasmic enzyme beta-galactosidase. Apparently the cloacin DF13 leaves the producing cells by an excretion process which is not similar to the mechanism proposed for bacterial secretory proteins. The processes of excretion by producing cells and of uptake by susceptible cells were also not identical because mutant cloacin DF13, which was not transported through the outer membrane into susceptible cells, was excreted like the wild-type cloacin DF13. The composition of the culture medium greatly affected production of cloacin DF13. The presence of sugars known to cause catabolite repression not only inhibited the production but also strongly reduced the excretion of cloacin DF13 into the culture medium.

Full text

PDF
418

Selected References

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

  1. Andreoli P. M., Nijkamp H. J. Mutants of the Clo DF13 plasmid in Escherichia coli with a decreased bacteriocinogenic activity. Mol Gen Genet. 1976 Mar 22;144(2):159–170. doi: 10.1007/BF02428104. [DOI] [PubMed] [Google Scholar]
  2. Andreoli P. M., Overbeeke N., Veltkamp E., van Embden J. D., Nijkamp H. J. Genetic map of the bacteriocinogenic plasmid CLO DF13 derived by insertion of the transposon Tn901. Mol Gen Genet. 1978 Mar 20;160(1):1–11. doi: 10.1007/BF00275113. [DOI] [PubMed] [Google Scholar]
  3. Bassford P., Beckwith J. Escherichia coli mutants accumulating the precursor of a secreted protein in the cytoplasm. Nature. 1979 Feb 15;277(5697):538–541. doi: 10.1038/277538a0. [DOI] [PubMed] [Google Scholar]
  4. Collier R. J. Diphtheria toxin: mode of action and structure. Bacteriol Rev. 1975 Mar;39(1):54–85. doi: 10.1128/br.39.1.54-85.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Curtis N. A., Richmond M. H., Sykes R. B. "Periplasmic" location of a -lactamase specified either by a plasmid or a chromosomal gene in Escherichia coli. J Bacteriol. 1972 Dec;112(3):1433–1434. doi: 10.1128/jb.112.3.1433-1434.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. De Graaf F. K., Klaasen-Boor P. Purification and characterization of a complex between cloacin and its immunity protein isolated from Enterobacter cloacae (Clo DF13). Dissociation and reconstitution of the complex. Eur J Biochem. 1977 Feb 15;73(1):107–114. doi: 10.1111/j.1432-1033.1977.tb11296.x. [DOI] [PubMed] [Google Scholar]
  7. De Graaf F. K., Planta R. J., Stouthamer A. H. Effect of a bacteriocin produced by Enterobacter cloacae on protein biosynthesis. Biochim Biophys Acta. 1971 Jun 17;240(1):123–136. [PubMed] [Google Scholar]
  8. Dessein A., Schwartz M., Ullmann A. Catabolite repression in Escherichia coli mutants lacking cyclic AMP. Mol Gen Genet. 1978 Jun 1;162(1):83–87. doi: 10.1007/BF00333853. [DOI] [PubMed] [Google Scholar]
  9. Durkacz B. W., Kennedy C. K., Sherratt D. J. Plasmid replication and the induced synthesis of colicins E1 and E2 in Escherichia coli. J Bacteriol. 1974 Mar;117(3):940–946. doi: 10.1128/jb.117.3.940-946.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Emr S. D., Schwartz M., Silhavy T. J. Mutations altering the cellular localization of the phage lambda receptor, an Escherichia coli outer membrane protein. Proc Natl Acad Sci U S A. 1978 Dec;75(12):5802–5806. doi: 10.1073/pnas.75.12.5802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gaastra W., Oudega B., de Graaf F. K. The use of mutants in the study of structure-function relationships in cloacin DF13. Biochim Biophys Acta. 1978 May 3;540(2):301–312. doi: 10.1016/0304-4165(78)90143-5. [DOI] [PubMed] [Google Scholar]
  12. Hardy K. G. Colicinogeny and related phenomena. Bacteriol Rev. 1975 Dec;39(4):464–515. doi: 10.1128/br.39.4.464-515.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Herschman H. R., Helinski D. R. Comparative study of the events associated with colicin induction. J Bacteriol. 1967 Sep;94(3):691–699. doi: 10.1128/jb.94.3.691-699.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Inouye H., Beckwith J. Synthesis and processing of an Escherichia coli alkaline phosphatase precursor in vitro. Proc Natl Acad Sci U S A. 1977 Apr;74(4):1440–1444. doi: 10.1073/pnas.74.4.1440. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Isaacson R. E., Konisky J. Studies of the regulation of colicin Ib synthesis. II. The synthesis of col Ib-P9 specific RNA in vivo. Mol Gen Genet. 1974;132(3):223–232. doi: 10.1007/BF00269395. [DOI] [PubMed] [Google Scholar]
  16. Jakes K. S., Model P. Mechanism of export of colicin E1 and colicin E3. J Bacteriol. 1979 Jun;138(3):770–778. doi: 10.1128/jb.138.3.770-778.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kool A. J., Nijkamp H. J. Isolation and characterization of a copy mutant of the bacteriocinogenic plasmid Clo DF13. J Bacteriol. 1974 Nov;120(2):569–578. doi: 10.1128/jb.120.2.569-578.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lugtenberg B., Peters R., Bernheimer H., Berendsen W. Influence of cultural conditions and mutations on the composition of the outer membrane proteins of Escherichia coli. Mol Gen Genet. 1976 Sep 23;147(3):251–262. doi: 10.1007/BF00582876. [DOI] [PubMed] [Google Scholar]
  19. Mock M., Schwartz M. Mechanism of colicin E3 production in strains harboring wild-type or mutant plasmids. J Bacteriol. 1978 Nov;136(2):700–707. doi: 10.1128/jb.136.2.700-707.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mooi F. R., de Graaf F. K., van Embden J. D. Cloning, mapping and expression of the genetic determinant that encodes for the K88ab antigen. Nucleic Acids Res. 1979 Mar;6(3):849–865. doi: 10.1093/nar/6.3.849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nakazawa A., Suzuki N., Tamada T. Requirements of glucose and incubation under static conditions for optimal colicin E1 induction. Antimicrob Agents Chemother. 1977 Feb;11(2):219–224. doi: 10.1128/aac.11.2.219. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Nakazawa A., Tamada T. Stimulation of colicin E 1 synthesis by cyclic 3', 5'-adenosine monophosphate in mitomycin C-induced Escherichia coli. Biochem Biophys Res Commun. 1972 Jan 31;46(2):1004–1010. doi: 10.1016/s0006-291x(72)80241-9. [DOI] [PubMed] [Google Scholar]
  23. Neu H. C., Heppel L. A. The release of enzymes from Escherichia coli by osmotic shock and during the formation of spheroplasts. J Biol Chem. 1965 Sep;240(9):3685–3692. [PubMed] [Google Scholar]
  24. O'Callaghan C. H., Morris A., Kirby S. M., Shingler A. H. Novel method for detection of beta-lactamases by using a chromogenic cephalosporin substrate. Antimicrob Agents Chemother. 1972 Apr;1(4):283–288. doi: 10.1128/aac.1.4.283. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Oudega B., Klaasen-Boor P., De Graaf F. K. Mode of action of the cloacin DF13-immunity protein. Biochim Biophys Acta. 1975 May 5;392(1):184–195. [PubMed] [Google Scholar]
  26. Oudega B., Klaasen-Boor P., Sneeuwloper G., De Graaf F. K. Interaction of the complex between cloacin and its immunity protein and of cloacin with the outer and cytoplasmic membranes of sensitive cells. Eur J Biochem. 1977 Sep;78(2):445–453. doi: 10.1111/j.1432-1033.1977.tb11757.x. [DOI] [PubMed] [Google Scholar]
  27. Oudega B., de Graaf F. K. Enzymatic properties of cloacin DF13 and kinetics of ribosome inactivation. Biochim Biophys Acta. 1976 Mar 17;425(3):296–304. doi: 10.1016/0005-2787(76)90256-2. [DOI] [PubMed] [Google Scholar]
  28. Pastan I., Adhya S. Cyclic adenosine 5'-monophosphate in Escherichia coli. Bacteriol Rev. 1976 Sep;40(3):527–551. doi: 10.1128/br.40.3.527-551.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Priest F. G. Extracellular enzyme synthesis in the genus Bacillus. Bacteriol Rev. 1977 Sep;41(3):711–753. doi: 10.1128/br.41.3.711-753.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Randall L. L., Hardy S. J., Josefsson L. G. Precursors of three exported proteins in Escherichia coli. Proc Natl Acad Sci U S A. 1978 Mar;75(3):1209–1212. doi: 10.1073/pnas.75.3.1209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Randall L. L., Hardy S. J. Synthesis of exported proteins by membrane-bound polysomes from Escherichia coli. Eur J Biochem. 1977 May 2;75(1):43–53. doi: 10.1111/j.1432-1033.1977.tb11502.x. [DOI] [PubMed] [Google Scholar]
  32. Sekizawa J., Inouye S., Halegoua S., Inouye M. Precursors of major outer membrane proteins of Escherichia coli. Biochem Biophys Res Commun. 1977 Aug 8;77(3):1126–1133. doi: 10.1016/s0006-291x(77)80095-8. [DOI] [PubMed] [Google Scholar]
  33. Stouthamer A. H., Tieze G. A. Bacteriocin production by members of the genus Klebsiella. Antonie Van Leeuwenhoek. 1966;32(2):171–182. doi: 10.1007/BF02097457. [DOI] [PubMed] [Google Scholar]
  34. Vasil M. L., Kabat D., Iglewski B. H. Structure-activity relationships of an exotoxin of Pseudomonas aeruginosa. Infect Immun. 1977 Apr;16(1):353–361. doi: 10.1128/iai.16.1.353-361.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Wanner B. L., Kodaira R., Neidhardt F. C. Regulation of lac operon expression: reappraisal of the theory of catabolite repression. J Bacteriol. 1978 Dec;136(3):947–954. doi: 10.1128/jb.136.3.947-954.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Witholt B., Boekhout M., Brock M., Kingma J., Heerikhuizen H. V., Leij L. D. An efficient and reproducible procedure for the formation of spheroplasts from variously grown Escherichia coli. Anal Biochem. 1976 Jul;74(1):160–170. doi: 10.1016/0003-2697(76)90320-1. [DOI] [PubMed] [Google Scholar]
  37. Witholt B., Heerikhuizen H. V., De Leij L. How does lysozyme penetrate through the bacterial outer membrane? Biochim Biophys Acta. 1976 Sep 7;443(3):534–544. doi: 10.1016/0005-2736(76)90471-5. [DOI] [PubMed] [Google Scholar]
  38. Witkin E. M. Ultraviolet mutagenesis and inducible DNA repair in Escherichia coli. Bacteriol Rev. 1976 Dec;40(4):869–907. doi: 10.1128/br.40.4.869-907.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. de Graaf F. K., Niekus H. G., Klootwijk J. Inactivation of bacterial ribosomes in vivo and in vitro by cloacin DF13. FEBS Lett. 1973 Sep 1;35(1):161–165. doi: 10.1016/0014-5793(73)80601-5. [DOI] [PubMed] [Google Scholar]
  40. de Graaf F. K., Spanjaerdt Speckman E. A., Stouthamer A. H. Mode of action of a bacteriocin produced by Enterobacter cloacae DF13. Antonie Van Leeuwenhoek. 1969;35(3):287–306. doi: 10.1007/BF02219150. [DOI] [PubMed] [Google Scholar]
  41. de Graaf F. K., Stukart M. J., Boogerd F. C., Metselaar K. Limited proteolysis of cloacin DF13 and characterization of the cleavage products. Biochemistry. 1978 Mar 21;17(6):1137–1142. doi: 10.1021/bi00599a031. [DOI] [PubMed] [Google Scholar]
  42. de Graaf F. K., Tieze G. A., Wendelaar Bonga S., Stouthamer A. H. Purification and genetic determination of bacteriocin production in Enterobacter cloacae. J Bacteriol. 1968 Feb;95(2):631–640. doi: 10.1128/jb.95.2.631-640.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. van Embden J. D. Translocation of an ampicillin resistance determinant within an R-factor aggregate in Salmonella panama. Antonie Van Leeuwenhoek. 1978;44(2):203–218. doi: 10.1007/BF00643223. [DOI] [PubMed] [Google Scholar]

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

RESOURCES