Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1991 Jan;59(1):357–364. doi: 10.1128/iai.59.1.357-364.1991

Polymorphism in the aerobactin-cloacin DF13 receptor genes from an enteroinvasive strain of Escherichia coli and pColV-K30 is associated only with a decrease in cloacin susceptibility.

C L Marolda 1, M A Valvano 1, J H Crosa 1
PMCID: PMC257749  PMID: 1987050

Abstract

We have cloned chromosomal genes mediating the aerobactin iron transport system from the enteroinvasive strain Escherichia coli 978-77. The physical map of the region spanning the siderophore biosynthesis genes and the upstream portion of the receptor gene in strain 978-77-derived clones was identical to the corresponding regions in pColV-K30, while the downstream portion was different. Recombinant plasmids derived from strain 978-77 encoded a 76-kDa outer membrane protein, in contrast to the 74-kDa polypeptide encoded by similar clones derived from pColV-K30. No differences were found in the uptake of ferric aerobactin mediated by either the 76-kDa- or the 74-kDa-encoding plasmids. In contrast, cells containing the 76-kDa-encoding plasmids showed a 16-fold decrease in susceptibility to cloacin compared with cells harboring the 74-kDa-encoding plasmids. Two classes of chimeric aerobactin receptor genes were constructed by exchanging sequences corresponding to the downstream portion from the aerobactin receptor gene of both systems. The pColV-K30-978-77 chimeric gene encoded a 76-kDa outer membrane protein which mediated a low level of cloacin susceptibility, whereas the 978-77-pColV-K30 type encoded a protein of 74 kDa determining a level of cloacin susceptibility identical to that mediated by pColV-K30.

Full text

PDF
357

Images in this article

360Image
on p.360

Selected References

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

  1. Actis L. A., Potter S. A., Crosa J. H. Iron-regulated outer membrane protein OM2 of Vibrio anguillarum is encoded by virulence plasmid pJM1. J Bacteriol. 1985 Feb;161(2):736–742. doi: 10.1128/jb.161.2.736-742.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bindereif A., Neilands J. B. Cloning of the aerobactin-mediated iron assimilation system of plasmid ColV. J Bacteriol. 1983 Feb;153(2):1111–1113. doi: 10.1128/jb.153.2.1111-1113.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bolivar F., Rodriguez R. L., Greene P. J., Betlach M. C., Heyneker H. L., Boyer H. W., Crosa J. H., Falkow S. Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene. 1977;2(2):95–113. [PubMed] [Google Scholar]
  4. Boyer H. W., Roulland-Dussoix D. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J Mol Biol. 1969 May 14;41(3):459–472. doi: 10.1016/0022-2836(69)90288-5. [DOI] [PubMed] [Google Scholar]
  5. Carbonetti N. H., Williams P. H. A cluster of five genes specifying the aerobactin iron uptake system of plasmid ColV-K30. Infect Immun. 1984 Oct;46(1):7–12. doi: 10.1128/iai.46.1.7-12.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Crosa J. H. The relationship of plasmid-mediated iron transport and bacterial virulence. Annu Rev Microbiol. 1984;38:69–89. doi: 10.1146/annurev.mi.38.100184.000441. [DOI] [PubMed] [Google Scholar]
  7. Crosa L. M., Wolf M. K., Actis L. A., Sanders-Loehr J., Crosa J. H. New aerobactin-mediated iron uptake system in a septicemia-causing strain of Enterobacter cloacae. J Bacteriol. 1988 Dec;170(12):5539–5544. doi: 10.1128/jb.170.12.5539-5544.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Derbyshire P., Baldwin T., Stevenson P., Griffiths E., Roberts M., Williams P., Hale T. L., Formal S. B. Expression in Escherichia coli K-12 of the 76,000-dalton iron-regulated outer membrane protein of Shigella flexneri confers sensitivity to cloacin DF13 in the absence of Shigella O antigen. Infect Immun. 1989 Sep;57(9):2794–2798. doi: 10.1128/iai.57.9.2794-2798.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fleming T. P., Nahlik M. S., Neilands J. B., McIntosh M. A. Physical and genetic characterization of cloned enterobactin genomic sequences from Escherichia coli K-12. Gene. 1985;34(1):47–54. doi: 10.1016/0378-1119(85)90293-8. [DOI] [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. Gibson F., Magrath D. I. The isolation and characterization of a hydroxamic acid (aerobactin) formed by Aerobacter aerogenes 62-I. Biochim Biophys Acta. 1969 Nov 18;192(2):175–184. doi: 10.1016/0304-4165(69)90353-5. [DOI] [PubMed] [Google Scholar]
  13. Griffiths E., Stevenson P., Hale T. L., Formal S. B. Synthesis of aerobactin and a 76,000-dalton iron-regulated outer membrane protein by Escherichia coli K-12-Shigella flexneri hybrids and by enteroinvasive strains of Escherichia coli. Infect Immun. 1985 Jul;49(1):67–71. doi: 10.1128/iai.49.1.67-71.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hull R. A., Gill R. E., Hsu P., Minshew B. H., Falkow S. Construction and expression of recombinant plasmids encoding type 1 or D-mannose-resistant pili from a urinary tract infection Escherichia coli isolate. Infect Immun. 1981 Sep;33(3):933–938. doi: 10.1128/iai.33.3.933-938.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Knauf V. C., Nester E. W. Wide host range cloning vectors: a cosmid clone bank of an Agrobacterium Ti plasmid. Plasmid. 1982 Jul;8(1):45–54. doi: 10.1016/0147-619x(82)90040-3. [DOI] [PubMed] [Google Scholar]
  16. Konopka K., Bindereif A., Neilands J. B. Aerobactin-mediated utilization of transferrin iron. Biochemistry. 1982 Dec 7;21(25):6503–6508. doi: 10.1021/bi00268a028. [DOI] [PubMed] [Google Scholar]
  17. Krone W. J., Luirink J., Koningstein G., Oudega B., de Graaf F. K. Subcloning of the cloacin DF13/aerobactin receptor protein and identification of a pColV-K30-determined polypeptide involved in ferric-aerobactin uptake. J Bacteriol. 1983 Nov;156(2):945–948. doi: 10.1128/jb.156.2.945-948.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Krone W. J., de Vries P., Koningstein G., de Jonge A. J., de Graaf F. K., Oudega B. Uptake of cloacin DF13 by susceptible cells: removal of immunity protein and fragmentation of cloacin molecules. J Bacteriol. 1986 Apr;166(1):260–268. doi: 10.1128/jb.166.1.260-268.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lawlor K. M., Payne S. M. Aerobactin genes in Shigella spp. J Bacteriol. 1984 Oct;160(1):266–272. doi: 10.1128/jb.160.1.266-272.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Marolda C. L., Valvano M. A., Lawlor K. M., Payne S. M., Crosa J. H. Flanking and internal regions of chromosomal genes mediating aerobactin iron uptake systems in enteroinvasive Escherichia coli and Shigella flexneri. J Gen Microbiol. 1987 Aug;133(8):2269–2278. doi: 10.1099/00221287-133-8-2269. [DOI] [PubMed] [Google Scholar]
  21. Nassif X., Sansonetti P. J. Correlation of the virulence of Klebsiella pneumoniae K1 and K2 with the presence of a plasmid encoding aerobactin. Infect Immun. 1986 Dec;54(3):603–608. doi: 10.1128/iai.54.3.603-608.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Payne S. M., Niesel D. W., Peixotto S. S., Lawlor K. M. Expression of hydroxamate and phenolate siderophores by Shigella flexneri. J Bacteriol. 1983 Sep;155(3):949–955. doi: 10.1128/jb.155.3.949-955.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Payne S. M. Synthesis and utilization of siderophores by Shigella flexneri. J Bacteriol. 1980 Sep;143(3):1420–1424. doi: 10.1128/jb.143.3.1420-1424.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Roberts M., Wooldridge K. G., Gavine H., Kuswandi S. I., Williams P. H. Inhibition of biological activities of the aerobactin receptor protein in rough strains of Escherichia coli by polyclonal antiserum raised against native protein. J Gen Microbiol. 1989 Sep;135(9):2387–2398. doi: 10.1099/00221287-135-9-2387. [DOI] [PubMed] [Google Scholar]
  26. Valvano M. A., Crosa J. H. Aerobactin iron transport genes commonly encoded by certain ColV plasmids occur in the chromosome of a human invasive strain of Escherichia coli K1. Infect Immun. 1984 Oct;46(1):159–167. doi: 10.1128/iai.46.1.159-167.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Valvano M. A., Crosa J. H. Molecular cloning, expression, and regulation in Escherichia coli K-12 of a chromosome-mediated aerobactin iron transport system from a human invasive isolate of E. coli K1. J Bacteriol. 1988 Dec;170(12):5529–5538. doi: 10.1128/jb.170.12.5529-5538.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Valvano M. A., Silver R. P., Crosa J. H. Occurrence of chromosome- or plasmid-mediated aerobactin iron transport systems and hemolysin production among clonal groups of human invasive strains of Escherichia coli K1. Infect Immun. 1986 Apr;52(1):192–199. doi: 10.1128/iai.52.1.192-199.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Van Tiel-Menkveld G. J., Mentjox-Vervuurt J. M., Oudega B., de Graaf F. K. Siderophore production by Enterobacter cloacae and a common receptor protein for the uptake of aerobactin and cloacin DF13. J Bacteriol. 1982 May;150(2):490–497. doi: 10.1128/jb.150.2.490-497.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Van Tiel-Menkvled G. J., Rezee A., De Graaf F. K. Production and excretion of cloacin DF13 by Escherichia coli harboring plasmid CloDF13. J Bacteriol. 1979 Nov;140(2):415–423. doi: 10.1128/jb.140.2.415-423.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wagegg W., Braun V. Ferric citrate transport in Escherichia coli requires outer membrane receptor protein fecA. J Bacteriol. 1981 Jan;145(1):156–163. doi: 10.1128/jb.145.1.156-163.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Warner P. J., Williams P. H., Bindereif A., Neilands J. B. ColV plasmid-specific aerobactin synthesis by invasive strains of Escherichia coli. Infect Immun. 1981 Aug;33(2):540–545. doi: 10.1128/iai.33.2.540-545.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Williams P. H. Novel iron uptake system specified by ColV plasmids: an important component in the virulence of invasive strains of Escherichia coli. Infect Immun. 1979 Dec;26(3):925–932. doi: 10.1128/iai.26.3.925-932.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES