Skip to main content
NCBI home page
The EMBO Journal logoLink to The EMBO Journal
. 1992 Dec;11(12):4359–4367. doi: 10.1002/j.1460-2075.1992.tb05535.x

Hemin uptake system of Yersinia enterocolitica: similarities with other TonB-dependent systems in gram-negative bacteria.

I Stojiljkovic 1, K Hantke 1
PMCID: PMC557009  PMID: 1425573

Abstract

The hemin receptor HemR of Yersinia enterocolitica was identified as a 78 kDa iron regulated outer membrane protein. Cells devoid of the HemR receptor as well as cells mutated in the tonB gene were unable to take up hemin as an iron source. The hemin uptake operon from Y. enterocolitica was cloned in Escherichia coli K12 and was shown to encode four proteins: HemP (6.5 kDa), HemR (78 kDa), HemS (42 kDa) and HemT (27 kDa). When expressed in E.coli hemA aroB, a plasmid carrying genes for HemP and HemR allowed growth on hemin as a porphyrin source. Presence of genes for HemP, HemR and HemS was necessary to allow E.coli hemA aroB cells to use hemin as an iron source. The nucleotide sequence of the hemR gene and its promoter region was determined and the amino acid sequence of the HemR receptor deduced. HemR has a signal peptide of 28 amino acids and a typical TonB box at its amino-terminus. Upstream of the first gene in the operon (hemP), a well conserved Fur box was found which is in accordance with the iron-regulated expression of HemR.

Full text

PDF
4359

Images in this article

4360Image
on p.4360
4361Image
on p.4361
4363Image
on p.4363

Selected References

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

  1. Angerer A., Klupp B., Braun V. Iron transport systems of Serratia marcescens. J Bacteriol. 1992 Feb;174(4):1378–1387. doi: 10.1128/jb.174.4.1378-1387.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BELJANSKI M. Sur la formation d'enzymes respiratoires chez un mutant d'Escherichia coli streptomycino-résistant et auxotrophe pour l'hémine. Ann Inst Pasteur (Paris) 1957 Mar;92(3):396–412. [PubMed] [Google Scholar]
  3. BURROWS T. W., JACKSON S. The virulence-enhancing effect of iron on nonpigmented mutants of virulent strains of Pasteurella pestis. Br J Exp Pathol. 1956 Dec;37(6):577–583. [PMC free article] [PubMed] [Google Scholar]
  4. Braun A., Ding R., Seidel C., Fies T., Kurtz A., Schärer K. Pharmacokinetics of recombinant human erythropoietin applied subcutaneously to children with chronic renal failure. Pediatr Nephrol. 1993 Feb;7(1):61–64. doi: 10.1007/BF00861571. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Brickman E., Beckwith J. Analysis of the regulation of Escherichia coli alkaline phosphatase synthesis using deletions and phi80 transducing phages. J Mol Biol. 1975 Aug 5;96(2):307–316. doi: 10.1016/0022-2836(75)90350-2. [DOI] [PubMed] [Google Scholar]
  7. Brubaker R. R. Factors promoting acute and chronic diseases caused by yersiniae. Clin Microbiol Rev. 1991 Jul;4(3):309–324. doi: 10.1128/cmr.4.3.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Carniel E., Antoine J. C., Guiyoule A., Guiso N., Mollaret H. H. Purification, location, and immunological characterization of the iron-regulated high-molecular-weight proteins of the highly pathogenic yersiniae. Infect Immun. 1989 Feb;57(2):540–545. doi: 10.1128/iai.57.2.540-545.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cornelis G. R., Biot T., Lambert de Rouvroit C., Michiels T., Mulder B., Sluiters C., Sory M. P., Van Bouchaute M., Vanooteghem J. C. The Yersinia yop regulon. Mol Microbiol. 1989 Oct;3(10):1455–1459. doi: 10.1111/j.1365-2958.1989.tb00129.x. [DOI] [PubMed] [Google Scholar]
  10. Daskaleros P. A., Stoebner J. A., Payne S. M. Iron uptake in Plesiomonas shigelloides: cloning of the genes for the heme-iron uptake system. Infect Immun. 1991 Aug;59(8):2706–2711. doi: 10.1128/iai.59.8.2706-2711.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dyer D. W., West E. P., Sparling P. F. Effects of serum carrier proteins on the growth of pathogenic neisseriae with heme-bound iron. Infect Immun. 1987 Sep;55(9):2171–2175. doi: 10.1128/iai.55.9.2171-2175.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Eaton J. W., Brandt P., Mahoney J. R., Lee J. T., Jr Haptoglobin: a natural bacteriostat. Science. 1982 Feb 5;215(4533):691–693. doi: 10.1126/science.7036344. [DOI] [PubMed] [Google Scholar]
  13. Fortin Y., Phoenix P., Drapeau G. R. Mutations conferring resistance to azide in Escherichia coli occur primarily in the secA gene. J Bacteriol. 1990 Nov;172(11):6607–6610. doi: 10.1128/jb.172.11.6607-6610.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. GIBBONS R. J., MACDONALD J. B. Hemin and vitamin K compounds as required factors for the cultivation of certain strains of Bacteroides melaninogenicus. J Bacteriol. 1960 Aug;80:164–170. doi: 10.1128/jb.80.2.164-170.1960. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Haddock B. A., Schairer H. U. Electron-transport chains of Escherichia coli. Reconstitution of respiration in a 5-aminolaevulinic acid-requiring mutant. Eur J Biochem. 1973 May;35(1):34–45. doi: 10.1111/j.1432-1033.1973.tb02806.x. [DOI] [PubMed] [Google Scholar]
  16. Hanson M. S., Pelzel S. E., Latimer J., Muller-Eberhard U., Hansen E. J. Identification of a genetic locus of Haemophilus influenzae type b necessary for the binding and utilization of heme bound to human hemopexin. Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1973–1977. doi: 10.1073/pnas.89.5.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hantke K. Regulation of ferric iron transport in Escherichia coli K12: isolation of a constitutive mutant. Mol Gen Genet. 1981;182(2):288–292. doi: 10.1007/BF00269672. [DOI] [PubMed] [Google Scholar]
  18. Hartmann A., Braun V. Iron uptake and iron limited growth of Escherichia coli K-12. Arch Microbiol. 1981 Dec 2;130(5):353–356. doi: 10.1007/BF00414599. [DOI] [PubMed] [Google Scholar]
  19. Heller K., Kadner R. J. Nucleotide sequence of the gene for the vitamin B12 receptor protein in the outer membrane of Escherichia coli. J Bacteriol. 1985 Mar;161(3):904–908. doi: 10.1128/jb.161.3.904-908.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Helms S. D., Oliver J. D., Travis J. C. Role of heme compounds and haptoglobin in Vibrio vulnificus pathogenicity. Infect Immun. 1984 Aug;45(2):345–349. doi: 10.1128/iai.45.2.345-349.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hu P. C., Yang G. C., Brubaker R. R. Specificity, induction, and absorption of pesticin. J Bacteriol. 1972 Oct;112(1):212–219. doi: 10.1128/jb.112.1.212-219.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kanner B. I., Gutnick D. L. Use of neomycin in the isolation of mutants blocked in energy conservation in Escherichia coli. J Bacteriol. 1972 Jul;111(1):287–289. doi: 10.1128/jb.111.1.287-289.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kolter R., Inuzuka M., Helinski D. R. Trans-complementation-dependent replication of a low molecular weight origin fragment from plasmid R6K. Cell. 1978 Dec;15(4):1199–1208. doi: 10.1016/0092-8674(78)90046-6. [DOI] [PubMed] [Google Scholar]
  24. Lee B. C. Iron sources for Haemophilus ducreyi. J Med Microbiol. 1991 Jun;34(6):317–322. doi: 10.1099/00222615-34-6-317. [DOI] [PubMed] [Google Scholar]
  25. Lewis L. A., Li K. B., Gousse A., Pereira F., Pacheco N., Pierre S., Kodaman P., Lawson S. Genetic and molecular analysis of spontaneous respiratory deficient (res-) mutants of Escherichia coli K-12. Microbiol Immunol. 1991;35(4):289–301. doi: 10.1111/j.1348-0421.1991.tb01558.x. [DOI] [PubMed] [Google Scholar]
  26. Matzanke B. F., Müller G. I., Bill E., Trautwein A. X. Iron metabolism of Escherichia coli studied by Mössbauer spectroscopy and biochemical methods. Eur J Biochem. 1989 Aug 1;183(2):371–379. doi: 10.1111/j.1432-1033.1989.tb14938.x. [DOI] [PubMed] [Google Scholar]
  27. McConville M. L., Charles H. P. Mutants of Escherichia coli K12 permeable to haemin. J Gen Microbiol. 1979 Jul;113(1):165–168. doi: 10.1099/00221287-113-1-165. [DOI] [PubMed] [Google Scholar]
  28. Miller V. L., Mekalanos J. J. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol. 1988 Jun;170(6):2575–2583. doi: 10.1128/jb.170.6.2575-2583.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Nau C. D., Konisky J. Evolutionary relationship between the TonB-dependent outer membrane transport proteins: nucleotide and amino acid sequences of the Escherichia coli colicin I receptor gene. J Bacteriol. 1989 Feb;171(2):1041–1047. doi: 10.1128/jb.171.2.1041-1047.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Otto B. R., Verweij-van Vught A. M., MacLaren D. M. Transferrins and heme-compounds as iron sources for pathogenic bacteria. Crit Rev Microbiol. 1992;18(3):217–233. doi: 10.3109/10408419209114559. [DOI] [PubMed] [Google Scholar]
  31. Pendrak M. L., Perry R. D. Characterization of a hemin-storage locus of Yersinia pestis. Biol Met. 1991;4(1):41–47. doi: 10.1007/BF01135556. [DOI] [PubMed] [Google Scholar]
  32. Perry R. D., Brubaker R. R. Accumulation of iron by yersiniae. J Bacteriol. 1979 Mar;137(3):1290–1298. doi: 10.1128/jb.137.3.1290-1298.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Perry R. D., Pendrak M. L., Schuetze P. Identification and cloning of a hemin storage locus involved in the pigmentation phenotype of Yersinia pestis. J Bacteriol. 1990 Oct;172(10):5929–5937. doi: 10.1128/jb.172.10.5929-5937.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Prentki P., Krisch H. M. In vitro insertional mutagenesis with a selectable DNA fragment. Gene. 1984 Sep;29(3):303–313. doi: 10.1016/0378-1119(84)90059-3. [DOI] [PubMed] [Google Scholar]
  35. Rioux C. R., Kadner R. J. Two outer membrane transport systems for vitamin B12 in Salmonella typhimurium. J Bacteriol. 1989 Jun;171(6):2986–2993. doi: 10.1128/jb.171.6.2986-2993.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Robins-Browne R. M., Prpic J. K. Effects of iron and desferrioxamine on infections with Yersinia enterocolitica. Infect Immun. 1985 Mar;47(3):774–779. doi: 10.1128/iai.47.3.774-779.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Schramm E., Mende J., Braun V., Kamp R. M. Nucleotide sequence of the colicin B activity gene cba: consensus pentapeptide among TonB-dependent colicins and receptors. J Bacteriol. 1987 Jul;169(7):3350–3357. doi: 10.1128/jb.169.7.3350-3357.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Schägger H., von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem. 1987 Nov 1;166(2):368–379. doi: 10.1016/0003-2697(87)90587-2. [DOI] [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. Stoebner J. A., Payne S. M. Iron-regulated hemolysin production and utilization of heme and hemoglobin by Vibrio cholerae. Infect Immun. 1988 Nov;56(11):2891–2895. doi: 10.1128/iai.56.11.2891-2895.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Stull T. L. Protein sources of heme for Haemophilus influenzae. Infect Immun. 1987 Jan;55(1):148–153. doi: 10.1128/iai.55.1.148-153.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Săsărman A., Surdeanu M., Szégli G., Horodniceanu T., Greceanu V., Dumitrescu A. Hemin-deficient mutants of Escherichia coli K-12. J Bacteriol. 1968 Aug;96(2):570–572. doi: 10.1128/jb.96.2.570-572.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Tabor S., Richardson C. C. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc Natl Acad Sci U S A. 1985 Feb;82(4):1074–1078. doi: 10.1073/pnas.82.4.1074. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Ubben D., Schmitt R. Tn1721 derivatives for transposon mutagenesis, restriction mapping and nucleotide sequence analysis. Gene. 1986;41(2-3):145–152. doi: 10.1016/0378-1119(86)90093-4. [DOI] [PubMed] [Google Scholar]
  45. Waalwijk C., MacLaren D. M., de Graaff J. In vivo function of hemolysin in the nephropathogenicity of Escherichia coli. Infect Immun. 1983 Oct;42(1):245–249. doi: 10.1128/iai.42.1.245-249.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Weinberg E. D. Iron withholding: a defense against infection and neoplasia. Physiol Rev. 1984 Jan;64(1):65–102. doi: 10.1152/physrev.1984.64.1.65. [DOI] [PubMed] [Google Scholar]
  47. de Lorenzo V., Herrero M., Jakubzik U., Timmis K. N. Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria. J Bacteriol. 1990 Nov;172(11):6568–6572. doi: 10.1128/jb.172.11.6568-6572.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES