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. 1986 Oct;54(1):126–132. doi: 10.1128/iai.54.1.126-132.1986

Influence of iron on growth, morphology, outer membrane protein composition, and synthesis of siderophores in Campylobacter jejuni.

L H Field, V L Headley, S M Payne, L J Berry
PMCID: PMC260126  PMID: 2944843

Abstract

Three human isolates of Campylobacter jejuni were grown in a biphasic culture medium with and without the addition of a synthetic chelator to induce iron limitation. Cells grown in low-iron medium exhibited slower growth rates and altered cellular morphology. Increased numbers of longer, more filamentous forms were seen in Gram-stained smears. Three proteins, with apparent Mrs of 82,000, 76,000, and 74,000, were consistently present in the outer membrane of cells grown in low-iron medium. At least one of these proteins (76,000 to 74,000) was exposed on the cell surface. A bioassay was used to look for the production of siderophores by these and other strains of C. jejuni. Seven of 26 strains tested produced detectable amounts of siderophores. Growing strains at 42 degrees C failed to suppress siderophore synthesis or to alter the outer membrane protein profiles of iron-starved cells. The ability of three strains to utilize exogenously supplied siderophores for growth in low-iron medium was also examined. All three strains were able to utilize enterochelin and ferrichrome, but none utilized aerobactin, rhodotorulic acid, or desferrioxamine B. The effect of iron on the virulence of C. jejuni for 11-day-old chicken embryos inoculated via the chorioallantoic membrane was also determined.

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Selected References

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  1. Ames G. F. Resolution of bacterial proteins by polyacrylamide gel electrophoresis on slabs. Membrane, soluble, and periplasmic fractions. J Biol Chem. 1974 Jan 25;249(2):634–644. [PubMed] [Google Scholar]
  2. Atkin C. L., Neilands J. B., Phaff H. J. Rhodotorulic acid from species of Leucosporidium, Rhodosporidium, Rhodotorula, Sporidiobolus, and Sporobolomyces, and a new alanine-containing ferrichrome from Cryptococcus melibiosum. J Bacteriol. 1970 Sep;103(3):722–733. doi: 10.1128/jb.103.3.722-733.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Blaser M. J., Hopkins J. A., Berka R. M., Vasil M. L., Wang W. L. Identification and characterization of Campylobacter jejuni outer membrane proteins. Infect Immun. 1983 Oct;42(1):276–284. doi: 10.1128/iai.42.1.276-284.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Blaser M. J., Taylor D. N., Feldman R. A. Epidemiology of Campylobacter jejuni infections. Epidemiol Rev. 1983;5:157–176. doi: 10.1093/oxfordjournals.epirev.a036256. [DOI] [PubMed] [Google Scholar]
  5. Brot N., Goodwin J., Fales H. In vivo and in vitro formation of 2,3-dihydroxybenzoylserine by Escherichia coli K12. Biochem Biophys Res Commun. 1966 Nov 22;25(4):454–461. doi: 10.1016/0006-291x(66)90227-0. [DOI] [PubMed] [Google Scholar]
  6. Buck G. E., Parshall K. A., Davis C. P. Electron microscopy of the coccoid form of Campylobacter jejuni. J Clin Microbiol. 1983 Aug;18(2):420–421. doi: 10.1128/jcm.18.2.420-421.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bullen J. J. The significance of iron in infection. Rev Infect Dis. 1981 Nov-Dec;3(6):1127–1138. doi: 10.1093/clinids/3.6.1127. [DOI] [PubMed] [Google Scholar]
  8. Butzler J. P., Skirrow M. B. Campylobacter enteritis. Clin Gastroenterol. 1979 Sep;8(3):737–765. [PubMed] [Google Scholar]
  9. Field L. H., Headley V. L., Underwood J. L., Payne S. M., Berry L. J. The chicken embryo as a model for campylobacter invasion: comparative virulence of human isolates of Campylobacter jejuni and Campylobacter coli. Infect Immun. 1986 Oct;54(1):118–125. doi: 10.1128/iai.54.1.118-125.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Filip C., Fletcher G., Wulff J. L., Earhart C. F. Solubilization of the cytoplasmic membrane of Escherichia coli by the ionic detergent sodium-lauryl sarcosinate. J Bacteriol. 1973 Sep;115(3):717–722. doi: 10.1128/jb.115.3.717-722.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Finkelstein R. A., Sciortino C. V., McIntosh M. A. Role of iron in microbe-host interactions. Rev Infect Dis. 1983 Sep-Oct;5 (Suppl 4):S759–S777. doi: 10.1093/clinids/5.supplement_4.s759. [DOI] [PubMed] [Google Scholar]
  12. Garibaldi J. A. Influence of temperature on the biosynthesis of iron transport compounds by Salmonella typhimurium. J Bacteriol. 1972 Apr;110(1):262–265. doi: 10.1128/jb.110.1.262-265.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Garibaldi J. A. Influence of temperature on the iron metabolism of a fluorescent pseudomonad. J Bacteriol. 1971 Mar;105(3):1036–1038. doi: 10.1128/jb.105.3.1036-1038.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Inouye M., Guthrie J. P. A mutation which changes a membrane protein of E. coli. Proc Natl Acad Sci U S A. 1969 Nov;64(3):957–961. doi: 10.1073/pnas.64.3.957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. Logan S. M., Trust T. J. Outer membrane characteristics of Campylobacter jejuni. Infect Immun. 1982 Dec;38(3):898–906. doi: 10.1128/iai.38.3.898-906.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Luckey M., Pollack J. R., Wayne R., Ames B. N., Neilands J. B. Iron uptake in Salmonella typhimurium: utilization of exogenous siderochromes as iron carriers. J Bacteriol. 1972 Sep;111(3):731–738. doi: 10.1128/jb.111.3.731-738.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Miles A. A., Khimji P. L. Enterobacterial chelators of iron: their occurrence, detection, and relation to pathogenicity. J Med Microbiol. 1975 Nov;8(4):477–490. doi: 10.1099/00222615-8-4-477. [DOI] [PubMed] [Google Scholar]
  20. NG L. K., Sherburne R., Taylor D. E., Stiles M. E. Morphological forms and viability of Campylobacter species studied by electron microscopy. J Bacteriol. 1985 Oct;164(1):338–343. doi: 10.1128/jb.164.1.338-343.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Neilands J. B. Microbial envelope proteins related to iron. Annu Rev Microbiol. 1982;36:285–309. doi: 10.1146/annurev.mi.36.100182.001441. [DOI] [PubMed] [Google Scholar]
  22. Neilands J. B. Microbial iron compounds. Annu Rev Biochem. 1981;50:715–731. doi: 10.1146/annurev.bi.50.070181.003435. [DOI] [PubMed] [Google Scholar]
  23. Newell D. G., McBride H., Pearson A. D. The identification of outer membrane proteins and flagella of Campylobacter jejuni. J Gen Microbiol. 1984 May;130(5):1201–1208. doi: 10.1099/00221287-130-5-1201. [DOI] [PubMed] [Google Scholar]
  24. O'Brien I. G., Gibson F. The structure of enterochelin and related 2,3-dihydroxy-N-benzoylserine conjugates from Escherichia coli. Biochim Biophys Acta. 1970 Aug 14;215(2):393–402. doi: 10.1016/0304-4165(70)90038-3. [DOI] [PubMed] [Google Scholar]
  25. Payne S. M., Finkelstein R. A. The critical role of iron in host-bacterial interactions. J Clin Invest. 1978 Jun;61(6):1428–1440. doi: 10.1172/JCI109062. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. Perry R. D., San Clemente C. L. Siderophore synthesis in Klebsiella pneumoniae and Shigella sonnei during iron deficiency. J Bacteriol. 1979 Dec;140(3):1129–1132. doi: 10.1128/jb.140.3.1129-1132.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Pollack J. R., Neilands J. B. Enterobactin, an iron transport compound from Salmonella typhimurium. Biochem Biophys Res Commun. 1970 Mar 12;38(5):989–992. doi: 10.1016/0006-291x(70)90819-3. [DOI] [PubMed] [Google Scholar]
  29. Prescott J. F., Munroe D. L. Campylobacter jejuni enteritis in man and domestic animals. J Am Vet Med Assoc. 1982 Dec 15;181(12):1524–1530. [PubMed] [Google Scholar]
  30. Rogers H. J. Iron-Binding Catechols and Virulence in Escherichia coli. Infect Immun. 1973 Mar;7(3):445–456. doi: 10.1128/iai.7.3.445-456.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sciortino C. V., Finkelstein R. A. Vibrio cholerae expresses iron-regulated outer membrane proteins in vivo. Infect Immun. 1983 Dec;42(3):990–996. doi: 10.1128/iai.42.3.990-996.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Shand G. H., Anwar H., Kadurugamuwa J., Brown M. R., Silverman S. H., Melling J. In vivo evidence that bacteria in urinary tract infection grow under iron-restricted conditions. Infect Immun. 1985 Apr;48(1):35–39. doi: 10.1128/iai.48.1.35-39.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sigel S. P., Payne S. M. Effect of iron limitation on growth, siderophore production, and expression of outer membrane proteins of Vibrio cholerae. J Bacteriol. 1982 Apr;150(1):148–155. doi: 10.1128/jb.150.1.148-155.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Smibert R. M. The genus Campylobacter. Annu Rev Microbiol. 1978;32:673–709. doi: 10.1146/annurev.mi.32.100178.003325. [DOI] [PubMed] [Google Scholar]
  35. Smith G. S., Blaser M. J. Fatalities associated with Campylobacter jejuni infections. JAMA. 1985 May 17;253(19):2873–2875. [PubMed] [Google Scholar]
  36. Sullivan K. H., Williams R. P. Use of iodo-gen and iodine-125 to label the outer membrane proteins of whole cells of Neisseria gonorrhoeae. Anal Biochem. 1982 Mar 1;120(2):254–258. doi: 10.1016/0003-2697(82)90344-x. [DOI] [PubMed] [Google Scholar]
  37. WINDER F. G., O'HARA C. Effects of iron deficiency and of zinc deficiency on the composition of Mycobacterium smegmatis. Biochem J. 1962 Jan;82:98–108. doi: 10.1042/bj0820098. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. 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]
  39. Wilkins T. D., Lankford C. E. Production by Salmonella typhimurium of 2,3-dihydroxybenzoylserine, and its stimulation of growth in human serum. J Infect Dis. 1970 Feb;121(2):129–136. doi: 10.1093/infdis/121.2.129. [DOI] [PubMed] [Google Scholar]
  40. Worsham P. L., Konisky J. Effect of growth temperature on the acquisition of iron by Salmonella typhimurium and Escherichia coli. J Bacteriol. 1984 Apr;158(1):163–168. doi: 10.1128/jb.158.1.163-168.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]

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