1887

Microbiology Society logo

Volume 142, Issue 5

Acquisition of iron by the non-siderophore-producing Pseudomonas fragi Free

Abstract

The iron requirement, siderophore production and iron uptake mechanisms of the type strain ATCC 4973 and five isolates from meat were analysed. The strains exhibited a high sensitivity to iron starvation: their growth was strongly inhibited in medium supplemented with the iron chelator ethylenediamine di(hydroxyphenylacetic acid) or in medium treated with 8-hydroxyquinoline to remove contaminating iron. No siderophores were detectable in the growth supernatants of iron-starved cells. Cross-feeding experiments in iron-depleted medium showed, however, that the bacterial growth could be strongly stimulated by siderophores of foreign origin including desferriferrioxamine B, enterobactin and some pyoverdines. Moreover, all the strains were capable of efficiently using the iron sources present in their natural environment, i.e. transferrin, lactoferrin and haemoglobin. Iron starvation led to the specific production of supplementary outer-membrane proteins of apparent molecular mass ranging from 80 to 88 kDa. Furthermore, growth in the presence of exogenous siderophores resulted, in some strains, in the induction of siderophore-mediated iron uptake systems. For one strain the concomitant synthesis of an iron-regulated, siderophore-inducible outer-membrane protein was observed.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): iron acquisition , Pseudomonas fragi and siderophore
© Society for General Microbiology 1996
Loading

Article metrics loading...

/content/journal/micro/10.1099/13500872-142-5-1191
1996-05-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/142/5/mic-142-5-1191.html?itemId=/content/journal/micro/10.1099/13500872-142-5-1191&mimeType=html&fmt=ahah

References

  1. Adams T.J., Vartivarian S., Cowart R.E. Iron acquisition of Listeria monocytogenes. Infect Immun 1990; 58:2715–2718
     [Google Scholar]
  2. Archibald F. Lactobacillus plantarum, an organism not requiring iron. FEMS Microbiol Lett 1983; 19:29–32
     [Google Scholar]
  3. Bagg A., Neilands J.B. Molecular mechanism of regulation of siderophore-mediated iron assimilation. Microbiol Rev 1987; 51:509–518
     [Google Scholar]
  4. Bitter W., Tommassen J., Weisbeek P.J. Identification and characterization of exbB, exbD and tonB genes of Pseudomonas putida WCS358: their involvement in ferric-pseudobactin transport. Mol Microbiol 1993; 7:117–130
     [Google Scholar]
  5. Braun V., Hantke K., Eick-Helmerich K., Köster W., Pressler U., Sauer M., Schäffer S., Schöffler H., Staudenmaier H., Zimmermann L. Iron transport systems in Escherichia coli. In Iron Transport in Microbes 1987 Edited by Winkelmann G., Van Der Helm D., Neilands J.B. Weinheim: VCH Verlagsgesellschaft; Plants and Animals, pp 35–51
     [Google Scholar]
  6. Budzikiewicz H. Secondary metabolites from fluorescent pseudomonads. FEMS Microbiol Rev 1993; 104:209–228
     [Google Scholar]
  7. Champomier-Vergfes M.C., Richard J. Antibacterial activity among Pseudomonas strains of meat origin. Lett Appl Microbiol 1994; 18:18–20
     [Google Scholar]
  8. Cody Y.S., Gross D.C. Characterization of pyoverdinPss, the fluorescent siderophore produced by Pseudomonas syringae pv. syringae. Appl Environ Microbiol 1987; 53:928–934
     [Google Scholar]
  9. Cornelis P., Hohnadel D., Meyer J.M. Evidence for different pyoverdine-mediated iron uptake systems among Pseudomonas aeruginosa strains. Infect Immun 1989; 57:3491–3497
     [Google Scholar]
  10. Cox C.D. Iron uptake with ferripyochelin and ferric citrate by Pseudomonas aeruginosa. J Bacteriol 1980; 142:581–587
     [Google Scholar]
  11. Cox C.D., Adams P. Siderophore activity of pyoverdin for Pseudomonas aeruginosa. Infect Immun 1985; 48:130–138
     [Google Scholar]
  12. Frost G., Rosenberg H. The inducible citrate-dependent iron transport system in Escherichia coli K12. Biochim Biophys Acta 1973; 330:90–101
     [Google Scholar]
  13. Gensberg K., Hughes K., Smith A.W. Siderophore -specific induction of iron uptake in Pseudomonas aeruginosa. J Gen Microbiol 1992; 138:2381–2387
     [Google Scholar]
  14. Gill C.O., Newton K.G. The development of aerobic flora on a meat stored at chill temperature. I Appl Bacteriol 1977; 43:189–195
     [Google Scholar]
  15. Guerinot M.L., Meidl E.J., Plessner O. Citrate as a siderophore in Bradyrhizobium japonicum. J Bacteriol 1990; 172:3298–3303
     [Google Scholar]
  16. Harding R.A., Royt P. Acquisition of iron from citrate by Pseudomonas aeruginosa. J Gen Microbiol 1990; 136:1859–1867
     [Google Scholar]
  17. Heinrichs D.E., Young L., Poole K. Pyochelin-mediated iron transport in Pseudomonas aeruginosa: involvement of a high-molecular-mass outer membrane protein. Infect Immun 1991; 59:3680–3684
     [Google Scholar]
  18. Hohnadel D., Meyer J.M. Specificity of pyoverdine-mediated iron uptake among fluorescent Pseudomonas strains. J Bacteriol 1988; 170:4865–4873
     [Google Scholar]
  19. Johnson W., Varner L., Poch M. Acquisition of iron by Legionella pneumophila: role of iron reductase. Infect Immun 1991; 59:2376–2381
     [Google Scholar]
  20. Jurkevitch E., Hadar Y., Chen Y. Differential siderophore utilization and iron uptake by soil rhizosphere bacteria. Appl Environ Microbiol 1992; 38:119–124
     [Google Scholar]
  21. King E.O., Ward M.K., Raney D.F. Two simple media for the demonstration of pyocyanin and fluorescein. J Lab Clin Med 1954; 44:301–307
     [Google Scholar]
  22. Koster M.C., Van De Vossenberg J., Leong J., Weisbeek P.J. Identification and characterization of the pupB gene encoding an inducible ferric-pseudobactin receptor of Pseudomonas putida WCS358. Mol Microbiol 1993; 8:591–601
     [Google Scholar]
  23. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of the bacteriophage T4. Nature 1970; 227:680–685
     [Google Scholar]
  24. Lesueur D., Diem H.J., Meyer J.M. Iron requirements and siderophore production in Bradyrhizobium strains isolated from Acacia mangium. J Appl Bacteriol 1993; 74:675–682
     [Google Scholar]
  25. Lesuisse E., Labbe P. Reductive and nonreductive mechanisms of iron assimilation by the yeast Saccharomyces cerevisiae. J Gen Microbiol 1989; 135:257–263
     [Google Scholar]
  26. Magazin M.D., Moores J.C., Leong J. Cloning of the gene coding for the outer membrane receptor for ferric pseudo-bactin, a siderophore from a plant growth promoting Pseudomonas strain. J Biol Chem 1986; 261:795–799
     [Google Scholar]
  27. Marugg J.D., De Weger L.A., Nielander H.B., Oorthuizen M., Recourt K., Lugtenberg B., Van Der Hofstad G.A.J., M. & Weisbeek P.J. Cloning and characterization of a gene encoding an outer membrane protein required for siderophore-mediated uptake of Fe3+ in Pseudomonas putida WCS358. J Bacteriol 1989; 171:2819–2826
     [Google Scholar]
  28. Martel N., Lee B.C. Acquisition of heme iron by Neisseria meningitidis does not involve meningococcal transferrin-binding proteins. Infect Immun 1994; 62:700–703
     [Google Scholar]
  29. Meyer J.M. Exogenous siderophore-mediated iron uptake in Pseudomonas aeruginosa. Possible involvement of porin OprF in iron translocation. J Gen Microbiol 1992; 138:951–958
     [Google Scholar]
  30. Meyer J.M., Abdallah M.A. The fluorescent pigment of Pseudomonas fluorescens: biosynthesis, purification and physicochemical properties. J Gen Microbiol 1978; 107:319–328
     [Google Scholar]
  31. Meyer J.M., Abdallah M.A. The siderochromes of non-fluorescent pseudomonads: production of nocardamine by Pseudomonas stützen. J Gen Microbiol 1980; 118:125–129
     [Google Scholar]
  32. Meyer J.M., Hallé F., Hohnadel D., Lemanceau P., Ratefiarivelo H. Siderophores of Pseudomonas - biological properties. In Iron Transport in Microbes 1987 Edited by Winkelmann G., Van Der Helm D., Neilands J.B. Weinheim: VCH Verlagsgesellschaft; Plants and Animals, pp 188–205
     [Google Scholar]
  33. Meyer J.M., Hallé F., Hohnadel D. Cepabactin from Pseudomonas cepacia, a new type of siderophore. J Gen Microbiol 1989; 135:1479–1487
     [Google Scholar]
  34. Meyer J.M., Hohnadel D., Kahn A., Cornelis P. Pyoverdine-facilitated iron uptake in Pseudomonas aeruginosa: immunological characterization of the ferripyoverdine receptor. Mol Microbiol 1990; 4:1401–1405
     [Google Scholar]
  35. Meyer J.M., Azelvandre P., Georges C. Iron metabolism in Pseudomonas: salicylic acid, a siderophore of Pseudomonas fluorescens CHAO. Biofactors 1992; 4:23–27
     [Google Scholar]
  36. Meyer J.M., Tran Van V., Stintzi A., Berge O., Winkelmann G. Ornibactin production and transport properties in strains of Burkholderia vietnamiensis and Burkholderia cepacia (formerly Pseudomonas cepacia). BioMetals 1995; 8:309–317
     [Google Scholar]
  37. Mizuno T., Kageyama A. Separation and characterization of outer membrane of Pseudomonas aeruginosa. J Biochem 1978; 84:179–191
     [Google Scholar]
  38. Moellering H., Gruber W. Determination of citrate with citrate lyase. Anal Biochem 1966; 17:369–376
     [Google Scholar]
  39. Molin G., Ternström A. Numerical taxonomy of psychrotrophic pseudomonads. J Gen Microbiol 1982; 128:1249–1264
     [Google Scholar]
  40. Morton D.J., Williams P. Siderophore-independent acquisition of transferrin-bound iron by Haemophilus influenzae type b. J Gen Microbiol 1990; 136:927–933
     [Google Scholar]
  41. Neilands J.B. A crystalline organo-iron pigment from a rust fungus (Ustilago sphaerogena). J Am Chem Soc 1952; 74:4846–4847
     [Google Scholar]
  42. Neilands J.B. Microbial iron compounds. Annu Rev Biochem 1981; 50:715–731
     [Google Scholar]
  43. Neilands J.B. Microbial envelope proteins related to iron. Annu Rev Microbiol 1982; 36:285–309
     [Google Scholar]
  44. O'Sullivan D.J., O'Gara F. Traits of fluorescent Pseudomonas spp involved in suppression of plant root pathogens. Microbiol Rev 1992; 56:662–676
     [Google Scholar]
  45. Pandey A., Bringet F., Meyer J.M. Iron requirement and search for siderophores in lactic acid bacteria. Appl Microbiol Biotechnol 1994; 40:735–739
     [Google Scholar]
  46. Poole K., Young L., Neshat S. Enterobactin-mediated iron transport in Pseudomonas aeruginosa. J Baderiol 1990; 172:6991–6996
     [Google Scholar]
  47. Poole K., Neshat S., Krebes K., Heinrichs D.E. Cloning and nucleotide sequence analysis of the ferripyoverdine receptor gene fpvA of Pseudomonas aeruginosa. J Bacterial 1993; 175:4597–4604
     [Google Scholar]
  48. Prince P.W., Cox C.D., Vasil M.L. Coordinate regulation of siderophore and exotoxin A production: molecular cloning and sequencing of the Pseudomonas aeruginosa fur gene. J Bacteriol 1993; 175:2589–2598
     [Google Scholar]
  49. Pugsley A.P., Oudega B. Methods for studying colicins and their plasmids. In Plasmids 1987 Edited by Hardy K.G. Oxford: IRL Press; a Practical Approach, pp 105–161
     [Google Scholar]
  50. Ratledge C. Iron metabolism in mycobacteria. In Iron Transport in Microbes 1987 Edited by Winkelmann G., Van Der Helm D., Neilands J.B. Weinheim: VCH V erlagsgesellschaft; Plants and Animals, pp 207–221
     [Google Scholar]
  51. Rogers H.J. Iron-binding catechols and virulence in Escherichia coli. Infect Immun 1973; 7:445–456
     [Google Scholar]
  52. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning: a Eaboratorj Manual 1989 Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  53. Sawatzki G., Anselstetter V., Kubanek B. Isolation of mouse transferrin using salting-out chromatography on Sepharose CL6B. Biochim Biophys Acta 1981; 667:132–138
     [Google Scholar]
  54. Schmithaeusler R., Ratefiarivelo H., Meyer J.M. Purification de transferrine (Tsf) humaine par Chromatographie d’échange d’ion à partir de la fraction IV de Cohn. In Premier Colloque National de Technologies de Purification de Protéines 1984 Paris, Oc t. 1984
    [Google Scholar]
  55. Schryvers A.B. Characterization of the human transferrin and lactoferrin receptors in Haemophilus influenzae. Mol Microbiol 1988; 2:467–472
     [Google Scholar]
  56. Schryvers A.B., Morris L.J. Identification and characterization of the transferrin receptor from Neisseria gonorrhoeae. Mol Microbiol 1988; 2:281–288
     [Google Scholar]
  57. Schwyn B., Neilands J.B. Universal chemical assay for the detection and determination of siderophores. Anal Biochem 1987; 160:47–56
     [Google Scholar]
  58. Simon N., Coulanges V., André P., Vidon D.J.-M. Utilization of exogenous siderophores and natural catechols by Eisteria monocytogenes. Appl Environ Microbiol 1995; 61:1643–1645
     [Google Scholar]
  59. Simonson C., Brenner D., Devoe I.W. Expression of a high-affinity mechanism for acquisition of transferrin iron by Neisseria meningitidis. Infect Immun 1982; 36:107–113
     [Google Scholar]
  60. Sokol P.A. Production and utilization of pyochelin by clinical isolates of Pseudomonas cepacia. J Clin Microbiol 1986; 23:560–562
     [Google Scholar]
  61. Stephan H., Freund S., Beck W., Jung G., Meyer J.M., Winkelmann G. Ornibactins - a new family of siderophores from Pseudomonas. BioMetals 1993; 6:93–100
     [Google Scholar]
  62. Ternstrôm A., Lindberg A.M., Molin G. Classification of the spoilage flora of raw and pasteurized bovine milk with special reference to Pseudomonas and Bacillus. J Appl Bacteriol 1993; 75:25–34
     [Google Scholar]
  63. Venturi V., Ottevanger C., Leong J., Weisbeek P.J. Identification and characterization of a siderophore regulatory gene (pfrA) of Pseudomonas putida WCS358: homology to the alginate regulatory gene algQ of Pseudomonas aeruginosa. Mol Microbiol 1993; 10:63–73
     [Google Scholar]
  64. Visca P., Ciervo A., Sanfilippo V., Orsi N. Iron-regulated salicylate synthesis by Pseudomonas spp. J Gen Microbiol 1993; 139:1995–2001
     [Google Scholar]
  65. Waring W.S., Werkman C.H. Growth of bacteria in an iron-free medium. Arch Biochem 1942; 1:303–310
     [Google Scholar]
  66. De Weger L.A., von Arendonk J.C.H.M., Recourt K., Van Der Hofstad G.A.J.M., Weisbeek P.J., Lugtenberg B. Siderophore-mediated iron uptake in the plant-stimulating Pseudomonas putida WCS358 and other rhizosphere microorganisms. J Bacteriol 1988; 170:4693–4698
     [Google Scholar]
  67. Wiebe C., Winkelmann G. Kinetics studies on the specificity of chelate iron uptake in Aspergillus. J Bacteriol 1975; 123:837–842
     [Google Scholar]
  68. Young I.G., Gibson F. Isolation of enterochelin from Escherichia coli. Methods Enzymol 1979; 56:394–398
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/13500872-142-5-1191
Loading
Acquisition of iron by the non-siderophore-producing Pseudomonas fragi
Microbiology 142, 1191 (1996); https://doi.org/10.1099/13500872-142-5-1191
/content/journal/micro/10.1099/13500872-142-5-1191
/content/journal/micro/10.1099/13500872-142-5-1191
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error