Ecological Significance of Siderophores in Soil

  • P. Bossier
  • M. Hofte
  • W. Verstraete
Part of the Advances in Microbial Ecology book series (AMIE, volume 10)


Among the extracellular secondary metabolites, microbial iron-chelating compounds, also called siderophores, have received considerable attention. The ecological interest in these compounds is gradually increasing, especially in terms of the possible function of these compounds in soil The current increasing interest and research on bacterial siderophores is to a great extent linked to investigations on the inoculation of plant seeds with fluorescent Pseudomonas spp. that are considered to produce siderophores counteracting deleterious microorganisms in the root zone. The research on the ecology of fungal siderophores has been focused on the role of the fungal siderophores in the acquisition of iron by plants. Much of the knowledge on siderophores is based on observations in vitro. There are, however, considerable differences between the environmental circumstances in soil and in synthetic media. Given these facts, it is of interest to consider the points on which the ecological research on siderophores should focus in order to obtain a better understanding of their role in the soil environment. It is our intention in this chapter to review the ecological significance of siderophores in natural environments such as the soil.


Ecological Significance Neurospora Crassa Axenic Culture Siderophore Production Penicillium Chrysogenum 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ahl, P., Voisard, C., and Defago, G., 1986, Iron bound-siderophores, cyanic acid and antibiotics involved in suppression of Thielaviopsis basicola by a Pseudomonas fluorescens strain, J. Phytopathol 116:121–134.CrossRefGoogle Scholar
  2. Akers, H. A., 1981, The effect of waterlogging on the quantity of microbial iron chelators (siderophores) in soil, Soil Scl 132:150–152.CrossRefGoogle Scholar
  3. Akers, H.A., 1983a, Multiple hydroxamic acid microbial chelators (siderophores) in soils, Soil Sei. 135:156–160.Google Scholar
  4. Akers, H. A., 1983b, Isolation of the siderophore schizokinen from soil of rice field, Appl. Environ. MierobioL 45:1704–1706.Google Scholar
  5. Atkin, C. L., Neilands, J. B., and Pfaff, H. J., 1970, Rhodotorulic acid from species of Leu- cosporidium, Rhodosporidium, Rhodoturula, Sporodia bolus andSporobolomyees and new alanine-containing ferrichrome from Cryptoeoeeus melibiosum, J. Bacteriol 103:722–733.PubMedGoogle Scholar
  6. Bakker, P. A. H. M., Weisbeek, P. J., and Schippers, B., 1986, The role of siderophores in plant growth stimulation by fluorescent Pseudomonas spp. Med. Fac. Landbouww. Rijksuniv. Gent. 51:1357–1362.Google Scholar
  7. Becker, J. O., Hedges, R. W., and Messens, E., 1985, Inhibitory effect of pseudobactin on the uptake of iron by higher plants. Appl. Environ. Microbiol. 49:1090–1093.PubMedGoogle Scholar
  8. Becker, J. O., Messens, E., and Hedges, R. W., 1986, A convenient autoradiographic technique for the study of uptake of minerals by plants roots and the effects of environmental factors upon the process. Plant Soli 92:299–302.CrossRefGoogle Scholar
  9. Bienfait, H. F., Druivenvoorden, J., and Verkerke, W., 1982, Ferric reduction of roots of chlorotic bean plants: Indications for an enzymatic process, J. Plant Nutr. 5:451–457.CrossRefGoogle Scholar
  10. Bienfait, H. F., Bino, R. J., Van den Bliek, A. M., Duivenvoorden, J. F., and Fontain, J. M., 1983, Characterisation of ferric reducing activity in roots of Fe deficient Phaseolus vulgaris, Physiol. Plant 59:196–202.CrossRefGoogle Scholar
  11. Bossier, P., and Verstraete, W., 1986a, A direct bioassay for the detection of hydroxamate siderophores in soil. Soil Biol. Biochem. 18:481–486.CrossRefGoogle Scholar
  12. Bossier, P., and Verstraete, W., 1986b, Ecology of Arthrobacter JG9 detectable hydroxamate siderophores in soils. Soil Biol Biochem. 18:487–492.CrossRefGoogle Scholar
  13. Brown, A. E., and Swinburne, T. R., 1981, Influence of iron and iron chelators on formation of progressive lesions of Colletotrichum musae on banana fruits. Trans. Br. Mycol. Soc. 77:119–124.CrossRefGoogle Scholar
  14. Burnham, B. F., and Neilands, J. A., 1961, Studies of the metabolic function of the ferrichrome compounds, J. Biol. Biochem. 236:554–559.Google Scholar
  15. Burr, T. J, and Caesar, A., 1984, Beneficial plant bacteria, Crit. Rev. Plant Sei. 2(l):l-20.Google Scholar
  16. Chariang, G., Bradford, N., Horowitz, N., and Horowitz, R. M., 1981, Cellular and extracellular siderophores of Aspergillus nidulans and Penicillium chrysogenum, Mol. Cell Biol. 1:94–100.Google Scholar
  17. Cline, G. R., Reid, C. P. P., Powell, P. E., and Szaniszlo, P. J., 1984, Effect of a hydroxamate siderophore on iron absorption by sunflower and sorghum. Plant Physiol. 76:36–39.PubMedCrossRefGoogle Scholar
  18. Crueger, W., and Zähner, H., 1968, Stoffwechselproduktie von Mikroorganismen. 70 Mitteilung. Uber der Einfluss der Kohlenstoffquelle auf die Sideraminebildung vonAspergillus melleus Yukawa, Arch. Mikrobiol 63:376–384.PubMedCrossRefGoogle Scholar
  19. Demange, P., Wendenbaum, S., Bateman, A., Dell, A., Meyer, J. M., and Abdallah, M. A., 1985, Bacterial siderophores: Structure of pyoverdine and related compounds, Advanced Nato Research Workshop, London (July 1985), Abstract.Google Scholar
  20. Deweger, L. A., Van Boxtel, R., Van der Burg, B., Gruters, R. A., Geels, F. P., Schippers, B., and Lugtenberg, B., 1986, Siderophores and outer membrane proteins of antagonistic, plant growth stimulating root-colonizing Pseudomonas spp, J. Bacteriol. 165:585–594.Google Scholar
  21. El Sayed, A., Verhe, R., Proot, M., Sandra, P., and Verstraete, W., 1986a, Binding of nitrite- N on polyphenols during nitrification. Plant Soil 94:369–382.CrossRefGoogle Scholar
  22. El Sayed, A., Vandenabeele, J., and Verstraete, W., 1986b, Nitrification and organic nitrogen formation in soils. Plant Soil 94:383–400.CrossRefGoogle Scholar
  23. El Sayed, A., Van Cleemput, O., and Verstraete, W., 1986c, Nitrification mediated nitrogen immobilization in soils.Plant Soil 94:401–440.CrossRefGoogle Scholar
  24. Emery, T., 1966, Initial steps in the biosynthesis of ferrichrome: Incorporation of 6-N- hydroxyomithine and 5-N-acetyl 5-N-hydroxyomithine,Biochemistry 5:3694–3701.PubMedCrossRefGoogle Scholar
  25. Focht, D. D., and Verstraete, W., 1977, Biochemical ecology of nitrification and denitrifi- cation, in: Advances in Microbial Ecology, Vol. 1 (M. Alexander, ed.) pp. 135–214. Plenum Press. New York.Google Scholar
  26. Frederick, C. B., Szaniszlo, P. J., Vickrey, P. E., Bentley, M. D., and Shive, W., 1981, Production and isolation of siderophores from the soil fungus Epicoccum purpurascens. Biochemistry 20:2432–2436.Google Scholar
  27. Grimes, H. D., and Mount, M. S., 1984, Influence of Pseudomonas putida in nodulation of Phaseolus vulgaris. Soil Biol Biochem. 16:27–30.CrossRefGoogle Scholar
  28. Haider, K., Mosier, A., and Heinemeyer, O., 1985, Phytotron experiments to evaluate the effect of growing plants on denitrification. Soil Sei. Soc. Am. J. 49:636–641.CrossRefGoogle Scholar
  29. Haller, T., and Stolp, H., 1985, Quantitative estimation of root exudation of maize plants. Plant Soil 86:207–216.CrossRefGoogle Scholar
  30. Harrington, G. J., and Neilands, J. B., 1982, Isolation and characterisation of dimerumic acid from Verticillium dahliae, J. Plant Nutr. 5:675–682.CrossRefGoogle Scholar
  31. Hemming, B. C, Orser, C., Jacobs, D. L., Sands, D. C, and Strobel, G. A., 1982, The effects of iron on microbial antagonism by fluorescent Pseudomonads, J. Plant. Nutr. 5:683–702.CrossRefGoogle Scholar
  32. Hohnadel, D., and Meyer, J. M., 1985, Pyoverdine-facilitated iron uptake among fluorescent pseudomonads. Advanced Nato Research Workshop, London (July 1985), Abstract.Google Scholar
  33. Huschka, H., Naegeli, H. V., Leuenberger-Ryf, H., Keller-Schierlein, W., and Winkelmann, G., 1985, Evidence for a common siderophore transport system but different sidero- phore receptors in Neurospora crassa, J. Bacteriol. 162:715–721.Google Scholar
  34. Iswandi, A., 1986, Seed inoculation with Pseudomonas spp., Ph.D. Thesis, State University of Gent, Faculty of Agricultural Sciences, Belgium.Google Scholar
  35. Jalal, M. A. F., Mocharia, R., Barnes, C. L., Hossain, M. B., Powell, D. G., Eng-Wilmot, D. L., Grayson, S. L., Benson, B. A., and Van der Helm, D., 1984, Extracellular siderophores from Aspergillus ochraceous, J. Bacteriol. 158:683–688.Google Scholar
  36. Jurkevitch, E., Hadar, Y., and Chen, Y., 1985, The effect of Pseudomonas siderophores on iron nutrition of peanuts. Advanced Nato Research Workshop, London (July 1985), Abstract.Google Scholar
  37. Kloepper, J. W., Leong, L., Teintze, M., and Schroth, M. N., 1980a, Enhanced plant growth by siderophores produced by PGPR, Nature 286:885–886.CrossRefGoogle Scholar
  38. Kloepper, J. W., Leong, J., Teintze, M., and Schroth, M. N., 1980b, Pseudomonas sidero- phores: A mechanism explaining disease suppressive soils, Curr. Microbiol. 4:317–320.CrossRefGoogle Scholar
  39. Knüsel, F., Schiess, B., and Zimmermann, W., 1969, The influence exerted by sideromycins on poly-U-directed incorporation of phenylalanine in the S-30 fraction of Staphylococcus aureus. Arch. Mikrobiol. 68:99–106.PubMedCrossRefGoogle Scholar
  40. Kraffczyck, J., Trolldenier, G., and Beringer, H., 1984, Soluble root exudates of maize: Influence of potassium supply and rhizosphere microorganisms. Soil Biol. Biochem. 16:315–322.CrossRefGoogle Scholar
  41. Lindsay, W. L., 1979,Chemical Equilibria in Soils, Wiley-Interscience, New York.Google Scholar
  42. Meyer, J. M., and Abdallah, M. A., 1978, The fluorescent pigment ofPseudomonas fluores- cens: Biosynthesis, purification and physico-chemical properties,J. Gen. Microbiol. 107:321–331.Google Scholar
  43. Murray, T., Lazaridis, I., and Seddon, B., 1985, Germination of spores of Bacillus brevis and inhibition by gramicidin S: A strategem for survival, Lett. Appl. Microbiol. 1:63–65.CrossRefGoogle Scholar
  44. Neilands, J. B., 1979, Biomedical and environmental significance of siderophores, in: Trace Metals in Health and Disease (N. Kharash, ed.) pp. 27–41, Raven Press, New York.Google Scholar
  45. Neilands, J. B., 1981, Iron absorption and transport in microorganisms,Annu. Rev. Nutr. 1:27–46.PubMedCrossRefGoogle Scholar
  46. Neilands, J. B., 1982, Iron envelope proteins, Annu. Rev. Microbiol. 36:285–309.PubMedCrossRefGoogle Scholar
  47. Olsen, R. A., Brown, J. C, Bennett, J. H., and Blume, D., 1982, Reduction of Fe3+ as it relates to Fe chlorosis, J. Plant Nutr. 5:433–447.CrossRefGoogle Scholar
  48. Page, E. R., 1966, Sideramines in plants and their possible role in iron metabolism, Biochem. J. 100:34.Google Scholar
  49. Page, W. J., and Dale, P. L., 1986, Stimulation of Agrobacterium tumefaciens growth by Azotabacter vinelandii ferrisiderophores, Appl. Environ. Microbiol. 51:451–454.PubMedGoogle Scholar
  50. Page, W. J., and Huyer, M., 1984, Derepression of theAzotobacter vinelandii siderophore system, using iron-containing minerals to limit iron repletion. J. Bacteriol. 158:496–502.PubMedGoogle Scholar
  51. Perlman, D., 1965, Microbial production of metal-organic compounds and complexes, in: Advances in Applied Microbiology, Vol. 7 (W. W. Umbreit, ed.), pp. 103–138, Academic Press, New York.Google Scholar
  52. Philson, S. B., and Llinas, M., 1982, Siderochromes from Pseudomonas fluorescens. I. Isolation and characterisation, J. Biol. Chem. 257: 8081–8085.PubMedGoogle Scholar
  53. Powell, P. E., Cline, G. R., Reid, C. P. P., and Szaniszlo, P. J., 1980, Occurrence of hydrox- amate siderophore iron chelators in soils. Nature 287:833–834.CrossRefGoogle Scholar
  54. Powell, P. E., Szaniszlo, P. J., Cline, G. R., and Reid, C. P. P., 1982, Hydroxamate siderophores in the iron nutrition of plants, J. Plant Nutr. 5:653–673.CrossRefGoogle Scholar
  55. Powell, P. E., Szaniszlo, P. J., and Reid, C. P. P., 1983, Confirmation of occurrence of hydroxamate siderophores in soil by a novel Escherichia coli bioassay, Appl. Environ. Microbiol. 46:1080–1083.PubMedGoogle Scholar
  56. Raymond, K. N., Mueller, G., and Matzanke, B. F., 1984, Complexation of iron by siderophores. A review of their solution and structural chemistry and biological function, Top. Curr. Chem. 123:49–102.CrossRefGoogle Scholar
  57. Reid, R. K., Reid, C. P. P., and Szaniszlo, P. J., 1985, Effects of synthetic and microbially producted chelates on the diffusion of iron and phosphorus to a simulated root in soil, Biol. Fertil. Soils 1:42–45.CrossRefGoogle Scholar
  58. Römheld, V., and Marschner, H., 1983, Mechanism of iron uptake by peanut plants, 1. Fe reduction, chelate splitting and release of phenolics. Plant Physiol. 71:949–954.PubMedCrossRefGoogle Scholar
  59. Römheld, V., and Marschner, H., 1986, Evidence for a specific uptake system for iron phy- tosiderophores in roots of grasses. Plant Physiol. 80:175–180.PubMedCrossRefGoogle Scholar
  60. Römheld, V., Marschner, H., and Kramer, D., 1982, Responses of Fe-deficiency in roots of "Fe-efiicient" plant species, J. Plant Nutr. 5: 489–499.CrossRefGoogle Scholar
  61. Scher, F. M., and Baker, R., 1982, Effect of Pseudomonas putida and a synthetic iron chelator on induction of soil suppressiveness toFusarium wilt pathogens, Phytopathology 72:1567–1573.CrossRefGoogle Scholar
  62. Schippers, B., Bakker, P. A. H. M., Bakker, A. W., Weisbeek, P. J., and Lutgenberg, B., 1986, Plant growth inhibiting and stimulating rhizosphere microorganisms, in: Microbial Communities in Soil (V. Jensen, A. Kjoller, and L. H. Sorensen, eds.), pp. 35–49, Elsevier, London.Google Scholar
  63. Slade, S. J., and Swinburne, T. R., 1985a, Infection development of Colletotrichum linde- muthianum race ß on resistant and susceptible cultivars of Phaseolus vulgaris affected by a bacterial siderophore. Advanced Nato Research Workshop, London (July 1985), Abstract.Google Scholar
  64. Slade, S. J., and Swinburne, T. R., 1985b, Phytoalexin accumulation elicited abiotically in Vicia faba reduced by a bacterial siderophore. Advanced Nato Research Workshop, London (July 1985), Abstract.Google Scholar
  65. Stiefel, E. L, Burgess, B. K., Wherland, S., Newton, W. E., Corbin, J. L., and Watt, G. D., 1980, Azotobacter vinelandii biochemistry: H2(D2)N2 relationships of nitrogenase and some aspects of iron metabolism in: Nitrogen Fixation, Vol. 1 (W. E. Newton and W. H. OrmeJohnson, eds.), pp. 221–222, University Park Press, Baltimore, Maryland.Google Scholar
  66. Stone, K. J., and Stominger, J. L., 1972, Inhibition of sterol biosynthesis by bacitracin, Proc. Natl Acad Sei. USA 69:1287.CrossRefGoogle Scholar
  67. Stutz, E., 1964, Aufnahme von ferrioxamine B durch Tomatenplanzen, Experimentia 20:430–431.CrossRefGoogle Scholar
  68. Sugiura, Y., and Nomoto, K., 1984, Phytosiderophores: Structures and properties of mugi- neic acids and their metal complexes. Structure Bonding 58:107–135.CrossRefGoogle Scholar
  69. Suslow, T. v., and Schroth, M. N., 1982, Role of deleterious rhizobacteria as minor pathogens in reducing crop growth, Phytopathology 72:111–115.CrossRefGoogle Scholar
  70. Szabo, I., Benedek, A., and Barabas, G., 1985, Possible role of streptomycin released from spore cell wall of Streptomyces griseus, Appl Environ. Microbiol. 50:438–440.PubMedGoogle Scholar
  71. Szaniszlo, P. J., Powell, P. E., Reid, C. P. P., and Cline, G. R., 1981, Production of hydrox- amate siderophore iron chelators by ectomycorrhizal fungi, Mycologia 73:1158–1175.CrossRefGoogle Scholar
  72. Szaniszlo, P. J., Tai, S. C., Crowley, D. E., and Reid, C. P. P., 1985, Mechanisms of iron acquisition from hydroxamate siderophores by two monocot plant species. Advanced Nato Research Workshop, London (July 1985), Abstract.Google Scholar
  73. Teintze, M., and Leong., J., 1981, Structure of pseudobactin A, a second siderophore from plant growth promoting Pseudomonas BIO, Biochemistry 20:6457–6462.PubMedCrossRefGoogle Scholar
  74. Teintze, M., Hossain, M. D., Barnes, C. L., Leong, J., and Van den Helm, D., 1981, Structure of ferric pseudobactin, a siderophore from a plant growth promoting Pseudomonas, Biochemistry 20:6446–6457.PubMedCrossRefGoogle Scholar
  75. Torres, L., Perez-Ortin, J. E., Tordera, V., and Beltran, J. P., 1986, Isolation and characterization of an Fe(III)-chelating compound produced by Pseudomonas syringae, Appl. Environ. Microbiol. 52:157–160.PubMedGoogle Scholar
  76. Trick, C. G., Andersen, R. J., Gillam, A., and Harrison, P. J., 1983, Prorocentrin: an extracellular siderophore produced by the marine dinoflagellate.Science 219:306–308.PubMedCrossRefGoogle Scholar
  77. Vandenbergh, P. A., Gonzalez, C. F., Wright, A. M., and Kunka, B. S., 1983, Iron-chelating compounds produced by soil pseudomonads: Correlation with fungal growth inhibition, Appl. Environ. Microbiol. 46:128–132.PubMedGoogle Scholar
  78. Warren, R. A. J., and Neilands, J. B., 1965, Mechanism of microbial catabolism of ferri- chrome A, J. Biol. Chem. 240:2055–2058.PubMedGoogle Scholar
  79. Wehrii, W., and Staehelin, M., 1971, Actions of the rifamycin, Bacteriol. Rev. 35:290–309.Google Scholar
  80. Wendenbaum, S., Demange, P., Dell, A., Meyer, J. M., and Abdallah, M. A., 1983, The structure of pyoverdine Pa, the siderophore of Pseudomonas aeruginosa, Tetrahedron Lett. 24:4877–4880.CrossRefGoogle Scholar
  81. Winkelmann, G., 1979, Surface iron polymers and hydroxy acids. A model of iron supply in sideramine-free fungi, Arch. Mikrobiol 121:43–51.Google Scholar
  82. Winkelmann, G., 1985, Specificity of siderophore iron uptake by fungi, in:The Biological Chemistry of Iron (H. B. Dunford, D. Dolphin, K. N. Raymond, and L. Sieker, eds.), pp. 107–116, D. Reidel, Dordrecht.Google Scholar
  83. Yang, C. C., and Leong, J., 1984, Structure of Pseudobactin 7SR1, a siderophore from a plant deleterious Pseudomonas, Biochemistry 23:3534–3540.PubMedCrossRefGoogle Scholar
  84. Zähner, H., Keller-Schierlein, W., Hutter, R., Hess-Leisinger, K., and Deer, A., 1963, Stoff- wechselprodukte van Mikroorganismen: 40. Mitteilung. Sideramine aus Äspergillaceen, Arch. Mikrobiol 45:119–135.CrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1988

Authors and Affiliations

  • P. Bossier
    • 1
  • M. Hofte
    • 1
  • W. Verstraete
    • 1
  1. 1.Laboratory of Microbial EcologyUniversity of GhentGhentBelgium

Personalised recommendations