, Volume 22, Issue 4, pp 625–632 | Cite as

Siderophore production by marine-derived fungi

  • Brian Holinsworth
  • Jessica D. MartinEmail author


Siderophore production by marine-derived fungi has not been extensively explored. Three studies have investigated the ability of marine-derived fungi to produce siderophores in response to iron limitation [(Vala et al. in Indian J Mar Sci 29:339–340, 2000; Can J Microbiol 52:603–607, 2006); Baakza et al. in J Exp Mar Biol Ecol 311:1–9, 2004]. In all, 24 of 28 marine fungal strains were found to secrete hydroxamate or carboxylate siderophores; no evidence was found for production of catecholate siderophores. These studies did not determine the structures of the iron-binding compounds. More recently, a study of the natural products secreted by a marine Penicillium bilaii revealed that this strain produced the rare catecholate siderophore pistillarin when grown under relatively high iron concentrations (Capon et al. J Nat Prod 70:1746–1752, 2007). Additionally, the production of rhizoferrin by a marine isolate of Cunninghamella elegans (ATCC36112) is reported in this manuscript. The current state of knowledge about marine fungal siderophores is reviewed in light of these promising results.


Siderophores Fungi Marine 



This publication was made possible by Grant Number P2PRR016478 from the National Center for Research Resources (NCRR), a component of the National Institutes of Health (NIH). Its contents are solely the responsibility of the authors and do not necessarily represent the official views of NCRR or NIH. NMR data were collected at the Oklahoma State University Statewide shared NMR facility. Special thanks to Prof. Alison Butler for conducting the mass spectral analyses.


  1. Adjimani JP, Emery T (1987) Iron uptake in Mycelia sterilia EP-76. J Bacteriol 169:3664–3668PubMedGoogle Scholar
  2. Adjimani JP, Emery T (1988) Stereochemical aspects of iron transport in Mycelia sterilia EP-76. J Bacteriol 170:1377–1379PubMedGoogle Scholar
  3. Ardon O, Weizman H, Libman J et al (1997) Iron uptake in Ustilago maydis: studies with fluorescent ferrichrome analogues. Microbiology 143:3625–3631CrossRefGoogle Scholar
  4. Ardon O, Nudelman R, Caris C et al (1998) Iron uptake in Ustilago maydis: tracking the iron path. J Bacteriol 180:2021–2026PubMedGoogle Scholar
  5. Baakza A, Vala AK, Dave BP et al (2004) A comparative study of siderophore production by fungi from marine and terrestrial habitats. J Exp Mar Biol Ecol 311:1–9CrossRefGoogle Scholar
  6. Barbeau K, Zhang G, Live DH, Butler A (2002) Petrobactin, a photoreactive siderophore produced by the oil-degrading marine bacterium Marinobacter hydrocarbonoclasticus. J Am Chem Soc 124:378–379PubMedCrossRefGoogle Scholar
  7. Bergeron RJ, Huang G, Smith RE et al (2003) Total synthesis and structure revision of petrobactin. Tetrahedron 59:2007–2014CrossRefGoogle Scholar
  8. Capon RJ, Stewart M, Ratnayake R et al (2007) Citromycetins and bilains A-C: new aromatic polyketides and diketopiperazines from Australian marine-derived and terrestrial Penicillium spp. J Nat Prod 70:1746–1752PubMedCrossRefGoogle Scholar
  9. Cerniglia CE, Perry JJ (1973) Crude oil degradation by microorganisms isolated from the marine environment. Z Allg Mikrobiol 13:299–306PubMedCrossRefGoogle Scholar
  10. Dancis A, Roman DG, Anderson GJ et al (1992) Ferric reductase of Saccharomyces cerevisiae: molecular characterization, role in iron uptake and transcriptional control by iron. Proc Natl Acad Sci USA 89:3869–3873PubMedCrossRefGoogle Scholar
  11. Drechsel H, Metzger J, Freund S et al (1991) Rhizoferrin—a novel siderophore from the fungus Rhizopus microsporus var. rhizopodiformis. Biometals 4:238–243Google Scholar
  12. Drechsel H, Jung G, Winkelmann G (1992) Stereochemical characterization of rhizoferrin and identification of its dehydration products. Biometals 5:141–148CrossRefGoogle Scholar
  13. Ecker DJ, Passavant CW, Emery T (1982) Role of two siderophores in Ustilago sphaerogena regulation and biosynthesis and uptake mechanisms. Biochim Biophys Acta 720:242–249PubMedCrossRefGoogle Scholar
  14. Emery T (1971) Role of ferrichrome as a ferric ionophore in Ustilago maydis. Biochemistry 10:1483–1488PubMedCrossRefGoogle Scholar
  15. Fekete FA, Chandhoke V, Jellison J (1989) Iron-binding compounds produced by wood-decaying basidiomycetes. Appl Environ Microbiol 55:2720–2722PubMedGoogle Scholar
  16. Hickford SJ, Küpper FC, Zhang G et al (2004) Petrobactin sulfonate, a new siderophore produced by the marine bacterium Marinobacter hydrocarbonoclasticus. J Nat Prod 67:1897–1899PubMedCrossRefGoogle Scholar
  17. Ismail A, Bedell GW, Lupan DM (1985) Siderophore production by the pathogenic yeast Candida albicans. Biochem Biophys Res Commun 130:885–891PubMedCrossRefGoogle Scholar
  18. Jalal MAF, van der Helm D (1991) Isolation and structural identification of fungal siderophores. In: Winkelmann G (ed) CRC handbook of microbial iron chelates, 1st edn. CRC Press, Boca Raton, pp 235–270Google Scholar
  19. Jellison J, Chandhoke V, Goodell B, Fekete FA (1991) The isolation and immunolocalization of iron-binding compounds. Appl Microbiol Biotechnol 35:805–809CrossRefGoogle Scholar
  20. Johnson KS, Coale KH, Elrod VA et al (1994) Iron photochemistry in seawater from the equatorial Pacific. Mar Chem 46:319–334CrossRefGoogle Scholar
  21. Johnson KS, Gordon RM, Coale KH (1997) What controls dissolved iron concentrations in the world ocean? Mar Chem 57:137–161CrossRefGoogle Scholar
  22. Küpper FC, Carrano CJ, Kuhn J-U, Butler A (2006) Photoreactivity of iron(III)-aerobactin: photoproduct structure and iron(III) coordination. Inorg Chem 45:6028–6033PubMedCrossRefGoogle Scholar
  23. Lesuisse E, Labbe P (1994) Reductive iron assimilation in Saccharomyces cerevisiae. In: Winkelmann G, Winge DR (eds) Metal ions in fungi. Marcel Dekker, New York, pp 149–178Google Scholar
  24. Lesuisse E, Simon-Casteras M, Labbe P (1998) Siderophore-mediated iron uptake in Saccharomyces cerevisiae: the sit1 gene encodes a ferrioxamine B permease that belongs to the major facilitator superfamily. Microbiology 144:3455–3462PubMedCrossRefGoogle Scholar
  25. Martin JH (1990) Glacial-interglacial CO2 change: the iron hypothesis. Paleoceanography 5:1–13CrossRefGoogle Scholar
  26. Martin JH, Fitzwater SE (1988) Iron deficiency limits phytoplankton growth in the north-east Pacific subarctic. Nature 331:341–343CrossRefGoogle Scholar
  27. Martin JH, Gordon RM, Fitzwater SE (1991) The case for iron. Limnol Oceanogr 36:1793–1802Google Scholar
  28. Martin JH, Coale KH, Johnson KS et al (1994) Testing the iron hypothesis in ecosystems of the equatorial Pacific Ocean. Nature 371:123–129CrossRefGoogle Scholar
  29. Martin JD, Ito Y, Homann VV et al (2006) Structure and membrane affinity of new amphiphilic siderophores produced by Ochrobactrum sp. SP18. J Biol Inorg Chem 11:633–641PubMedCrossRefGoogle Scholar
  30. Moore JK, Doney SC, Glover DM et al (2001) Iron cycling and nutrient-limitation patterns in surface waters of the World Ocean. Deep Sea Res Pt II 49:463–507CrossRefGoogle Scholar
  31. Morel FMM, Price NM (2003) The biogeochemical cycles of trace metals in the oceans. Science 300:944–947PubMedCrossRefGoogle Scholar
  32. Morel FMM, Milligan AJ, Saito MA (2003) Marine bioinorganic chemistry: the role of trace metals in the oceanic cycles of major nutrients. In: Turekian KK, Holland HD (eds) Treatise on geochemistry. Elsevier Science Ltd, CambridgeGoogle Scholar
  33. Müller G, Barclay SJ, Raymond KN (1985a) The mechanism and specificity of iron transport in Rhodotorula pilmanae probed by synthetic analogs of rhodotorulic acid. J Biol Chem 260:13916–13920PubMedGoogle Scholar
  34. Müller G, Isowa Y, Raymond KN (1985b) Stereospecificity of siderophore-mediated iron uptake by Rhodotorula pilmanae as probed by enantiorhodotorulic acid and isomers of chromic rhodotorulate. J Biol Chem 260:13921–13926PubMedGoogle Scholar
  35. Munzinger M, Taraz K, Budzikiewicz H et al (1999) S, S-rhizoferrin (enantio-rhizoferrin)—a siderophore of Ralstonia (Pseudomonas) pickettii DSM 6297—the optical antipode of R, R-rhizoferrin isolated from fungi. Biometals 12:189–193CrossRefGoogle Scholar
  36. Neilands JB (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270:26723–26726PubMedGoogle Scholar
  37. O’Sullivan DW, Hanson AK, Miller WL et al (1991) Measurement of Fe(II) in surface water of the equatorial Pacific. Limnol Oceanogr 36:1727–1741CrossRefGoogle Scholar
  38. Renshaw JC, Robson GD, Trinci APJ et al (2002) Fungal siderophores: structures, functions and applications. Mycol Res 106:1123–1142CrossRefGoogle Scholar
  39. Sigel A, Sigel H (eds) (1998) Iron Transport and Storage in Microorganisms, Plants and Animals. Metal Ions in Biological Systems, vol 35. Marcel Dekker, New YorkGoogle Scholar
  40. Steglich W, Steffan B, Stroech K, Wolf M (1984) Pistillarin, a characteristic metabolite of Clavariadelphus pistillaris and several Ramaria species (Basidiomycetes). Z Naturforschung [C] 39C:10–12Google Scholar
  41. Templeton DM (2000) Molecular and cellular iron transport. Marcel Dekker, New YorkGoogle Scholar
  42. Thieken A, Winkelmann G (1992) Rhizoferrin: a complexone type siderophore of the mucorales and entomophthorales (Zygomycetes). FEMS Microbiol Lett 73:37–41PubMedCrossRefGoogle Scholar
  43. Vala AK, Vaidya SY, Dube HC (2000) Siderophore production by facultative marine fungi. Indian J Mar Sci 29:339–340Google Scholar
  44. Vala AK, Dave BP, Dube HC (2006) Chemical characterization and quantification of siderophores produced by marine and terrestrial aspergilli. Can J Microbiol 52:603–607PubMedCrossRefGoogle Scholar
  45. van der Helm D, Winkelmann G (1994) Hydroxamates and polycarboxylates as iron transport agents (siderophores) in fungi. In: Winkelmann G, Winge D (eds) Metal ions in fungi. Marcel Dekker, New York, pp 39–98Google Scholar
  46. Winkelmann G (1990) Structural and stereochemical aspects of iron transport in fungi. Biotechnol Adv 8:207–231PubMedCrossRefGoogle Scholar
  47. Winkelmann G, Huschka H (1987) Molecular recognition and transport of siderophores in fungi. In: Winkelmann G, van der Helm D, Neilands JB (eds) Iron transport in microbes, plants, animals. VCH, Weinheim, pp 317–336Google Scholar

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© Springer Science+Business Media, LLC. 2009

Authors and Affiliations

  1. 1.Department of Natural SciencesNortheastern State UniversityTahlequahUSA

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