Skip to main content
Log in

Identification of a fungal triacetylfusarinine C siderophore transport gene (TAF1) in Saccharomyces cerevisiae as a member of the major facilitator superfamily

  • Published:
Biometals Aims and scope Submit manuscript

Abstract

Transport proteins of microorganisms may either belong to the ATP-binding cassette (ABC) superfamily or to the major facilitator (MFS)-superfamily. MFS transporters are single-polypeptide membrane transporters that transport small molecules via uniport, symport or antiport mechanisms in response to a chemiosmotic gradient. Although Saccharomyces cerevisiae is a non-siderophore producer, various bacterial and fungal siderophores can be utilized as an iron source. From yeast genome sequencing data six genes of the unknown major facilitator (UMF) family were known of which YEL065w Sce was recently identified as a transporter for the bacterial siderophore ferrioxamine B (Sit1p). The present investigation shows that another UMF gene, YHL047c Sce, encodes a transporter for the fungal siderophore triacetylfusarinine C. The gene YHL047c Sce (designated TAF1) was disrupted using the kanMX disruption module in a fet3 background (strain DEY 1394 Δfet3), possessing a defect in the high affinity ferrous iron transport. Growth promotion assays and transport experiments with 55Fe-labelled triacetylfusarinine C showed a complete loss of iron utilization and uptake in the disrupted strain, indicating that TAF1 is the gene for the fungal triacetylfusarinine transport in Saccharomyces cerevisiae and possibly in other siderophore producing fungi.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adjimani JP, Emery T. 1987 Iron uptake in Mycelia sterilia EP-76. J Bacteriol 169, 3664-3668.

    Google Scholar 

  • Anke H. 1977 Metabolic products of microorganisms 163. Desferritriacetylfusigen, an antibiotic from Aspergillus deflectus. J Antbiotics 30, 125-128.

    Google Scholar 

  • Askwith CC, De Silva D, Kaplan J. 1996 Molecular biology of iron acquisition in Saccharomyces cerevisiae. Molec Microbiol 20, 27-34.

    Google Scholar 

  • Braun V, Hantke K. 1997 Receptor-mediated bacterial iron transport. In: Winkelmann G, Carrano CJ, eds. Transition Metals in Microbial Metabolism Amsterdam, Harwood Academic Publisher.

    Google Scholar 

  • Carrano C, Thieken A, Winkelmann G. 1996 Specificity and mechanism of rhizoferrin mediated metal ion uptake. BioMetals 9, 185-189.

    Google Scholar 

  • Dancis A, Klausner RD, Hinnebusch AG, Barriocanal JG. 1990 Genetic evidence that ferric reductase is required for iron uptake in Saccharomyces cerevisiae. Mol Cell Biol 10, 2294-2301.

    Google Scholar 

  • Deiss K, Hantke K, Winkelmann G. 1998 Molecular recognition of siderophores: A study with cloned ferrioxamine receptors (FoxA) from Erwinia herbicola and Yersinia enterocolitica. BioMetals 11, 131-137.

    Google Scholar 

  • Diekmann H, Zähner H. 1967 Konstitution von Fusigen und dessen Abbau zu Δ2-Anhydromevalonsäurelacton. Eur J Biochem 3, 213-218.

    Google Scholar 

  • Diekmann H, Krezdorn E. 1975 Stoffwechselprodukte von Mikroorganismen. 150. Mitteilung Ferricrocin, Triacetylfusigen und andere Sideramine aus Pilzen der Gattung Aspergillus, Gruppe Fumigatus. Arch Microbiol 106, 191-194.

    Google Scholar 

  • Drechsel H, Winkelmann G. 1997 Iron chelation and siderophores. In: Transition Metals in Microbial Metabolism, Amsterdam, Harwood Academic Publishers, 1-49.

    Google Scholar 

  • Eng-Wilmot DL, Adjimani JP, Van der Helm D. 1992 Siderophore-mediated iron(III) transport in the mycelia of the cultivated fungus Agaricus bisporus. J Inorg Chem 48, 183-195.

    Google Scholar 

  • Goffeau A, Park J, Paulsen IT, Jonniaux J-L, Dinh T, Mordant P, Saier MH. 1997 Multidrug-resistant transport proteins in yeast: complete inventory and phylogenetic characterization of yeast open reading frames within the major facilitator superfamily. Yeast 13, 43-54.

    Google Scholar 

  • Güldener U, Heck S, Fiedler T, Beinhauer J, Hegemann JH. 1996 A new efficient gene disruption cassette for repeated use in budding yeast. Nucl Acid Res 24, 2519-2524.

    Google Scholar 

  • Haselwandter K, Dobernigg B, Beck W, Jung G, Cansier A, Winkelmann G. 1992 Isolation and identification of hydroxamate siderophores of ericoid mycorrhizal fungi. BioMetals 5, 51-56.

    Google Scholar 

  • Heymann P, Ernst JF, Winkelmann G. 1999 Functional assignment of the unknown facilitator superfamily genes as membrane tranporter genes for fungal ferrichromes in Saccharomyces cerevisiae (submitted).

  • Howard DH. 1999 Acquisition, transport and storage of iron by pathogenic fungi. Clin Microbiol Rev 12, 394-404.

    Google Scholar 

  • Huschka H, Winkelmann G. 1984 A study on the mechanism of siderophore transport-a proton symport. J Plant Nutr 7, 479-487.

    Google Scholar 

  • Huschka, H. and Winkelmann, G. 1989 Iron limitation and its effect on membrane proteins and siderophore transport in Neurospora crassa. BioMetals 2, 108-113.

    Google Scholar 

  • Huschka H, Müller G, Winkelmann G. 1983 The membrane potential is the driving force for siderophore iron transport in fungi. FEMS Microbiol Lett 20, 125-129.

    Google Scholar 

  • Huschka H, Naegeli HU, Leuenberger-Ryf H, Keller-Schierlein W, Winkelmann G. 1985 Evidence for a common siderophore transport system but different siderophore receptors in Neurospora crassa. J Bacteriol. 162, 715-721.

    Google Scholar 

  • Huschka H, Jalal MAF, Van der Helm D, Winkelmann G. 1986 Molecular recognition of siderophores in fungi: Role of iron-surrounding N-acyl residues and the peptide backbone during membrane transport in Neurospora crassa. J Bacteriol 167, 1020-1024

    Google Scholar 

  • Hossain MB, Eng-Wilmot DL, Loghry RA, Van der Helm D. 1980 Circular dichroism, crystal stucture, and absolute configuration of the siderophore ferric N, N′, N″-triacetylfusarinine, FeC39H57N6O15. J Am Chem Soc 102, 5766-5773.

    Google Scholar 

  • Konetschny-Rapp S, Huschka H, Winkelmann G. 1988 High-performance liquid chromatography of siderophores from fungi. BioMetals 1, 9-17.

    Google Scholar 

  • Lesuisse E, Labbe P. 1994 Reductive iron assimilation in Saccharomyces cerevisiae. In: Metal Ions in Fungi Winkelmann G, Winge DR, eds. New York, Marcel Dekker Inc., 149-178.

    Google Scholar 

  • 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, 3455-3462.

    Google Scholar 

  • Leong SA, Winkelmann G. 1998 Molecular biology of iron transport in fungi. In: Sigel H, Sigel A, eds. Metal Ions in Biological Systems, Vol. 35. New York, Marcel dekker, Inc.

    Google Scholar 

  • Münzinger M, Taraz K, Budzikiewics H, Drechsel H, Heymann P, Winkelmann g, Meyer J-M. 1999 S,S-Rhizoferrin (enantiorhizoferrin) — a siderophore of Ralstonia (Pseudomonas) pickettii DSM 6297 — the optical antipode of R,R-Rhizoferrin isolated from fungi. BioMetals 12, 189-193.

    Google Scholar 

  • Neilands JB, Konopka K, Schwyn B, Coy M, Francis RT, Paw BH, Bagg A. 1987 Comparative Biochemistry of microbial iron assimilation. In: Winkelmann G, Van der Helm D, Neilands JB, eds. Iron Transport in Microbes, Plants and Animals VCH 1997, 3-33.

  • Pao SS, Paulsen IT, Saier MH Jr. 1998 Major facilitator superfamily. Microbiol Molec Biol Rev 62, 1-34.

    Google Scholar 

  • Sayer JM, Emery T. 1968 Structures of naturally occuring hydroxamic acids, fusarinine A and B. Biochemistry 7, 184-190.

    Google Scholar 

  • Van der Helm D, Winkelmann G. 1994 Hydroxamates and polycarboxylates as iron transport agents (siderophores) in fungi. In: Winkelmann G, Winge DR, eds. Metal Ions in Fungi New York, Marcel Dekker, Inc. 39-98.

    Google Scholar 

  • Wach A, Brachat A, Pohlmann R, Philippsen P. 1994 New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10, 1793-1808.

    Google Scholar 

  • Wiebe C, Winkelmann G. 1975 Kinetic studies on the specificity of chelate-iron uptake in Aspergillus. Arch Microbiol 123, 837-842.

    Google Scholar 

  • Winkelmann G. 1979 Evidence for stereospecific uptake of iron chelates in fungi. FEBS Lett. 97, 43-46.

    Google Scholar 

  • Winkelmann G, Braun V. 1981 Stereoselective recognition of ferrichrome by fungi and bacteria. FEMS Microbiol Lett 11, 237-241.

    Google Scholar 

  • Winkelmann, G. (ed.) 1991 Handbook of Microbial Iron Chelates. Boca Raton, CRC Press Inc., FL.

    Google Scholar 

  • Winkelmann G. 1993 Kinetics, energetics, and mechanisms of siderophore iron transport in fungi. In: Barton LL, Hemming BC, eds. Iron Chelation in Plants and Soil Organisms New York, Academic Press, 219-239.

    Google Scholar 

  • Winkelmann G, Winge DR (eds.) 1994 Metal Ions in Fungi. New York, Marcel Dekker, Inc.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Heymann, P., Ernst, J.F. & Winkelmann, G. Identification of a fungal triacetylfusarinine C siderophore transport gene (TAF1) in Saccharomyces cerevisiae as a member of the major facilitator superfamily. Biometals 12, 301–306 (1999). https://doi.org/10.1023/A:1009252118050

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1009252118050

Navigation