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Linear fusigen as the major hydroxamate siderophore of the ectomycorrhizal Basidiomycota Laccaria laccata and Laccaria bicolor

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Abstract

A screening for siderophores produced by the ectomycorrhizal fungi Laccaria laccata and Laccaria bicolor in synthetic low iron medium revealed the release of several different hydroxamate siderophores of which four major siderophores could be identified by high resolution mass spectrometry. While ferricrocin, coprogen and triacetylfusarinine C were assigned as well as other known fungal siderophores, a major peak of the siderophore mixture revealed an average molecular mass of 797 for the iron-loaded compound. High resolution mass spectrometry indicated an absolute mass of m/z = 798.30973 ([M + H]+). With a relative error of Δ = 0.56 ppm this corresponds to linear fusigen (C33H52N6O13Fe; MW = 797.3). The production of large amounts of linear fusigen by these basidiomycetous mycorrhizal fungi may possibly explain the observed suppression of plant pathogenic Fusarium species. For comparative purposes Fusarium roseum was included in this study as a well known producer of cyclic and linear fusigen.

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References

  • Anke H, Kinn J, Bergquist K-E, Sterner O (1992) Production of siderophores by strains of the genus Trichoderma. Isolation and characterization of new lipophilic coprogen derivative, palmitoylcoprogen. Biometals 4:176–180

    Google Scholar 

  • Bartholdy BA, Berreck M, Haselwandter K (2001) Hydroxamate siderophore synthesis by Phialocephala fortinii, a typical dark septate fungal root endophyte. Biometals 14:33–42

    Article  PubMed  CAS  Google Scholar 

  • Blume HP, Brümmer GW, Schwertmann U, Horn R, Kögel-Knabner I, Stahr K, Auerswald K, Beyer L, Hartmann A, Litz N, Scheinost A, Stanjek H, Welp G, Wilke BM (2002) Lehrbuch der bodenkunde. Spektrum Akademischer Verlag, Heidelberg

    Google Scholar 

  • Cornell RM, Schwertmann U (1993) The iron oxides. Wiley-VCH, Weinheim

    Google Scholar 

  • Courty PE, Hoegger PJ, Kilaru S, Kohler A, Buée M, Garbaye J, Martin F, Kües U (2009) Phylogenetic analysis, genomic organization, and expression analysis of multi-copper oxidases in the ectomycorrhizal basidiomycete Laccaria bicolor. New Phytol 182:736–750

    Article  PubMed  CAS  Google Scholar 

  • Deml G, Voges K, Jung G, Winkelmann G (1984) Tetraglycylferrichrome—the first heptapeptide ferrichrome. FEBS Lett 173:53–57

    Article  CAS  Google Scholar 

  • Diekmann H (1967) Stoffwechselprodukte von Mikroorganismen. 56 Mitteilung. Fusigen—ein neues Sideramin aus Pilzen. Arch Microbiol 58:1–5

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Emery T (1976) Fungal ornithine esterases: relationship to iron transport. Biochemistry 15:2723–2728

    Article  PubMed  CAS  Google Scholar 

  • Essén SA, Bylund D, Holmström SJM, Moberg M, Lundström US (2006) Quantification of hydroxamate siderophores in soil solutions of podzolic profiles in Sweden. Biometals 19:269–282

    Article  PubMed  Google Scholar 

  • Gardes M, Mueller GM, Fortin JA, Kropp BR (1991a) Mitochondrial DNA polymorphisms in Laccaria bicolor, L. laccata, L proxima and L. amethystina. Mycol Res 95:206–216

    Article  Google Scholar 

  • Gardes M, White TJ, Fortin JA, Bruns TD, Taylor JW (1991b) Identification of indigenous and introduced symbiotic fungi in ECM by amplification of nuclear and mitochondrial ribosomal DNA. Can J Bot 69:180–190

    Article  CAS  Google Scholar 

  • Haas H (2003) Molecular genetics of fungal siderophore biosynthesis and uptake: the role of siderophores in iron uptake and storage. Appl Microbiol Biotechnol 62:316–330

    Article  PubMed  CAS  Google Scholar 

  • Haas H, Eisendle M, Turgeon BG (2008) Siderophores in fungal physiology and virulence. Annu Rev Phytopathol 46:149–187

    Article  PubMed  CAS  Google Scholar 

  • Harrington JM, Winkelmann G, Haselwandter K, Crumbliss AL (2011) Fe(III)-complexes of the tripodal trishydroxamate siderophore basidiochrome: potential biological implications. J Inorg Biochem 105:1670–1674

    Article  PubMed  CAS  Google Scholar 

  • Haselwandter K (1995) Mycorrhizal fungi: siderophore production. Crit Rev Biotechnol 15:287–291

    Article  CAS  Google Scholar 

  • Haselwandter K (2008) Structure and function of siderophores produced by mycorrhizal fungi. Mineral Mag 72:61–64

    Article  CAS  Google Scholar 

  • Haselwandter K, Bowen GD (1996) Mycorrhizal relations in trees for agroforestry and land rehabilitation. For Ecol Manage 81:1–17

    Article  Google Scholar 

  • Haselwandter K, Winkelmann G (1998) Identification and characterization of siderophores of mycorrhizal fungi. In: Varma A (ed) Mycorrhiza manual. Springer, Berlin, pp 243–254

    Chapter  Google Scholar 

  • Haselwandter K, Winkelmann G (2002) Ferricrocin—an ectomycorrhizal siderophore of Cenococcum geophilum. Biometals 15:73–77

    Article  PubMed  CAS  Google Scholar 

  • Haselwandter K, Winkelmann G (2007) Siderophores of symbiotic fungi. In: Chincholkar SB, Varma A (eds) Microbial Siderophores. Soil Biology Series.vol 12. Springer, Berlin, pp 91–103

  • Haselwandter K, Winkelmann G (2009) Siderophores of mycorrhizal fungi: detection, isolation and identification. In: Varma A (ed) Mycorrhiza manual, 2nd edn. Springer, Berlin, pp 393–402

    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

    Article  CAS  Google Scholar 

  • Haselwandter K, Passler V, Reiter S, Schmid DG, Nicholson G, Hentschel P, Albert K, Winkelmann G (2006) Basidiochrome—a novel siderophore of the orchidaceous mycorrhizal fungi Ceratobasidium and Rhizoctonia spp. Biometals 19:335–343

    Article  PubMed  CAS  Google Scholar 

  • Haselwandter K, Häninger G, Ganzera M (2011) Hydroxamate siderophores of the ectomycorrhizal fungi Suillus granulatus and S. luteus. Biometals 24:153–157

    Article  PubMed  CAS  Google Scholar 

  • Hoffland E, Kuyper TW, Wallander H, Plassard C, Gorbushina AA, Haselwandter K, Holmström S, Landeweert R, Lundström US, Rosling A, Sen R, Smits MM, van Hees PAW, van Breemen N (2004) The role of fungi in weathering. Front Ecol Environ 2:258–264

    Article  Google Scholar 

  • Holmström SJM, Lundström US, Finlay RD, van Hees PAW (2004) Siderophores in forest soil solution. Biogeochemistry 71(247–258):2004

    Google Scholar 

  • Hördt W, Römheld V, Winkelmann G (2000) Fusarinines and dimerum acid, mono- and dihydroxamate siderophores from Penicillium chrysogenum, improve iron utilization by strategy I and strategy II plants. Biometals 13:37–46

    Article  PubMed  Google Scholar 

  • Jalal MAF, Love SK, van der Helm D (1986) Siderophore mediated iron(III) uptake in Gliocladium virens. 1. Properties of cis-fusarinine, trans-fusarinine, dimerum acid, and their ferric complexes. J Inorg Chem 28:417–430

    CAS  Google Scholar 

  • Kraemer SM (2004) Iron oxide dissolution and solubility in the presence of siderophores. Aquat Sci 66:3–18

    Article  CAS  Google Scholar 

  • Kragl C, Schrettl M, Abt B, Sarg B, Lindner HH, Haas H (2007) EstB-mediated hydrolysis of the siderophore triacetylfusarinine C optimizes iron uptake of Aspergillus fumigatus. Eukaryot Cell 6:1278–1285

    Article  PubMed  CAS  Google Scholar 

  • Kropp BR, Mueller GM (1999) Laccaria. In: Cairney JWG, Chambers SM (eds) Ectomycorrhizal fungi. Springer, Berlin, pp 65–88

    Chapter  Google Scholar 

  • Landeweert R, Hoffland E, Finlay RD, Kuyper TW, van Breemen N (2001) Linking plants to rocks: ectomycorrhizal fungi mobilize nutrients from minerals. Trends Ecol Evol 16:248–254

    Article  PubMed  Google Scholar 

  • Leyval C, Berthelin J (1989) Interactions between Laccaria laccata, Agrobacterium radiobacter and beech roots: influence on P, K, Mg and Fe mobilization from minerals and plant growth. Plant Soil 117:103–110

    Article  CAS  Google Scholar 

  • Leyval C, Watteau F, Berthelin J, Reid CPPR (1992) Production of siderophores by ectomycorrhizal fungi. In: Mycorrhizas in Ecosystems. Cambridge: CAB International, pp 389–390

  • Martin F, Aerts A, Ahrén D, Brun A, Duchaussoy F et al (2008) The genome sequence of the basidiomycete fungus Laccaria bicolor provides insights into the mycorrhizal symbiosis. Nature 452:88–92

    Article  PubMed  CAS  Google Scholar 

  • Moore RE, Emery T (1976) N-acetylfusarinines: isolation, characterization and properties. Biochemistry 15:2719–2723

    Article  PubMed  CAS  Google Scholar 

  • Powell PE, Cline GR, Reid CPP, Szaniszlo PJ (1980) Occurrence of hydroxamate siderophore iron chelators in soils. Nature 287:833–834

    Article  CAS  Google Scholar 

  • Prabhu V, Biolchini PF, Boyer GL (1996) Detection and identification of ferricrocin produced by ectendomycorrhizal fungi in the genus Wilcoxina. Biometals 9:229–234

    Article  CAS  Google Scholar 

  • Sayer JM, Emery TF (1968) Structures of the naturally occurring hydroxamic acids, fusarinines A and B. Biochemistry 7:184–190

    Article  PubMed  CAS  Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    Article  PubMed  CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Elsevier, Amsterdam

    Google Scholar 

  • Stack RW, Sinclair WA (1975) Protection of Douglas-fir seedlings against Fusarium root rot by a mycorrhizal fungus in the absence of mycorrhiza formation. Phytopathology 65:468–472

    Article  Google Scholar 

  • Sylvia DM, Sinclair WA (1983a) Suppressive influence of Laccaria laccata on Fusarium oxysporum and on Douglas-fir seedlings. Phytopathology 73:384–389

    Article  Google Scholar 

  • Sylvia DM, Sinclair WA (1983b) Phenolic compounds and resistance to fungal pathogens induced in primary roots of Douglas-fir seedlings by the ectomycorrhizal fungus Laccaria laccata. Phytopathology 73:390–397

    Article  Google Scholar 

  • Szaniszlo PJ, Powell PE, Reid CPP, Cline GR (1981) Production of hydroxamate siderophore iron chelators by ectomycorrhizal fungi. Mycologia 73:1158–1174

    Article  CAS  Google Scholar 

  • Van Hees PA, Rosling A, Essén S, Godbold DL, Jones DL, Finlay RD (2006) Oxalate and ferricrocin exudation by the extramatrical mycelium of an ectomycorrhizal fungus in symbiosis with Pinus sylvestris. New Phytol 169:367–378

    Article  PubMed  Google Scholar 

  • Welzel K, Eisfeld K, Antelo L, Anke T, Anke H (2005) Characterization of the ferrichrome A biosynthetic gene cluster in the homobasidiomycete Omphalotus olearius. FEMS Microbiol Lett 249:157–163

    Article  PubMed  CAS  Google Scholar 

  • Winkelmann G (2007) Ecology of siderophores with special reference to the fungi. Biometals 20:379–392

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The dikaryotic parental strain S238N and the sib-monokaryotic S238N-H82 of L. bicolor (Maire) P.D. Orton were kindly provided by F. Martin, INRA-Nancy, F-54280 Champenoux.

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Haselwandter, K., Häninger, G., Ganzera, M. et al. Linear fusigen as the major hydroxamate siderophore of the ectomycorrhizal Basidiomycota Laccaria laccata and Laccaria bicolor . Biometals 26, 969–979 (2013). https://doi.org/10.1007/s10534-013-9673-8

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