Skip to main content

Advertisement

SpringerLink
Log in

The fate of siderophores: antagonistic environmental interactions in exudate-mediated micronutrient uptake

  • Published:
BioMetals Aims and scope Submit manuscript

Abstract

Organisms acquire metals from the environment by releasing small molecules that solubilize and promote their specific uptake. The best known example of this nutrient uptake strategy is the exudation of siderophores, which are a structurally-diverse class of molecules that are traditionally viewed as being integral to iron uptake. Siderophores have been proposed to act through a variety of processes, but their effectiveness can be mitigated by a variety of chemical and physical processes of both biotic and abiotic origin. Processes that occur at the surface of minerals can degrade or sequester siderophores, preventing them from fulfilling their function of returning metals to the organism. In addition, biotic processes including enzymatic degradation of the siderophore and piracy of the metal or of the siderophore complex also disrupt iron uptake. Some organisms have adapted their nutrient acquisition strategies to address these potential pitfalls, producing multiple siderophores and other exudates that take advantage of varying kinetic and thermodynamic factors to allow the continued uptake of metals. A complete understanding of the factors that contribute to metal uptake in nature will require a concerted effort to study processes identified in laboratory systems in the context of more complicated environmental systems.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abergel RJ, Wilson MK, Arceneaux JEL, Hoette TM, Strong RK, Byers BR, Raymond KN (2006) Anthrax pathogen evades the mammalian immune system through stealth siderophore production. Proc Natl Acad Sci USA 103:18499–18503

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ahmed E, Holmstrom SJM (2014) The effect of soil horizon and mineral type on the distribution of siderophores in soil. Geochim Cosmochim Acta 131:184–195

    CAS  Google Scholar 

  • Akafia MM, Harrington JM, Bargar JR, Duckworth OW (2014) Metal oxyhydroxide dissolution as promoted by structurally diverse siderophores and oxalate. Geochimica et Cosmochimica Acta 141:258–269. doi:10.1016/j.gca.2014.06.024

    CAS  Google Scholar 

  • Albrecht-Gary AM, Crumbliss AL (1998) Coordination chemistry of siderophores: thermodynamics and kinetics of iron chelation and release. Met Ions Biol Syst 35:239–327

    CAS  PubMed  Google Scholar 

  • Amin SA, Green DH, Hart MC, Küpper FC, Sunda WG, Carrano CJ (2009) Photolysis of iron–siderophore chelates promotes bacterial–algal mutualism. Proc Natl Acad Sci 106:17071–17076. doi:10.1073/pnas.0905512106

    PubMed Central  CAS  PubMed  Google Scholar 

  • Baig BH, Wachsmuth IK, Morris GK (1986) Utilization of exogenous siderophores by Campylobacter species. J Clin Microbiol 23:431–433

    PubMed Central  CAS  PubMed  Google Scholar 

  • Barbeau K, Rue EL, Bruland KW, Butler A (2001a) Photochemical cycling of iron in the surface ocean mediated by microbial iron(III)-binding ligands. Nature 413:409–413

    CAS  PubMed  Google Scholar 

  • Barbeau K, Zhang G, Live DH, Butler A (2001b) Petrobactin, a Photoreactive siderophore produced by the oil-degrading marine bacterium Marinobacter hydrocarbonoclasticus. J Am Chem Soc 124:378–379. doi:10.1021/ja0119088

    Google Scholar 

  • Barbeau K, Rue EL, Trick CG, Bruland KW, Butler A (2003) Photochemical reactivity of siderophores produced by marine heterotrophic bacteria and cyanobacteria, based on characteristic Fe(III) binding groups. Limnol Oceanogr 48:1069

    CAS  Google Scholar 

  • Borer P, Kraemer SM, Sulzberger B, Hug SJ, Kretzschmar R (2009) Photodissolution of lepidocrocite (gamma-FeOOH) in the presence of desferrioxamine B and aerobactin. Geochim Cosmochim Acta 73:4673–4687

    CAS  Google Scholar 

  • Buss HL, Lüttge A, Brantley SL (2007) Etch pit formation on iron silicate surfaces during siderophore-promoted dissolution. Chem Geol 240:326–342

    CAS  Google Scholar 

  • Butler A, Martin JD (2005) The marine biogeochemistry of iron. In: Sigel A, Sigel H, Sigel RKO (eds) Metal ions in biological systems, vol 44., pp 21–46

    Google Scholar 

  • Butler A, Theisen RM (2010) Iron(III)-siderophore coordination chemistry: reactivity of marine siderophores. Coord Chem Rev 254:288–296

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cervini-Silva J, Sposito G (2002) Steady-state dissolution kinetics of aluminum-goethite in the presence of desferrioxamine-B and oxalate ligands. Environ Sci Technol 36:337–342

    CAS  PubMed  Google Scholar 

  • Cheah SF, Kraemer SM, Cervini-Silva J, Sposito G (2003) Steady-state dissolution kinetics of goethite in the presence of desferrioxamine B and oxalate ligands: Implications for the microbial acquisition of iron. Chem Geol 198:63–75

    CAS  Google Scholar 

  • Chuang CY et al (2013) Role of biopolymers as major carrier phases of Th, Pa, Pb, Po, and Be radionuclides in settling particles from the Atlantic Ocean. Mar Chem 157:131–143. doi:10.1016/j.marchem.2013.10.002

    CAS  Google Scholar 

  • Cocozza C, Tsao CCG, Cheah SF, Kraemer SM, Raymond KN, Miano TM, Sposito G (2002) Temperature dependence of goethite dissolution promoted by trihydroxamate siderophores. Geochim Cosmochim Acta 66:431–438

    CAS  Google Scholar 

  • Correnti C, Strong RK (2012) Mammalian siderophores, siderophore-binding lipocalins, and the labile iron pool. J Biol Chem 287:13524–13531

    PubMed Central  CAS  PubMed  Google Scholar 

  • Crichton R (2009) Iron Metabolism: From Molecular Mechanisms to Clinical Consequences, 3rd edn. Wiley, New York

    Google Scholar 

  • Crowley D (2000) Function of siderophores in the plant rhizosphere. In: Pinton R, Varanini Z, Nannipieri P (eds) The Rhizosphere. Dekker, New York, pp 223–261

    Google Scholar 

  • Crowley D (2007) Microbial siderophores in the plant rhizosphere. In: Barton LL, Abadia J (eds) Iron nutrition in plants and rhizospheric microorganisms. Springer, Dordrecht, pp 169–198

    Google Scholar 

  • Crumbliss AL, Harrington JM (2009) Iron sequestration by small molecules: thermodynamic and kinetic studies of natural siderophores and synthetic model compounds. In: van Eldik R (ed) Advances in inorganic chemistry, vol 61., pp 179–250

    Google Scholar 

  • Cullen JT, Bergquist BA, Moffett JW (2006) Thermodynamic characterization of the partitioning of iron between soluble and colloidal species in the Atlantic Ocean. Mar Chem 98:295–303. doi:10.1016/j.marchem.2005.10.007

    CAS  Google Scholar 

  • Dehner CA, Awaya JD, Maurice PA, Dubois JL (2010) Roles of siderophores, oxalate, and ascorbate in mobilization of iron from hematite by the aerobic bacterium pseudomonas mendocina. Appl Environ Microbiol 76:2041–2048

    PubMed Central  CAS  PubMed  Google Scholar 

  • Dhungana S, Crumbliss AL (2005) Coordination chemistry and redox processes in siderophore-mediated iron transport. Geomicrobiol J 22:87–98

    CAS  Google Scholar 

  • Dhungana S, White PS, Crumbliss AL (2003) Crystal and molecular structures of Ionophore–Siderophore host-guest supramolecular assemblies relevant to molecular recognition. J Am Chem Soc 125:14760–14767

    CAS  PubMed  Google Scholar 

  • Dhungana S, Anthony CR, Hersman LE (2007) Ferrihydrite dissolution by pyridine-2,6-bis(monothiocarboxylic acid) and hydrolysis products. Geochim Cosmochim Acta 71:5651–5660. doi:10.1016/j.gca.2007.07.022

    CAS  Google Scholar 

  • Duckworth OW, Sposito G (2005a) Siderophore-manganese(III) interactions I. Air-oxidation of manganese(II) promoted by desferrioxamine B. Environ Sci Technol 39:6037–6044

    CAS  PubMed  Google Scholar 

  • Duckworth OW, Sposito G (2005b) Siderophore-manganese(III) interactions II. Manganite dissolution promoted by desferrioxamine B. Environ Sci Technol 39:6045–6051

    CAS  PubMed  Google Scholar 

  • Duckworth OW, Bargar JR, Sposito G (2008) Sorption of ferric iron from ferrioxamine B to synthetic and biogenic layer type manganese oxides. Geochim Cosmochim Acta 72:3371–3380

    CAS  Google Scholar 

  • Duckworth OW, Bargar JR, Sposito G (2009a) Coupled biogeochemical cycling of iron and manganese as mediated by microbial siderophores. Biometals 22:605–613

    CAS  PubMed  Google Scholar 

  • Duckworth OW, Holmstrom SJM, Pena J, Sposito G (2009b) Biogeochemistry of iron oxidation in a circumneutral freshwater habitat. Chem Geol 260:149–158

    CAS  Google Scholar 

  • Duckworth OW, Jarzecki AA, Bargar JR, Oyerinde O, Spiro TG, Sposito G (2009c) An exceptionally stable cobalt(III)-desferrioxamine B complex. Marine Chem 113:114–122

    CAS  Google Scholar 

  • Duckworth OW, Akafia MM, Andrews MY, Bargar JR (2014) Siderophore-promoted dissolution of chromium from hydroxide minerals. Environ Sci 16:1348–1359

    CAS  Google Scholar 

  • Essén SA, Bylund D, Holmstrom SJM, Moberg M, Lundstrom US (2006) Quantification of hydroxamate siderophores in soil solutions of podzolic soil profiles in Sweden. Biometals 19:269–282. doi:10.1007/s10534-005-8418-8

    PubMed  Google Scholar 

  • Expert D (1999) Withholding and exchanging iron: Interactions between Erwinia spp. and their plant hosts. Annu Rev Phytopathol 37:307–334

    CAS  PubMed  Google Scholar 

  • Farkas E, Enyedy EA, Zekany L, Deak G (2001) Interaction between iron(II) and hydroxamic acids: oxidation of iron(II) to iron(III) by desferrioxamine B under anaerobic conditions. J Inorg Biochem 83:107–114

    CAS  PubMed  Google Scholar 

  • Farkas E, Enyedy EA, Fabian I (2003) New insight into the oxidation of Fe(II) by desferrioxamine B (DFB): spectrophotometric and capillary electrophoresis (CE) study. Inorg Chem Commun 6:131–134 (Pii S1387-7003(02)00703-7)

    CAS  Google Scholar 

  • Franke J, Ishida K, Hertweck C (2014) Evolution of siderophore pathways in human pathogenic bacteria. J Am Chem Soc 136:5599–5602

    CAS  PubMed  Google Scholar 

  • Garibaldi JA, Neilands JB (1956) Formation of iron-binding compounds by micro-organisms [5]. Nature 177:526–527

    CAS  PubMed  Google Scholar 

  • Gledhill M, Buck KN (2012) The organic complexation of iron in the marine environment: a review. Front Microbiol 3 doi:10.3389/fmicb.2012.00069

  • Gustafsson JP, Persson I, Kleja DB, Van Schaik JWJ (2007) Binding of iron(III) to organic soils: EXAFS spectroscopy and chemical equilibrium modeling. Environ Sci Technol 41:1232–1237. doi:10.1021/Es0615730

    CAS  PubMed  Google Scholar 

  • Harrington JM, Bargar JM, Jarzecki AA, Sombers LA, Roberts JG, Duckworth OW (2012) Trace metal complexation by the triscatecholate siderophore protochelin: structure and stability. Biometals 25:393–412

    CAS  PubMed  Google Scholar 

  • Harrison F, Paul J, Massey RC, Buckling A (2008) Interspecific competition and siderophore-mediated cooperation in Pseudomonas aeruginosa. ISME J 2:49–55

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Haselwandter K, Winkelmann G (2009) Siderophores of mycorrhizal fungi: Detection, isolation and identification. In: Varma A, Kharkwal AC (eds) Symbiotic fungi. Soil Biology series, vol 18. Springer, Berlin, pp 393–402

  • Haselwandter K et al (2006) Basidiochrome—a novel siderophore of the orchidaceous mycorrhizal fungi Ceratobasidium and Rhizoctonia spp. Biometals 19:335–343

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Haselwandter K, Häninger G, Ganzera M, Haas H, Nicholson G, Winkelmann G (2013) Linear fusigen as the major hydroxamate siderophore of the ectomycorrhizal Basidiomycota Laccaria laccata and Laccaria bicolor. Biometals 26:969–979

    CAS  PubMed  Google Scholar 

  • Hersman L, Maurice P, Sposito G (1996) Iron acquisition from hydrous Fe(III) -oxides by an aerobic Pseudomonas sp. Chem Geol 132:25–31

    CAS  Google Scholar 

  • Hesseltine CW, Pidacks C, Whitehill AR, Bohonos N, Hutchings BL, Williams JH (1952) Coprogen, a new growth factor for coprophilic fungi [1]. J Am Chem Soc 74:1362

    CAS  Google Scholar 

  • Hider RC, Kong X (2010) Chemistry and biology of siderophores. Natural Product Reports 27:637–657

    CAS  PubMed  Google Scholar 

  • Higashi RM, Fan TWM, Lane AN (1998) Association of desferrioxamine with humic substances and their interaction with cadmium(II) as studied by pyrolysis gas chromatography mass spectrometry and nuclear magnetic resonance spectroscopy. Analyst 123:911–918

    CAS  Google Scholar 

  • Hoffland E et al (2004) The role of fungi in weathering. Front Ecol Environ 2:258–264

    Google Scholar 

  • Holmen BA, Casey WH (1996) Hydroxamate ligands, surface chemistry, and the mechanism of ligand-promoted dissolution of goethite. Geochim Cosmochim Acta 60:4403–4416

    CAS  Google Scholar 

  • Holmen BA, Tejedor-Tejedor I, Casey WH (1997) Hydroxamate complexes in solution and at the goethite-water interface: a cylindrical internal reflection Fourier transform infrared spectroscopy study. Langmuir 13:2197–2206

    CAS  Google Scholar 

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

    Google Scholar 

  • Homann VV, Sandy M, Tincu JA, Templeton AS, Tebo BM, Butler A (2009) Loihichelins A-F, a suite of amphiphilic siderophores produced by the marine bacterium halomonas LOB-5. J Nat Prod 72:884–888

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hunter KA, Boyd PW (2007) Iron-binding ligands and their role in the ocean biochemistry of iron. Environ Chem 4:221–232

    CAS  Google Scholar 

  • Johnson L (2008) Iron and siderophores in fungal-host interactions. Mycol Res 112:170–183

    CAS  PubMed  Google Scholar 

  • Kim D, Duckworth OW, Strathmann TJ (2009) Hydroxamate siderophore-promoted reactions between iron(II) and nitroaromatic groundwater contaminants. Geochim Cosmochim Acta 73:1297–1311

    CAS  Google Scholar 

  • Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Pseudomonas siderophores: a mechanism explaining disease-suppressive soils. Curr Microbiol 4:317–320

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Kraemer SM, Duckworth OW, Harrington JM, Schenkeveld WDC (2014) Metallophores and trace metal biogeochemistry. Aquat Geochem, 1–37

  • Kraepiel AML, Bellenger JP, Wichard T, Morel FMM (2009) Multiple roles of siderophores in free living nitrogen fixing bacteria. Biometals 22:573–581. doi:10.1007/s10534-009-9222-7

    CAS  PubMed  Google Scholar 

  • Krewulak KD, Vogel HJ (2008) Structural biology of bacterial iron uptake. Biochimica et Biophysica Acta—Biomembr 1778:1781–1804

    CAS  Google Scholar 

  • Kuhn KM, Dehner CA, Dubois JL, Maurice PA (2012) Iron acquisition from natural organic matter by an aerobic pseudomonas mendocina bacterium: siderophores and cellular iron status. Geomicrobiol J 29:780–791. doi:10.1080/01490451.2011.619639

    CAS  Google Scholar 

  • Kuhn KM, Maurice PA, Neubauer E, Hofmann T, Von Der Kammer F (2014) Accessibility of humic-associated Fe to a microbial siderophore: implications for bioavailability. Environ Sci Technol 48:1015–1022

    CAS  PubMed  Google Scholar 

  • Leong SA, Winkelmann G (1998) Molecular biology of iron transport in fungi. Met Ions Biol Syst 35:147–186

    CAS  PubMed  Google Scholar 

  • Liermann LJ, Kalinowski BE, Brantley SL, Ferry JG (2000) Role of bacterial siderophores in dissolution of hornblende. Geochim Cosmochim Acta 64:587–602

    CAS  Google Scholar 

  • Loaces I, Ferrando L, Scavino AF (2011) Dynamics, diversity and function of endophytic siderophore-producing bacteria in rice. Microb Ecol 61:606–618

    PubMed  Google Scholar 

  • Loring JS, Simanova AA, Persson P (2008) Highly mobile iron pool from a dissolution-readsorption process. Langmuir 24:7054–7057. doi:10.1021/la800785u

    CAS  PubMed  Google Scholar 

  • Martin ST (2005) Precipitation and dissolution of iron and manganese oxides. In: Grassian VH (ed) Environmental catalysis. Marcel-Dekker, CRC Press, Boca Raton, pp 61–81

    Google Scholar 

  • Maurice P, Haack E, Mishra B (2009) Siderophore sorption to clays. Biometals 22:649–658. doi:10.1007/s10534-009-9242-3

    CAS  PubMed  Google Scholar 

  • Miethke M, Marahiel MA (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol Rev 71:413–451

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mishra B, Haack EA, Maurice PA, Bunker BA (2010) A spectroscopic study of the effects of a microbial siderophore on Pb adsorption to kaolinite. Chem Geol 275:199–207. doi:10.1016/j.chemgeo.2010.05.009

    CAS  Google Scholar 

  • Morris AJ, Hesterberg DL (2012) Iron(III) coordination and phosphate sorption in peat reacted with ferric or ferrous iron. Soil Sci Soc Am J 76:101–109. doi:10.2136/sssaj2011.0097

    CAS  Google Scholar 

  • Muller G, Raymond KN (1984) Specificity and mechanism of ferrioxamine-mediated iron transport in Streptomyces pilosus. J Bacteriol 160:304–312

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nannipieri P, Kandeler E, Ruggiero P (2002) Enzyme activities and microbiological and biochemical processes in soil. In: Burns RG, Dick RP (eds) Enzymes in the environment: activity, ecology, and applications. Dekker, New York, pp 1–33

    Google Scholar 

  • Neilands JB (1952) A crystalline organo-iron pigment from a rust fungus (Ustilago sphaerogena). J Am Chem Soc 74:4846–4847

    CAS  Google Scholar 

  • Neubauer U, Nowack B, Furrer G, Schulin R (2000) Heavy metal sorption on clay minerals affected by the siderophore desferrioxamine B. Environ Sci Technol 34:2749–2755

    CAS  Google Scholar 

  • Oide S, Moeder W, Krasnoff S, Gibson D, Haas H, Yoshioka K, Turgeon BG (2006) NPS6, encoding a nonribosomal peptide synthetase involved in siderophore-mediated iron metabolism, is a conserved virulence determinant of plant pathogenic ascomycetes. Plant Cell 18:2836–2853

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pierwola A, Krupinski T, Zalupski P, Chiarelli M, Castignetti D (2004) Degradation pathway and generation of monohydroxamic acids from the trihydroxamate siderophore deferrioxamine B. Appl Environ Microbiol 70:831–836

    PubMed Central  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Ratledge C, Dover LG (2000) Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54:881–941

    CAS  PubMed  Google Scholar 

  • Reichard PU, Kretzschmar R, Kraemer SM (2007a) Dissolution mechanisms of goethite in the presence of siderophores and organic acids. Geochim Cosmochim Acta 71:5635–5650

    CAS  Google Scholar 

  • Reichard PU, Kretzschmar R, Kraemer SM (2007b) Rate laws of steady-state and non-steady-state ligand-controlled dissolution of goethite. Colloids and Surfaces a-Physicochemical and Engineering Aspects 306:22–28. doi:10.1016/j.colsurfa.2007.03.001

    CAS  Google Scholar 

  • Renshaw JC, Robson GD, Trinci APJ, Wiebe MG, Livens FR, Collison D, Taylor RJ (2002) Fungal siderophores: Structures, functions and applications. Mycol Res 106:1123–1142

    CAS  Google Scholar 

  • Robin A, Vansuyt G, Hinsinger P, Meyer JM, Briat JF, Lemanceau P (2008) Iron Dynamics in the Rhizosphere: Consequences for Plant Health and Nutrition. In: Sparks DL (ed) Advances in Agronomy, vol 99, 1st edn., Briat JFAcademic Press, Oxford, pp 183–225

    Google Scholar 

  • Romheld V (1991) The role of phytosiderophores in acquisition of iron and other micronutrients in gramineous species—an ecological approach. Plant Soil 130:127–134

    Google Scholar 

  • Rosconi F et al (2013) Identification and structural characterization of serobactins, a suite of lipopeptide siderophores produced by the grass endophyte Herbaspirillum seropedicae. Environ Microbiol 15:916–927

    CAS  PubMed  Google Scholar 

  • Saal LB, Duckworth OW (2010) Synergistic dissolution of manganese oxides as promoted by siderophores and small organic acids. Soil Sci Soc Am J 74:2021–2031

    CAS  Google Scholar 

  • Schalk IJ, Hannauer M, Braud A (2011) New roles for bacterial siderophores in metal transport and tolerance. Environ Microbiol 13:2844–2854. doi:10.1111/j.1462-2920.2011.02556.x

    CAS  PubMed  Google Scholar 

  • Schenkeveld WDC, Oburger E, Gruber B, Schindlegger Y, Hann S, Puschenreiter M, Kraemer SM (2014) Metal mobilization from soils by phytosiderophores - experiment and equilibrium modeling. Plant Soil 383:59–71. doi:10.1007/s11104-014-2128-3

    PubMed Central  CAS  PubMed  Google Scholar 

  • Schrettl M et al (2004) Siderophore biosynthesis but not reductive iron assimilation is essential for Aspergillus fumigatus virulence. J Exp Med 200:1213–1219

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sia AK, Allred BE, Raymond KN (2013) Siderocalins: siderophore binding proteins evolved for primary pathogen host defense. Curr Opin Chem Biol 17:150–157

    PubMed Central  CAS  PubMed  Google Scholar 

  • Siebner-Freibach H, Hadar Y, Chen Y (2004) Interaction of iron chelating agents with clay minerals. Soil Sci Soc Am J 68:470–480

    CAS  Google Scholar 

  • Siebner-Freibach H, Hadar Y, Yariv S, Lapides I, Chen Y (2006) Thermospectroscopic study of the adsorption mechanism of the hydroxamic siderophore ferrioxamine B by calcium montmorillonite. J Agric Food Chem 54:1399–1408

    CAS  PubMed  Google Scholar 

  • Simanova AA, Persson P, Loring JS (2010) Hydrolysis of desferrioxamine-B at the surface of goethite in the dark at pH 6. Geochim Cosmochim Acta 74:A963

    Google Scholar 

  • Solinas V (1994) Cation effects on adsorption of desferrioxamine-B (DFOB) by humic acid. In: Sensei N, Miano TM (eds) Humic substances in the global environment and implications on human health. Elsevier, Amsterdam, pp 1183–1188

    Google Scholar 

  • Stintzi A, Barnes C, Xu J, Raymond KN (2000) Microbial iron transport via a siderophore shuttle: a membrane ion transport paradigm. Proc Natl Acad Sci USA 97:10691–10696

    PubMed Central  CAS  PubMed  Google Scholar 

  • Stumm W (1997) Reactivity at the mineral-water interface: dissolution and inhibition. Coll Surf A 120:143–166

    CAS  Google Scholar 

  • Sutton R, Sposito G (2005) Molecular Structure in Soil Humic Substances: The New View. Environ Sci Technol 39:9009–9015. doi:10.1021/es050778q

    CAS  PubMed  Google Scholar 

  • Thieme J, Kilcoyne D, Tyliszczak T, Haselwandter K (2013) Spatially resolved NEXAFS spectroscopy of siderophores in biological matrices. Journal of Physics: Conference Series 463

  • Tipping E, Rey-Castro C, Bryan SE, Hamilton-Taylor J (2002) Al(III) and Fe(III) binding by humic substances in freshwaters, and implications for trace metal speciation. Geochim Cosmochim Acta 66:3211–3224 (S0016-7037(02)00930-4)

    CAS  Google Scholar 

  • Traxler MF, Seyedsayamdost MR, Clardy J, Kolter R (2012) Interspecies modulation of bacterial development through iron competition and siderophore piracy. Mol Microbiol 86:628–644

    PubMed Central  CAS  PubMed  Google Scholar 

  • Valdebenito M, Crumbliss AL, Winkelmann G, Hantke K (2006) Environmental factors influence the production of enterobactin, salmochelin, aerobactin, and yersiniabactin in Escherichia coli strain Nissle 1917. Int J Med Microbiol 296:513–520

    CAS  PubMed  Google Scholar 

  • Villavicencio M, Neilands JB (1965) An inducible ferrichrome A-degrading peptidase from pseudomonas FC-1. Biochemistry 4:1092–1097

    CAS  PubMed  Google Scholar 

  • Von Wiren N, Khodr H, Hider RC (2000) Hydroxylated phytosiderophore species possess an enhanced chelate stability and affinity for iron(III). Plant Physiol 124:1149–1157

    Google Scholar 

  • Vraspir JM, Butler A (2009) Chemistry of marine ligands and siderophores. Annu Rev Mar Sci 1:43–63

    Google Scholar 

  • Vraspir JM, Holt PD, Butler A (2011) Identification of new members within suites of amphiphilic marine siderophores. Biometals 24:85–92

    PubMed Central  CAS  PubMed  Google Scholar 

  • Warren RA, Neilands JB (1964) Microbial degradation of the ferrichrome compounds. J Gen Microbiol 35:459–470

    CAS  PubMed  Google Scholar 

  • Warren RA, Neilands JB (1965) Mechanism of microbial catabolism of ferrichrome A. J Biol Chem 240:2055–2058

    CAS  PubMed  Google Scholar 

  • Winkelmann G (2002) Microbial siderophore-mediated transport. Biochem Soc Trans 30:691–696

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Winkelmann G, Busch B, Hartmann A, Kirchhof G, Süßmuth R, Jung G (1999) Degradation of desferrioxamines by Azospirillum irakense: assignment of metabolites by HPLC/electrospray mass spectrometry. Biometals 12:255–264

    CAS  PubMed  Google Scholar 

  • Xu C et al (2008) Colloidal cutin-like substances cross-linked to siderophore decomposition products mobilizing plutonium from contaminated soils. Environ Sci Technol 42:8211–8217

    CAS  PubMed  Google Scholar 

  • Zaya N, Roginsky A, Williams J, Castignetti D (1998) Evidence that a deferrioxamine B degrading enzyme is a serine protease. Can J Microbiol 44:521–527

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

OWD is grateful for support received from the National Science Foundation Geobiology and Low-Temperature Geochemistry Program (EAR-0921313).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Trace Inorganics Department, Technologies for Industry and the Environment, RTI International, Durham, NC, 27709, USA

    James M. Harrington

  2. Department of Soil Science, North Carolina State University, Raleigh, NC, 27695-7619, USA

    Owen W. Duckworth

  3. Department of Microbiology, University of Innsbruck, Technikerstr. 25, 6020, Innsbruck, Austria

    Kurt Haselwandter

Authors
  1. James M. Harrington
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Owen W. Duckworth
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kurt Haselwandter
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to James M. Harrington.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Harrington, J.M., Duckworth, O.W. & Haselwandter, K. The fate of siderophores: antagonistic environmental interactions in exudate-mediated micronutrient uptake. Biometals 28, 461–472 (2015). https://doi.org/10.1007/s10534-015-9821-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10534-015-9821-4

Keywords

Search

Navigation