Aquatic Geochemistry

, Volume 21, Issue 2–4, pp 159–195 | Cite as

Metallophores and Trace Metal Biogeochemistry

  • Stephan M. Kraemer
  • Owen W. Duckworth
  • James M. Harrington
  • Walter D. C. Schenkeveld
Original Paper


Trace metal limitation not only affects the biological function of organisms, but also the health of ecosystems and the global cycling of elements. The enzymatic machinery of microbes helps to drive critical biogeochemical cycles at the macroscale, and in many cases, the function of metalloenzyme-mediated processes may be limited by the scarcity of essential trace metals. In response to these nutrient limitations, some organisms employ a strategy of exuding metallophores, biogenic ligands that facilitate the uptake of metal ions. For example, bacterial, fungal, and graminaceous plant species are known to use Fe(III)-binding siderophores for nutrient acquisition, providing the best known and most thoroughly studied example of metallophores. However, recent breakthroughs have suggested or established the role of metallophores in the uptake of several other metallic nutrients. Furthermore, these metallophores may influence environmental trace metal fate and transport beyond nutrient acquisition. These discoveries have resulted in a deeper understanding of trace metal geochemistry and its relationship to the cycling of carbon and nitrogen in natural systems. In this review, we provide an overview of the current state of knowledge on the biogeochemistry of metallophores in trace metal acquisition, and explore established and potential metallophore systems.


Metallophore Siderophore Trace metals Nutrient uptake 



O.W.D. thanks the National Science Foundation Geobiology and Low-Temperature Geochemistry Program (EAR-0921313) and the North Carolina Agricultural Research Service (0223867 and 1001361) for support. SMK thanks the Austrian Science Fund (FWF): [P22798-B16] for support.

Supplementary material

10498_2014_9246_MOESM1_ESM.doc (72 kb)
Supplementary material 1 (DOC 72 kb)


  1. Abergel RJ, Warner JA, Shuh DK, Raymond KN (2006a) Enterobactin protonation and iron release: structural characterization of the salicylate coordination shift in ferric enterobactin. J Am Chem Soc J128:8920–8931Google Scholar
  2. Abergel RJ, Wilson MK, Arceneaux JEL, Hoette TM, Strong RK, Byers BR, Raymond KN (2006b) Anthrax pathogen evades the mammalian immune system through stealth siderophore production. Proc Natl Acad Sci USA 103:18499–18503Google Scholar
  3. Abergel RJ, Durbin PW, Kullgren B, Ebbe SN, Xu JD, Chang PY, Bunin DI, Blakely EA, Bjornstad KA, Rosen CJ, Shuh DK, Raymond KN (2010) Biomimetic actinide chelators: an update on the preclinical development of the orally active hydroxypyridonate decorporation agents 3,4,3-Li(1,2-HOPO) AND 5-LiO(Me-3,2-HOPO). Health Phys 99:401–407Google Scholar
  4. Adriano DC (2001) Trace elements in terrestrial environments: biogeochemistry, bioavailability, and risks of metals, 2nd edn. Springer, New YorkGoogle Scholar
  5. Ahmed E, Holmstrom SJM (2014) Siderophores in environmental research: roles and applications. Microbiol Biotechnol 7:196–208Google Scholar
  6. Akafia MM, Harrington JM, Duckworth OW (2014) Metal hydroxide dissolution as promoted by structurally diverse siderophores and oxalate. Geochim Cosmochim Acta 141:258–269Google Scholar
  7. Albrecht-Gary AM, Crumbliss AL (1998) Coordination chemistry of siderophores: thermodynamics and kinetics of iron chelation and release. Met Ions Biol Syst 35(35):239–327Google Scholar
  8. Ambundo EA, Deydier MV, Grall AJ, Aguera-Vega N, Dressel LT, Cooper TH, Heeg MJ, Ochrymowycz LA, Rorabacher DB (1999) Influence of coordination geometry upon copper(II/I) redox potentials. Physical parameters for twelve copper tripodal ligand complexes. Inorg Chem 38:4233–4242Google Scholar
  9. Anderegg G, L’Eplattenier F, Schwarzenbach G (1963) Hydroxamatkomplexe II. Die anwendung der pH-methode. Hel Chim Acta 46:1400–1408Google Scholar
  10. Andrews MY, Holmstrom SJM, Santelli CM, Duckworth OW (2014) Siderophore production by Mn oxidizing fungi. Goldschmidt, SacrametoGoogle Scholar
  11. Arai Y (2010) X-ray absorption spectroscopic investigation of molybdenum multinuclear sorption mechanism at the goethite-water interface. Environ Sci Technol 44:8491–8496Google Scholar
  12. Armstrong FA (2008) Why did nature choose manganese to make oxygen. Philos Trans R Soc Lond Ser B 363:1263–1270Google Scholar
  13. Balasubramanian R, Rosenzweig AC (2008) Copper methanobactin: a molecule whose time has come. Cur Opin Chem Biol 12:245–249Google Scholar
  14. Balasubramanian R, Kenney GE, Rosenzweig AC (2011) Dual pathways for copper uptake by methanotrophic bacteria. J Biol Chem 286:37313–37319Google Scholar
  15. Bandow NL, Gallagher WH, Behling L, Choi DW, Semrau JD, Hartsel SC, Gilles VS, DiSpirito AA (2011) Isolation of methanobactin from the spent media of methane-oxidizing bacteria. In: Rosenzweig AC, Ragsdale SW (eds) Methods in enzymology: methods in methane metabolism, vol 495., Elsevier, San Diego, pp 259–269Google Scholar
  16. Bandow N, Gilles VS, Freesmeier B, Semrau JD, Krentz B, Gallagher W, McEllistrem MT, Hartsel SC, Choi DW, Hargrove MS, Heard TM, Chesner LN, Braunreiter KM, Cao BV, Gavitt MM, Hoopes JZ, Johnson JM, Polster EM, Schoenick BD, Umlauf AM, DiSpirito AA (2012) Spectral and copper binding properties of methanobactin from the facultative methanotroph Methylocystis strain SB2. J Inorg Biochem 110:72–82Google Scholar
  17. Barron AR, Wurzburger N, Bellenger JP, Wright SJ, Kraepiel AML, Hedin LO (2009) Molybdenum limitation of asymbiotic nitrogen fixation in tropical forest soils. Nat Geosci 2:42–45Google Scholar
  18. Bartlett RJ (1988) Manganese redox reactions and organic interactions in soils. In: Graham RD, Hannam RJ, Uren NC (eds) Manganese in soils and plants. Kluwer, Dordrecht, pp 59–73Google Scholar
  19. Bartlett RJ, James BR (1993) Redox chemistry of soils. Adv Agron 50:151–209Google Scholar
  20. Barton LE, Quicksall AN, Maurice PA (2012) Siderophore-mediated dissolution of hematite (α-Fe2O3): effects of nanoparticle size. Geomicrobiol J 29:314–322Google Scholar
  21. Basiliko N, Yavitt JB (2001) Influence of Ni Co, Fe, and Na additions on methane production in Sphagnum-dominated Northern American peatlands. Biogeochemistry 52:133–153Google Scholar
  22. Batka D, Farkas E (2006) Pb(II)-binding capability of aminohydroxamic acids: primary hydroxamic acid derivatives of alpha-amino acids as possible sequestering agents for Pb(II). J Inorg Biochem 100:27–35Google Scholar
  23. Behling LA, Hartsel SC, Lewis DE, DiSpirito AA, Choi DW, Masterson LR, Veglia G, Gallagher WH (2008) NMR, mass spectrometry and chemical evidence reveal a different chemical structure for methanobactin that contains oxazolone rings. J Am Chem Soc 130:12604–12605Google Scholar
  24. Bellenger JP, Arnaud-Neu F, Asfari Z, Myneni SCB, Stiefel EI, Kraepiel AML (2007) Complexation of oxoanions and cationic metals by the biscatecholate siderophore azotochelin. J Biol Inorg Chem 12:367–376Google Scholar
  25. Bellenger JP, Wichard T, Kraepiel AML (2008a) Vanadium requirements and uptake kinetics in the dinitrogen-fixing bacterium Azotobacter vinelandii. Appl Environ Microbiol 74:1478–1484Google Scholar
  26. Bellenger JP, Wichard T, Kustka AB, Kraepiel AML (2008b) Uptake of molybdenum and vanadium by a nitrogen-fixing soil bacterium using siderophores. Nat Geosci 1:243–246Google Scholar
  27. Bellenger JP, Wichard T, Xu Y, Kraepiel AML (2011) Essential metals for nitrogen fixation in a free-living N2-fixing bacterium: chelation, homeostasis and high use efficiency. Environ Microbiol 13:1395–1411Google Scholar
  28. Bellenger JP, Xu Y, Zhang X, Morel FMM, Kraepiel AML (2014) Possible contribution of alternative nitrogenases to nitrogen fixation by asymbiotic N-2-fixing bacteria in soils. Soil Biol Biochem 69:413–420Google Scholar
  29. Bender M, Conrad R (1995) Effect of CH4 concentrations and soil conditions on the induction of CH4 oxidation activity. Soil Biol Biochem 27:1517–1527Google Scholar
  30. Bi YQ, Hesterberg DL, Duckworth OW (2010) Siderophore-promoted dissolution of cobalt from hydroxide minerals. Geochim Cosmochim Acta 74:2915–2925Google Scholar
  31. Biver M, Shotyk W (2012) Experimental study of the kinetics of ligand-promoted dissolution of stibnite (Sb2S3). Chem Geol 294:165–172Google Scholar
  32. Black A, McLaren RG, Reichman SM, Speir TW, Condron LM, Houliston G (2012) Metal bioavailability dynamics during a two-year trial using ryegrass (Lolium perenne L.) grown in soils treated with biosolids and metal salts. Soil Res 50:304–311Google Scholar
  33. Boer JL, Mulrooney SB, Hausinger RP (2014) Nickel-dependent metalloenzymes. Arch Biochem Biophys 544:142–152Google Scholar
  34. Boiteau RM, Fitzsimmons JN, Repeta DJ, Boyle EA (2013) Detection of iron ligands in seawater and marine cyanobacteria cultures by high-performance liquid chromatography-inductively coupled plasma-mass spectrometry. Anal Chem 85:4357–4362Google Scholar
  35. Borer PM, Sulzberger B, Reichard P, Kraemer SM (2005) Effect of siderophores on the light-induced dissolution of colloidal iron(III) (hydr)oxides. Marine Chem 93:179–193Google Scholar
  36. Borgias BA, Cooper SR, Koh YB, Raymond KN (1984) Synthetic, structural, and physical studies of titanium complexes of catechol and 3,5-di-tert-butylcatechol. Inorg Chem 23:1009–1016Google Scholar
  37. Boukhalfa H, Crumbliss AL (2002) Chemical aspects of siderophore mediated iron transport. Biometals 15:325–339Google Scholar
  38. Boukhalfa H, Reilly SD, Neu MP (2007) Complexation of Pu(IV) with the natural siderophore desferrioxamine B and the redox properties of Pu(IV)(siderophore) complexes. Inorg Chem 46:1018–1026Google Scholar
  39. Boye M, Nishioka J, Croot PL, Laan P, Timmermans KR, de Baar HJW (2005) Major deviations of iron complexation during 22 days of a mesoscale iron enrichment in the open Southern Ocean. Marine Chem 96:257–271Google Scholar
  40. Brainard JR, Strietelmeier BA, Smith PH, Langston-Unkefer PJ, Barr ME, Ryan RR (1992) Actinide binding and solubilization by microbial siderophores. Radiochim Acta 58:357–363Google Scholar
  41. Braud A, Hoegy F, Jezequel K, Lebeau T, Schalk IJ (2009) New insights into the metal specificity of the Pseudomonas aeruginosa pyoverdine-iron uptake pathway. Environ Microbiol 11:1079–1091Google Scholar
  42. Brown PH, Welch RM, Cary EE (1987) Nickel: amicronutrient essential for higher plants. Plant Physiol 85:801–803Google Scholar
  43. Bruland KW (1980) Oceanographic distributions of cadmium, zinc, nickel, and copper in the North Pacific. Earth Planet Sci Lett 47:176–198Google Scholar
  44. Budzikiewicz H, Georgias H, Taraz K (2002) Diastereomeric pyoverdin-chromium(III) complexes. Zeitschrift Fur Naturforschung C-a. J Biosci 57:954–956Google Scholar
  45. Buglyo P, Culeddu N, Kiss T, Micera G, Sanna D (1995) Vanadium (IV) and vanadium (V) complexes of desferrioxamine B in aqueous solution. J Inorg Biochem 60:45–49Google Scholar
  46. Bundy JG, Kille P, Liebeke M, Spurgeon DJ (2013) Metallothioneins may not be enough—the role of phytochelatins in invertebrate metal detoxification. Environ Sci Technol 48:885–886Google Scholar
  47. Butler A (1998) Acquisition and utilization of transition metal ions by marine organisms. Science 281:207–210Google Scholar
  48. Butler A, Carrano CJ (1991) Coordination chemistry of vanadium in biological systems. Coord Chem Rev 109:61–105Google Scholar
  49. Butler A, Martin JD (2005) The marine biogeochemistry of iron. Met Ions Biol Syst 44:21–46Google Scholar
  50. Butler A, Theisen RM (2010) Iron(III)-siderophore coordination chemistry: reactivity of marine siderophores. Coord Chem Rev 254:288–296Google Scholar
  51. Callahan DL, Baker AJM, Kolev SD, Wedd AG (2006) Metal ion ligands in hyperaccumulating plants. J Biol Inorg Chem 11:2–12Google Scholar
  52. Cameron V, Vance D (2014) Heavy nickel isotope composition in rivers and the oceans. Geochim Cosmochim Acta 128:195–211Google Scholar
  53. Cammack R (1988) A 3rd bacterial nitrogenase. Nature 333:595–596Google Scholar
  54. Campbell PGC (1995) Interactions between trace metals and aquatic organisms: a critique of the free-ion activity model, metal speciation and bioavailability in aquatic systems. Wiley, Chichester, pp 45–102Google Scholar
  55. Carrano CJ, Cooper SR, Raymond KN (1979) Coordination chemistry of microbial iron transport compounds.11. Solution equilibria and electrochemistry of ferric rhodotorulate complexes. J Am Chem Soc 101:599–604Google Scholar
  56. Carrano CJ, Drechsel H, Kaiser D, Jung G, Matzanke B, Winkelmann G, Rochel N, Albrecht-Gary AM (1996) Coordination chemistry of the carboxylate type siderophore rhizoferrin: the iron(III) complex and its metal analogues. Inorg Chem 35:6429–6436Google Scholar
  57. Carrasco N, Kretzschmar R, Pesch ML, Kraemer SM (2007) Low concentrations of surfactants enhance siderophore-promoted dissolution of goethite. Environ Sci Technol 41:3633–3638Google Scholar
  58. 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 36:337–342Google Scholar
  59. Chaney RL, Brown JC, Tiffin LO (1972) Obligatory reduction of ferric chelates in iron uptake by soybeans. Plant Physiol 50:208–213Google Scholar
  60. 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 198:63–75Google Scholar
  61. Cherrier MV, Martin L, Cavazza C, Jacquamet L, Lemaire D, Gaillard J, Fontecilla-Camps JC (2005) Crystallographic and spectroscopic evidence for high affinity binding of FeEDTA(H2O)- to the periplasmic nickel transporter NikA. J Am Chem Soc 127:10075–10082Google Scholar
  62. Cherrier MV, Cavazza C, Bochot C, Lemaire D, Fontecilla-Camps JC (2008) Structural characterization of a putative endogenous metal chelator in the periplasmic nickel transporter NikA. Biochemistry 47:9937–9943Google Scholar
  63. Chi Fru E, Gray ND, Mccann C, Baptista JDC, Christgen B, Talbot HM, El Ghazouani A, Dennison C, Graham DW (2011) Effects of copper mineralogy and methanobactin on cell growth and sMMO activity in Methylosinus trichosporium OB3b. Biogeosciences 8:2887–2894Google Scholar
  64. Chivers PT, Benanti EL, Heil-Chapdelaine V, Iwig JS (2012) Identification of Ni-(L-His)2 as a substrate for NikABCDE-dependent nickel uptake in Escherichia coli. Metallomics 4:1043–1050Google Scholar
  65. Choi DW, Do YS, Zea CJ, McEllistrem MT, Lee S-W, Semrau JD, Pohl NL, Kisting CJ, Scardino LL, Hartsel SC, Boyd ES, Geesey GG, Riedel TP, Shafe PH, Kranski KA, Tritsch JR, Antholine WE, DiSpirito AA (2006) Spectral and thermodynamic properties of Ag(I), Au(III), Cd(II), Co(II), Fe(III), Hg(II), Mn(II), Ni(II), Pb(II), U(IV), and Zn(II) binding by methanobactin from Methylosinus trichosporium OB3b. J Inorg Biochem 100:2150–2161Google Scholar
  66. Christenson EA, Schijf J (2011) Stability of YREE complexes with the trihydroxamate siderophore desferrioxamine B at seawater ionic strength. Geochim Cosmochim Acta 75:7047–7062Google Scholar
  67. 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 66:431–438Google Scholar
  68. Collins JM, Uppal R, Incarvito CD, Valentine AM (2005) Titanium(IV) citrate speciation and structure under environmentally and biologically relevant conditions. Inorg Chem 44:3431–3440Google Scholar
  69. Cornejo-Garrido H, Fernandez-Lomelin P, Guzman J, Cervini-Silva J (2008) Dissolution of arsenopyrite (FeAsS) and galena (PbS) in the presence of desferrioxamine-B at pH 5. Geochim Cosmochim Acta 72:2754–2766Google Scholar
  70. Cornelis R (2005) Handbook of elemental speciation II—species in the environment, food, medicine and occupational health. Wiley, HobokenGoogle Scholar
  71. Cornish AS, Page WJ (1995) Production of the tricatecholate siderophore protochelin by Azotobacter vinelandii. Biometals 8:332–338Google Scholar
  72. Cornish AS, Page WJ (2000) Role of molybdate and other transition metals in the accumulation of protochelin by Azotobacter vinelandii. Appl Environ Microbiol 66:1580–1586Google Scholar
  73. Cotton FA, Wilkinson G, Murrillo C, Bochmann M (1999) Advanced inorganic chemistry. Wiley, New YorkGoogle Scholar
  74. Croot PL, Moffett JW, Brand LE (2000) Production of extracellular Cu complexing ligands by eucaryotic phytoplankton in response to Cu stress. Limnol Oceanogr 45:619–627Google Scholar
  75. Crumbliss AL (1990) Iron bioavailability and the coordination chemistry of hydroxamic acids. Coordin Chem Rev 105:155–179Google Scholar
  76. Crumbliss AL, Harrington JM (2009) Iron sequestration by small molecules: thermodynamic and kinetic studies of natural siderophores and synthetic model compounds. Metal ion controlled reactivity. Adv Inorg Chem 61:179–250Google Scholar
  77. Cukrowski I, Cukrowska E, Hancock RD, Anderegg G (1995) The effect of chelate ring size on metal ion size-based selectivity in polyamine ligands containing pyridyl and saturated nitrogen donor groups. Anal Chim Acta 312:307–321Google Scholar
  78. Dahlheimer SR, Neal CR, Fein JB (2007) Potential mobilization of platinum-group elements by siderophores in surface environments. Environ Sci Technol 41:870–875Google Scholar
  79. Datta A, Raymond KN (2009) Gd–hydroxypyridinone (HOPO)-based high-relaxivity magnetic resonance imaging (MRI) contrast agents. Acc Chem Res 42:938–947Google Scholar
  80. Dhungana S, Harrington JM, Geblhardt P, Mollmann U, Crumbliss AL (2007) Iron chelation equilibria, redox, and siderophore activity of a saccharide platform ferrichrome analogue. Inorg Chem 46:8362–8371Google Scholar
  81. Dion HG, Mann PJG (1946) Three-valent manganese in soils. J Agric Sci 36:239–245Google Scholar
  82. DiSpirito AA, Zahn JA, Graham DW, Kim HJ, Larive CK, Derrick TS, Cox CD, Taylor A (1998) Copper-binding compounds from Methylosinus trichosporium OB3b. J Bacteriol 180:3606–3613Google Scholar
  83. Donat JR, Bruland KW (1995) Trace elements in the ocean. In: Salbu B, Steinnes E (eds) Trace elements in natural waters. CRC Press, Boca Raton, pp 247–281Google Scholar
  84. D’Onofrio A, Crawford JM, Stewart EJ, Witt K, Gavrish E, Epstein S, Clardy J, Lewis K (2010) Siderophores from neighboring organisms promote the growth of uncultured bacteria. Chem Biol 17:254–264Google Scholar
  85. Dosanjh NS, Michel SLJ (2006) Microbial nickel metalloregulation: NikRs for nickel ions. Curr Opin Chem Biol 10:123–130Google Scholar
  86. Duckworth OW, Sposito G (2005a) Siderophore-manganese(III) interactions II. Manganite dissolution promoted by desferrioxamine B. Environ Sci Technol 39:6045–6051Google Scholar
  87. Duckworth OW, Sposito G (2005b) Siderophore-manganese(III) interactions. I. Air-oxidation of manganese(II) promoted by desferrioxamine B. Environ Sci Technol 39:6037–6044Google Scholar
  88. Duckworth OW, Sposito G (2007) Siderophore-promoted dissolution of synthetic and biogenic layer type Mn oxides. Chem Geol 242:500–511Google Scholar
  89. 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 72:3371–3380Google Scholar
  90. Duckworth OW, Bargar JR, Sposito G (2009a) Coupled biogeochemical cycling of iron and manganese as mediated by microbial siderophores. Biometals 22:605–613Google Scholar
  91. Duckworth OW, Bargar JR, Sposito G (2009b) Quantitative-structure activity relationships for aqueous metal-siderophore complexes. Environ Sci Technol 43:343–349Google Scholar
  92. Duckworth OW, Jarzecki AA, Bargar JR, Oyerinde O, Spiro TG, Sposito G (2009c) An exceptionally stable cobalt(III)-desferrioxamine B complex. Marine Chem 113:114–122Google Scholar
  93. Duckworth OW, Akafia MM, Andrews MY, Bargar JR (2014) Siderophore-promoted dissolution of chromium from hydroxide minerals. Environ Sci Process Impacts 16:1348–1359Google Scholar
  94. Duhme AK, Hider RC, Khodr HH (1997) Synthesis and iron-binding properties of protochelin, the tris(catecholamide) siderophore of Azotobacter vinelandii. Chem Ber Recl 130:969–973Google Scholar
  95. Duhme AK, Hider RC, Naldrett MJ, Pau RN (1998) The stability of the molybdenum–azotochelin complex and its effect on siderophore production in Azotobacter vinelandii. J Biol Inorg Chem 3:520–526Google Scholar
  96. Duhme-Klair AK (2009) From siderophores and self-assembly to luminescent sensors: the binding of molybdenum by catecholamides. Eur J Inorg Chem 2009:3689–3701Google Scholar
  97. Dupont CL, Barbeau K, Palenik B (2008) Ni uptake and limitation in marine Synechococcus strains. Appl Environ Microbiol 74:23–31Google Scholar
  98. Edberg F, Kalinowski BE, Holmstrom SJM, Holm K (2010) Mobilization of metals from uranium mine waste: the role of pyoverdines produced by Pseudomonas fluorescens. Geobiology 8:278–292Google Scholar
  99. Egleston ES, Morel FMM (2008) Nickel limitation and zinc toxicity in a urea-grown diatom. Limnol Oceanogr 53:2462–2471Google Scholar
  100. El Ghazouani A, Basle A, Gray J, Graham DW, Firbank SJ, Dennison C (2012) Variations in methanobactin structure influences copper utilization by methane-oxidizing bacteria. Proc Natl Acad Sci USA 109:8400–8404Google Scholar
  101. Ellwood MJ, van Der Berg CMG (2001) Determination of organic complexation of cobalt in seawater by cathodic stripping voltammetry. Marine Chem 75:33–47Google Scholar
  102. Enyedy ÉA, Pócsi I, Farkas E (2004) Complexation of desferricoprogen with trivalent Fe, Al, Ga, In and divalent Fe, Ni, Cu, Zn metal ions: effects of the linking chain structure on the metal binding ability of hydroxamate based siderophores. J Inorg Biochem 98:1957–1966Google Scholar
  103. Eskew DL, Welch RM, Norwell WA (1984) Nickel in higher plants. Further evidence for an essential role. Plant Physiol 76:691–693Google Scholar
  104. Evangelou MWH, Ebel M, Schaeffer A (2007) Chelate assisted phytoextraction of heavy metals from soil. Effect, mechanism, toxicity, and fate of chelating agents. Chemosphere 68:989–1003Google Scholar
  105. Evers A, Hancock RD, Martell AE, Motekaitis RJ (1989) Metal ion recognition in ligands with negatively charged oxygen donor groups. Complexation of Fe(III), Ga(III), In(III), Al(III) and other highly charged ions. Inorg Chem 28:2189–2195Google Scholar
  106. Farkas E, Szabo O (2012) Co(II) and Co(III) hydroxamate systems: a solution equilibrium study. Inorganica Chimica Acta 30:354–361Google Scholar
  107. Farkas E, Buglyo P, Enyedy TA, Gerlei VA, Santos AM (2002) Factors affecting the metal ion-hydroxamate interactions: effect of the position of the peptide function in the connecting chain on the Fe(III), Mo(VI) and V(V) complexation of some new desferrioxamine B (DFB) model dihydroxamic acids. Inorg Chim Acta 339:215–223Google Scholar
  108. Farkas E, Csoka H, Toth I (2003) New insights into the solution equilibrium of molybdenum(VI)-hydroxamate systems: 1H and 17O NMR spectroscopic study of Mo(VI)-desferrioxamine B and Mo(VI)-monohydroxamic acid systems. Dalton Trans 2003:1645–1652Google Scholar
  109. Farkas E, Buglyo P, Enyedy EA, Santos MA (2004) Factors affecting the metal ion-hydroxamate interactions II: effect of the length of the connecting chain on the Fe(III), Mo(VI) and V(V) complexation of some new desferrioxamine B (DFB) model dihydroxamic acids. Inorg Chim Acta 357:2451–2461Google Scholar
  110. Farkas E, Batka D, Kremper G, Pocsi I (2008) Structure-based differences between the metal ion selectivity of two siderophores desferrioxamine B (DFB) and desferricoprogen (DFC): why DFC is much better Pb(II) sequestering agent than DFB? J Inorg Biochem 102:1654–1659Google Scholar
  111. Faulkner KM, Stevens RD, Fridovich I (1994) Characterization of Mn(III) complexes of linear and cyclic desferrioxamine as mimics of superoxide dismutase activity. Arch Biochem Biophys 310:341–346Google Scholar
  112. Foley TL, Simeonov A (2012) Targeting iron assimilation to develop new antibacterials. Expert Opin Drug Discov 7:831–847Google Scholar
  113. Fraústo da Silva JJR, Williams RJP (2001) The biological chemistry of the elements—the inorganic chemistry of life, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  114. Frazier SW, Kretzschmar R, Kraemer SM (2005) Bacterial siderophores promote dissolution of UO2 under reducing conditions. Environ Sci Technol 39:5709–5715Google Scholar
  115. Fukushima T, Allred BE, Sia AK, Nichiporuk R, Andersen UN, Raymond KN (2013) Gram-positive siderophore-shuttle with iron-exchange from Fe-siderophore to apo-siderophore by Bacillus cereus YxeB. Proc Natl Acad Sci USA 110:13821–13826Google Scholar
  116. Gärdes A, Triana C, Amin SA, Green DH, Romano A, Trimble L, Carrano CJ (2013) Detection of photoactive siderophore biosynthetic genes in the marine environment. Biometals 26:507–516Google Scholar
  117. Garibaldia JA, Neilands JB (1956) Formation of iron-binding compounds by micro-organisms. Nature 177:526–527Google Scholar
  118. Gledhill M, McCormack P, Ussher S, Achterbeg EP, Mantoura RFC, Worsfold PJ (2004) Production of siderophore type chelates by mixed bacterioplankton populations in nutrient enriched seawater incubations. Marine Chem 88:75–83Google Scholar
  119. Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374Google Scholar
  120. Gorden AEV, Xu JD, Raymond KN, Durbin P (2003) Rational design of sequestering agents for plutonium and other actinides. Chem Rev 103:4207–4282Google Scholar
  121. Graham DW, Kim HJ (2011) Production, isolation, purification, and functional characterization of methanobactins. In: Rosenzweig AC, Ragsdale SW (eds) Methods in enzymology: methods in methane metabolism, vol 495. Elsevier, San Diego, pp 227–245Google Scholar
  122. Griffin AS, West SA, Buckling A (2004) Cooperation and competition in pathogenic bacteria. Nature 430:1024–1027Google Scholar
  123. Grunden AM, Shanmugam KT (1997) Molybdate transport and regulation in bacteria. Arch Microbiol 168:345–354Google Scholar
  124. Haack EA, Johnston CT, Maurice PA (2008) Mechanisms of siderophore sorption to smectite and siderophore-enhanced release of structural Fe3+. Geochim Cosmochim Acta 72:3293–3586Google Scholar
  125. Hakemian AS, Tinberg CE, Kondapalli KC, Telser J, Hoffman BM, Stemmler TL, Rosenzweig AC (2005) The copper chelator methanobactin from Methylosinus trichosporium OB3b binds copper(I). J Am Chem Soc 127:17142–17143Google Scholar
  126. Hancock RD, Melton DL, Harrington JM, McDonald FC, Gephart RT, Boone LL, Jones SB, Dean NE, Whitehead JR, Cockrell GM (2007) Metal ion recognition in aqueous solution by highly preorganized non-macrocyclic ligands. Coord Chem Rev 251:1678–1689Google Scholar
  127. Harrington JM, Crumbliss AL (2009) The redox hypothesis in siderophore-mediated iron uptake. Biometals 22:679–689Google Scholar
  128. Harrington JM, Winkelmann G, Haselwandter K, Crumbliss AL (2011) Fe(III)-complexes of the tripodal trishydroxamate siderophore basidiochrome: potential biological implications. J Inorg Biochem 105:1670–1674Google Scholar
  129. Harrington JM, Bargar JM, Jarzecki AA, Sombers LA, Roberts JG, Duckworth OW (2012a) Trace metal complexation by the triscatecholate siderophore protochelin: structure and stability. Biometals 25:393–412Google Scholar
  130. Harrington JM, Parker DL, Bargar JR, Jarzecki AA, Tebo BM, Sposito G, Duckworth OW (2012b) Structural dependence of Mn complexation by siderophores: donor group dependence on complex stability and reactivity. Geochim Cosmochim Acta 88:106–119Google Scholar
  131. Harris WR, Amin SA, Kupper FC, Green DH, Carrano CJ (2007) Borate binding to siderophores: structure and stability. J Am Chem Soc 129:12263–12271Google Scholar
  132. Heddle J, Scott DJ, Unzai S, Park SY, Tame JRH (2003) Crystal structures of the liganded and unliganded nickel-binding protein NikA from Escherichia coli. J Biol Chem 278:50322–50329Google Scholar
  133. Heintze SG, Mann PJG (1949) Studies on soil manganese. J Agric Sci 39:80–95Google Scholar
  134. Hepinstall SE, Turner BF, Maurice PA (2005) Effects of siderophores on Pb and Cd adsorption to kaolinite. Clays Clay Miner 53:557–563Google Scholar
  135. Hernlem BJ, Vane LM, Sayles GD (1996) Stability constants for complexes of the siderophore desferrioxamine B with selected heavy metal cations. Inorg Chim Acta 244:179–184Google Scholar
  136. Hernlem BJ, Vane LM, Sayles GD (1999) The application of siderophores for metal recovery and waste remediation: examination of correlations for prediction of metal affinities. Water Resour 33:951–960Google Scholar
  137. Hider RC (1984) Siderophore mediated absorption of iron. Struct Bond 58:25–87Google Scholar
  138. Hider RC, Kong X (2010) Chemistry and biology of siderophore. Nat Prod Rep 27:637–657Google Scholar
  139. Hilger S, Sigg L, Barbieri A (1999) Size fractionation of phosphorus (dissolved, colloidal and particulate) in two tributaries to Lake Lugano. Aquat Sci 61:337–353Google Scholar
  140. Ho T-Y (2013) Nickel limitation of nitrogen fixation in Trichodesmium. Limnol Oceanogr 58:112–120Google Scholar
  141. Holler T, Wegener G, Knittel K, Boetius A, Brunner B, Kuypers MMM, Widdel F (2009) Substantial 13C/12C and D/H fractionation during anaerobic oxidation of methane by marine consortia enriched in vitro. Environ Microbiol Rep 1:370–376Google Scholar
  142. Hou ZG, Raymond KN, O’Sullivan B, Esker TW, Nishio T (1998) A preorganized siderophore: thermodynamic and structural characterization of alcaligin and bisucaberin, microbial macrocyclic dihydroxamate chelating agents. Inorg Chem 37:6630–6637Google Scholar
  143. Howard JB, Rees DC (2006) How many metals does it take to fix N-2? A mechanistic overview of biological nitrogen fixation. Proc Natl Acad Sci USA 103:17088–17093Google Scholar
  144. Inoue H, Kobayashi T, Nozoye T, Takahashi M, Kakei Y, Suzuki K, Nakazono M, Nakanishi H, Mori S, Nishizawa NK (2009) Rice OsYSL15 Is an iron-regulated Iron(III)-deoxymugineic acid transporter expressed in the roots and is essential for iron uptake in early growth of the seedlings. J Biol Chem 284:3470–3479Google Scholar
  145. Jacquot JE, Horak REA, Amin SA, Devol AH, Ingalls AE, Armbrust EV, Stahl DA, Moffett JW (2014) Assessment of the potential for copper limitation of ammonia oxidation by Archaea in a dynamic estuary. Marine Chem 162:37–49Google Scholar
  146. Jansen S, Gonzalez-Gil G, van Leeuwen HP (2007) The impact of Co and Ni speciation on methanogenesis in sulfidic media-Biouptake versus metal dissolution. Enzyme Microbial Technol 40:823–830Google Scholar
  147. Jarvis NV, Hancock RD (1991) Some correlations involving the stability of complexes of transuranium metal ions and ligands with negatively charged oxygen donors. Inorg Chim Acta 182:229–232Google Scholar
  148. Jean ME, Phalyvong K, Forest-Drolet J, Bellenger JP (2013) Molybdenum and phosphorus limitation of asymbiotic nitrogen fixation in forests of Eastern Canada: influence of vegetative cover and seasonal variability. Soil Biol Biochem 67:140–146Google Scholar
  149. John SG, Ruggiero CE, Hersman LE, Tung CS, Neu MP (2001) Siderophore mediated plutonium accumulation by Microbacterium flavescens (JG-9). Environ Sci Technol 35:2942–2948Google Scholar
  150. Karpishin TB, Dewey TM, Raymond KN (1993) Coordination chemistry of microbial iron transport.49. the vanadium(IV) enterobactin complex—structural, spectroscopic, and electrochemical characterization. J Am Chem Soc 115:1842–1851Google Scholar
  151. Kenney GE, Rosenzweig AC (2012) Chemistry and biology of the copper chelator methanobactin. ACS Chem Biol 7:A-IGoogle Scholar
  152. Kenney GE, Rosenzweig AC (2013) Genome mining for methanobactins. BMC Biol 11:17Google Scholar
  153. Khodr HH, Hider RC, Duhme-Klair AK (2002) The iron-binding properties of aminochelin, the mono(catecholamide) siderophore of Azotobacter vinelandii. J Biol Inorg Chem 7:891–896Google Scholar
  154. Kim HJ, Graham DW, DiSpirito AA, Alterman MA, Galeva N, Larive CK, Asunskis D, Sherwood PMA (2004) Methanobactin, a copper-acquisition compound from methane-oxidizing bacteria. Science 305:1612–1615Google Scholar
  155. Kim D, Duckworth OW, Strathmann TJ (2009) Hydroxamate siderophore-promoted reduction of nitroaromatic contaminants by iron(II). Geochim Cosmochim Acta 22:605–613Google Scholar
  156. Kletzin A, Adams MWW (1996) Tungsten in biological systems. FEMS Microbiol Rev 18:5–63Google Scholar
  157. Knapp CW, Fowle DA, Kulczycki E, Roberts JA, Graham DW (2007) Methane monooxygenase gene expression mediated by methanobactin in the presence of mineral copper sources. Proc Nat Acad Sci USA 104:12040–12045Google Scholar
  158. Knauer K, Behra R, Sigg L (1997) Effects of free Cu2+ and Zn2+ ions on growth and metal accumulation in freshwater algae. Environ Toxicol Chem 16:220–229Google Scholar
  159. Kraemer SM (2004) Iron oxide dissolution and solubility in the presence of siderophores. Aquat Sci 66:3–18Google Scholar
  160. Kraemer SM, Cheah SF, Zapf R, Xu J, Raymond KN, Sposito G (1999) Effect of hydroxamate siderophores on Fe release and Pb(II) adsorption by goethite. Geochim Cosmochim Acta 63:3003–3008Google Scholar
  161. Kraemer SM, Xu JD, Raymond KN, Sposito G (2002) Adsorption of Pb(II) and Eu(III) by oxide minerals in the presence of natural and synthetic hydroxamate siderophores. Environ Sci Technol 36:1287–1291Google Scholar
  162. Kraemer SM, Butler A, Borer P, Cervini-Silva J (2005) Siderophores and the dissolution of iron-bearing minerals in marine systems. In: Banfield JF, Cervini-Silva J, Nealson KH (eds) Molecular geomicrobiology. Mineralogical Society of America, Chantilly, pp 53–84Google Scholar
  163. Kraemer SM, Crowley DE, Kretzschmar R (2006) Geochemical aspects of phytosiderophore-promoted iron acquisition by plants. Adv Agron 91:1–46Google Scholar
  164. Kraepiel AML, Bellenger JP, Wichard T, Morel FMM (2009) Multiple roles of siderophores in free-living nitrogen-fixing bacteria. Biometals 22:573–581Google Scholar
  165. Kranzler C, Rudolf M, Keren N, Schleiff E (2013) Iron in Cyanobacteria. Adv Bot Res 65:57–105Google Scholar
  166. Krentz BD, Mulheron HJ, Semrau JD, DiSpirito AA, Bandow NL, Haft DH, Vuilleumier S, Murrell JC, McEllistrem MT, Hartsel SC, Gallagher WH (2010) A comparison of methanobactins from methylosinus trichosporium OB3b and methylocystis strain SB2 predicts methanobactins are synthesized from diverse peptide precursors modified to create a common core for binding and reducing copper ions. Biochemistry 49:10117–10130Google Scholar
  167. Kulczycki E, Fowle DA, Knapp C, Graham DW, Roberts JA (2007) Methanobactin-promoted dissolution of Cu-substituted borosilicate glass. Geobiology 5:251–263Google Scholar
  168. Leach LH, Morris JC, Lewis TA (2007) The role of the siderophore pyridine-2,6-bis (thiocarboxylic acid) (PDTC) in zinc utilization by Pseudomonas putida DSM 3601. Biometals 20:717–726Google Scholar
  169. Leal MFC, Vasconcelos MTSD, van den Berg CMG (1999) Copper-induced release of complexing ligands similar to thiols by Emiliania huxleyi in seawater cultures. Limnol Oceanogr 44:1750–1762Google Scholar
  170. Lebeau T, Braud A, Jezequel K (2008) Performance of bioaugmentation-assisted phytoextraction applied to metal contaminated soils: a review. Environ Pollut 153:497–522Google Scholar
  171. Lebrette H, Iannello M, Fontecilla-Camps JC, Cavazza C (2013) The vinding mode of Ni-(L-His)2 in NikA revealed by X-ray crystallography. J Inorg Biochem 121:16–18Google Scholar
  172. Leong J, Raymond KN (1975) Coordination isomers of biological iron transport compounds. IV. Geometrical Isomers of chromic desferrioxamine B. J Am Chem Soc 97:293–296Google Scholar
  173. Lewis K, Epstein S, D’Onofrio A, Ling LL (2010) Uncultured microorganisms as a source of secondary metabolites. J Antibiot 63:468–476Google Scholar
  174. Li YJ, Zamble DB (2009) Nickel homeostasis and nickel regulation: an overview. Chem Rev 109:4617–4643Google Scholar
  175. Lidstrom ME, Semrau JD (1995) Metals and microbiology—the influence of copper on methane oxidation. In: Huang CP, OMelia CR, Morgan JJ (eds) Aquatic chemistry—interfacial and interspecies processes, pp 195–201Google Scholar
  176. Liermann LJ, Guynn RL, Anbar A, Brantley SL (2005) Production of a molybdophore during metal-targeted dissolution of silicates by soil bacteria. Chem Geol 220:285–302Google Scholar
  177. Lloyd T (1999) Dissolution of Fe(III) and Mn(III, IV)-(hydr)oxides by desferrioxamine B. California Institute of Technology, PasadenaGoogle Scholar
  178. Loomis LD, Raymond KN (1991) Solution equilibria of enterobactin and metal-enterobactin complexes. Inorg Chem 30:906–911Google Scholar
  179. Madison AS, Tebo BM, Mucci A, Sundby B, Luther GW (2013) Abundant porewater Mn(III) is a major component of the sedimentary redox system. Science 341:875–878Google Scholar
  180. Maldonado MT, Allen AE, Chong JS, Lin K, Leus D, Karpenko N, Harris S (2006) Copper-dependent iron transport in coastal and oceanic diatoms. Limnol Oceanogr 51:1729–1743Google Scholar
  181. Manecki M, Maurice PA (2008) Siderophore promoted dissolution of pyromorphite. Soil Sci 173:821–830Google Scholar
  182. Martell AE, Hancock RD, Motekaitis RJ (1994) Factors affecting stabilities of chelate, macrocyclic and macrobicyclic complexes in solution. Coordin Chem Rev 133:39–65Google Scholar
  183. Martell AE, Smith RM, Moetekaitis M (2005) Critical evaluation of stability constants NIST Data Base 46, Washington, DCGoogle Scholar
  184. Martin JH, Fitzwater SE (1988) Iron-deficiency limits phytoplankton growth in the northeast pacific subarctic. Nature 331:341–343Google Scholar
  185. Martinez JS, Butler A (2007) Marine amphiphilic siderophores: marinobactin structure, uptake, and microbial partitioning. J Inorg Biochem 101:1692–1698Google Scholar
  186. Mawji E, Gledhill M, Milton JA, Tarran GA, Ussher S, Thompson A, Wolff GA, Worsfold PJ, Achterberg EP (2008) Hydroxamate Siderophores: occurrence and Importance in the Atlantic Ocean. Environ Sci Technol 42:8675–8680Google Scholar
  187. McCormack P, Worsfold PJ, Gledhill M (2003) Separation and detection of siderophores produced by marine bacterioplankton using high-performance liquid chromatography with electrospray ionization mass spectrometry. Anal Chem 75:2647–2652Google Scholar
  188. Milner MJ, Kochian LV (2008) Investigating heavy-metal hyperaccumulation using thlaspi caerulescens as a model system. Ann Bot 102:3–13Google Scholar
  189. Mishra B, Haack EA, Maurice PA, Bunker BA (2009) Effects of the microbial siderophore DFO-B on Pb and Cd speciation in aqueous solution. Environ Sci Technol 43:94–100Google Scholar
  190. 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 275:199–207Google Scholar
  191. Moffett JW, Brand LE (1996) Production of strong, extracellular Cu chelators by marine cyanobacteria in response to Cu stress. Limnol Oceanogr 41:388–395Google Scholar
  192. Moll H, Glorius M, Bernhard G (2008a) Curium(III) complexation with desferrioxamine B (DFO) investigated using fluorescence spectroscopy. Bull Chem Soc Jpn 81:857–862Google Scholar
  193. Moll H, Glorius M, Bernhard G, Johnsson A, Pedersen K, Schafer M, Budzikiewicz H (2008b) Characterization of pyoverdins secreted by a subsurface strain of Pseudomonas fluorescens and their interactions with Uranium(VI). Geomicrobiol J 25:157–166Google Scholar
  194. Moll H, Johnsson A, Schafer M, Pedersen K, Budzikiewicz H, Bernhard G (2008c) Curium(III) complexation with pyoverdins secreted by a groundwater strain of Pseudomonas fluorescens. Biometals 21:219–228Google Scholar
  195. Morel FMM (2008) The co-evolution of phytoplankton and trace elements in the ocean. Geobiology 6:318–324Google Scholar
  196. Morel FMM, Milligan AJ, Saito MA (2006) Marine bioinorganic chemistry: the role of trace metals in the oceanic cycles of major nutrients. In: Elderfield H (ed) The oceans and marine chemistry. Elsevier/Pergamon, Oxford, pp 113–144Google Scholar
  197. Morgan JJ (2000) Manganese in natural waters and Earth’s crust: it’s availability to organisms. Met Ions Biol Syst 37:1–34Google Scholar
  198. Morgan JJ (2005) Kinetics of reaction between O2 and Mn(II) species in aqueous solution. Geochim Cosmochim Acta 69:35–48Google Scholar
  199. Mucha P, Rekowshi P, Kosakowska A, Kupryszewski G (1999) Separation of siderophore by capillary electrophoresis. J Chromatogr A 830:183–189Google Scholar
  200. Mulrooney SB, Hausinger RP (2003) Nickel uptake and utilization by microorganisms. FEMS Microbiol Rev 27:239–261Google Scholar
  201. Murakami T, Ise K, Hayakawa M, Kamei S, Takagi S (1989) Stabilities of metal complexes of mugineic acids and their specific affinities for iron(III). Chem Lett 18:2137–2140Google Scholar
  202. Murata Y, Ma JF, Yamaji N, Ueno D, Nomoto K, Iwashita T (2006) A specific transporter for iron(III)-phytosiderophore in barley roots. Plant J 46:563–572Google Scholar
  203. Neilands JB (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270:26723–26726Google Scholar
  204. Nevitt T (2011) War–Fe–re: iron at the core of fungal virulence and host immunity. Biometals 24:547–558Google Scholar
  205. Nowack B, Schulin R, Robinson BH (2006) Critical assessment of chelant-enhanced metal phytoextraction. Environ Sci Technol 40:5225–5232Google Scholar
  206. Page WJ, von Tigerstrom M (1982) Iron-repressible and molybdenum-repressible outer-membrane proteins in competent Azotobacter-vinelandii. J Bacteriol 151:237–242Google Scholar
  207. Pakhomova SV, Rozanov AG, Yakushev EV (2009) Dissolved and particulate forms of iron and manganese in the redox zone of the Black Sea. Oceanology 49:773–787Google Scholar
  208. Pankow JF (1991) Aquatic chemistry concepts. CRC-Press, Boca RatonGoogle Scholar
  209. Parker DL, Sposito G, Tebo BM (2004) Manganese(III) binding to a pyoverdine siderophore produced by a manganese(II)-oxidizing bacterium. Geochim Cosmochim Acta 68:4809–4820Google Scholar
  210. Parker DL, Morita T, Mozafarzadeh ML, Verity R, McCarthy JK, Tebo BM (2007) Inter-relationships of MnO2 precipitation, siderophore-Mn-(III) complex formation, siderophore degradation, and iron limitation in Mn-(II)-oxidizing bacterial cultures. Geochim Cosmochim Acta 71:5672–5683Google Scholar
  211. Patel U, Baxi MD, Modi VV (1988) Evidence for the involvement of iron siderophore in the transport of molybdenum in cowpea rhizobium. Curr Microbiol 17:179–182Google Scholar
  212. Pearson RG (1963) Hard and soft acids and bases. J Am Chem Soc 85:3533–3539Google Scholar
  213. Peers G, Quesnel S-A, Price NM (2005) Copper requirements for iron acquisition and growth of coastal and oceanic diatoms. Limnol Oceanogr 50:1149–1158Google Scholar
  214. Peijnenburg WJGM, Zablotskaja M, Vijver MG (2007) Monitoring metals in terrestrial environments within a bioavailability framework and a focus on soil extraction. Ecotoxicol Environ Saf 67:163–179Google Scholar
  215. Peña J, Duckworth OW, Bargar JR, Sposito G (2007) Dissolution of hausmannite in the presence of the trihydroxamate siderophore desferrioxamine B. Geochim Cosmochim Acta 71:5661–5671Google Scholar
  216. Pesch ML, Christl I, Barmetller K, Kraemer SM, Kretzschmar R (2011) Isolation and purification of Cu-free methanobactin from Methylosinus trichosporium OB3b. Geochem Trans 12:2Google Scholar
  217. Pesch ML, Christl I, Hoffmann MK, Kraemer SM, Kretzschmar R (2012) Copper complexation of methanobactin isolated from Methylosinus trichosporium OB3b: pH- dependent speciation and modeling. J Inorg Biochem 116:55–62Google Scholar
  218. Pesch ML, Hoffmann M, Christl I, Kraemer SM, Kretzschmar R (2013) Competitive ligand exchange between Cu-humic acid complexes and methanobactin. Geobiology 11:44–54Google Scholar
  219. Pierwola A, Krupinski T, Zalupski P, Chiarelli M, Castignetti D (2004) Degradation pathway and generation of monohydroxamic acids from the trihydroxamate siderophore desferrioxamine B. Appl Environ Microbiol 70:831–836Google Scholar
  220. Price NM, Morel FMM (1990) Cadmium and cobalt substitution for zinc in a marine diatom. Nature 344:658–660Google Scholar
  221. Price NM, Morel FMM (1991) Colimitation of phytoplankton growth by nickel and nitrogen. Limnol Oceanogr 36:1071–1077Google Scholar
  222. Rabsch W, Winkelmann G (1991) The specificity of bacterial siderophore receptors probed by bioassays. Biol Metals 4:244–250Google Scholar
  223. Rajkumar M, Ae N, Freitas H (2009a) Endophytic bacteria and their potential to enhance heavy metal phytoextraction. Chemosphere 77:153–160Google Scholar
  224. Rajkumar M, Prasad MNV, Freitas H, Ae N (2009b) Biotechnological applications of serpentine soil bacteria for phytoremediation of trace metals. Crit Rev Biotechnol 29:120–130Google Scholar
  225. Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149Google Scholar
  226. Rajkumar M, Sandhya S, Prasad MNV, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv 30:1562–1574Google Scholar
  227. Raymond KN, Muller G, Matzanke BF (1984) Complexation of iron by siderophores—a review of their solution and structural chemistry and biological function. Top Curr Chem 123:49–102Google Scholar
  228. Reichard PU, Kraemer SM, Frazier SW, Kretzschmar R (2005) Goethite dissolution in the presence of phytosiderophores: rates, mechanisms, and the synergistic effect of oxalate. Plant Soil 276:115–132Google Scholar
  229. Reichard PU, Kretzschmar R, Kraemer SM (2007a) Dissolution mechanisms of goethite in the presence of siderophores and organic acids. Geochim Cosmochim Acta 71:5635–5650Google Scholar
  230. Reichard PU, Kretzschmar R, Kraemer SM (2007b) Rate laws of steady-state and non-steady-state ligand-controlled dissolution of goethite. Colloid Surf A-Physicochem Eng Asp 306:22–28Google Scholar
  231. Reid RT, Live DH, Faulkner DJ, Butler A (1993) A siderophore from a marine bacterium with an exceptional ferric ion affinity constant. Nature 366:455–458Google Scholar
  232. Robin A, Vansuyt G, Hinsinger P, Meyer JM, Briat JF, Lemanceau P (2008) Iron dynamics in the rhizosphere: consequences for plant health and nutrition. Adv Agron 99(99):183–225Google Scholar
  233. Robinson B, Fernandez JE, Madejon P, Maranon T, Murillo JM, Green S, Clothier B (2003) Phytoextraction: an assessment of biogeochemical and economic viability. Plant Soil 249:117–125Google Scholar
  234. Robson RL, Eady RR, Richardson TH, Miller RW, Hawkins M, Postgate JR (1986) The alternative nitrogenase of Azotobacter-chroococcum is a vanadium enzyme. Nature 322:388–390Google Scholar
  235. Römheld V (1991) The role of phytosiderophores in acquisition of iron and other micronutrients in graminaceous species—an ecological approach. Plant Soil 130:127–134Google Scholar
  236. Romheld V, Marschner H (1986) Evidence for a specific uptake system for iron phytosiderophores in roots of grasses. Plant Physiol 80:175–180Google Scholar
  237. Rue EL, Bruland KW (1995) Complexation of Iron (III) by natural organic ligand in the Central North Pacific as determined by a new competitive ligand equilibration adsorption cathodic strippin voltammetric method. Marine Chem 50:117–138Google Scholar
  238. Saal LB, Duckworth OW (2010) Synergistic dissolution of manganese oxides as promoted by siderophores and small organic acids. Soil Sci Soc Am J 74:2032–2038Google Scholar
  239. Saito MA, Moffett JW (2001) Complexation of cobalt by natural organic ligands in the Sargasso Sea as determined by a new high sensitivity electrochemical cobalt speciation method suitable for open ocean work. Marine Chem 75:49–68Google Scholar
  240. Saito MA, Moffett JW, Chisholm SW, Waterbury JB (2002) Cobalt limitation and uptake in Prochlorococcus. Limnol Oceanogr 47:1629–1636Google Scholar
  241. Saito MA, Rocap G, Moffett JW (2005) Production of cobalt binding ligands in a Synechococcus feature at the Costa Rica upwelling dome. Limnol Oceanogr 50:279–290Google Scholar
  242. Santner J, Smolders E, Wenzel WW, Degryse F (2012) First observation of diffusion-limited plant root phosphorus uptake from nutrient solution. Plant Cell Environ 35:1558–1566Google Scholar
  243. Saxena B, Vithlani L, Modi VV (1989) Siderophore-mediated transport of molybdenum in Azospirillum lipoferum strain D-2. Curr Microbiol 19:291–295Google Scholar
  244. Schalk IJ, Hannauer M, Braud A (2011) New roles for bacterial siderophores in metal transport and tolerance. Environ Microbiol 13:2844–2854Google Scholar
  245. Schenkeveld WDC, Dijcker R, Reichwein AM, Temminghoff EJM, Van Riemsdijk WH (2008) The effectiveness of soil-applied FeEDDHA treatments in preventing iron chlorosis in soybean as a function of the o, o-FeEDDHA content. Plant Soil 303:161–176Google Scholar
  246. Schenkeveld WDC, Temminghoff EJM, Reichwein AM, van Riemsdijk WH (2010) FeEDDHA-facilitated Fe uptake in relation to the behaviour of FeEDDHA components in the soil-plant system as a function of time and dosage. Plant Soil 332:69–85Google Scholar
  247. Schenkeveld WDC, Reichwein AM, Temminghoff EJM, van Riemsdijk WH (2012) Effect of soil parameters on the kinetics of the displacement of Fe from FeEDDHA chelates by Cu. J Phys Chem A 116:6582–6589Google Scholar
  248. Schenkeveld WDC, Oburger E, Gruber B, Schindlegger Y, Hann S, Puschenreiter M, Kraemer SM (2014a) Metal mobilization from soils by phytosiderophores—experiment and equilibrium modeling. Plant Soil 383:59–71Google Scholar
  249. Schenkeveld WDC, Schindlegger Y, Oburger E, Puschenreiter M, Hann S, Kraemer SM (2014b) Geochemical processes constraining iron uptake in strategy II Fe acquisition. Environ Sci Technol 48:12662–70Google Scholar
  250. Schubert S, Fischer D, Heesemann J (1999) Ferric enterochelin transport in Yersinia enterocolitica: molecular and evolutionary aspects. J Bacteriol 181:6387–6395Google Scholar
  251. Self WT, Grunden AM, Hasona A, Shanmugam KT (2001) Molybdate transport. Res Microbiol 152:311–321Google Scholar
  252. Semrau JD, DiSpirito AA, Yoon S (2010) Methanotrophs and copper. Fems Microbiol Rev 34:496–531Google Scholar
  253. Semrau JD, Jagadevan S, DiSpirito AA, Khalifa A, Scanlan J, Bergman BH, Freemeier BC, Baral BS, Bandow NL, Vorobev A, Haft DH, Vuilleumier S, Murrell JC (2013) Methanobactin and MmoD work in concert to act as the ‘copper-switch’ in methanotrophs. Environ Microbiol 15:3077–3086Google Scholar
  254. Shenker M, Hadar Y, Chen Y (1996) Stability constants of the fungal siderophore rhizoferrin with various microelements and calcium. Soil Sci Soc Am J 60:1140–1144Google Scholar
  255. Sheoran V, Sheoran AS, Poonia P (2010) Role of hyperaccumulators in phytoextraction of metals from contaminated mining sites: a review. Crit Rev Environ Sci Technol 41:168–214Google Scholar
  256. Siebner-Freibach H, Hadar Y, Chen Y (2004) Interaction of iron chelating agents with clay minerals. Soil Sci Soc Am J 68:470–480Google Scholar
  257. 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 54:1399–1408Google Scholar
  258. Silvester WB (1989) Molybdenum limitation of asymbiotic nitrogen-fixation in forests of Pacific Northwest America. Soil Biol Biochem 21:283–289Google Scholar
  259. Spasojevic I, Armstrong SK, Brickman TJ, Crumbliss AL (1999) Electrochemical behavior of the Fe(III) complexes of the cyclic hydroxamate siderophores alcaligin and desferrioxamine E. Inorg Chem 38:449–454Google Scholar
  260. Srivastava PC (1997) Biochemical significance of molybdenum in crop plants. In: Gupta UC (ed) Molybdenum in agriculture. Cambridge University Press, New YorkGoogle Scholar
  261. Stone AT (1996) Reactions of extracellular organic ligands with dissolved metal ions and mineral surfaces. In: Banfield JF, Nielson KH (eds) Geomicrobiology: interactions between microbes and minerals. Mineralogical Society of America, WashingtonGoogle Scholar
  262. Stumm W (1997) Reactivity at the mineral-water interface: dissolution and inhibition. Coll Surf A 120:143–166Google Scholar
  263. Sudek LA, Templeton AS, Tebo BM, Staudigel H (2009) Microbial ecology of Fe (hydr)oxide mats and basaltic rock from Vailulu’u Seamount, American Samoa. Geomicrobiol J 26:581–596Google Scholar
  264. Sunda WG, Huntsman SA (1995) Cobalt and zinc interreplacement in marine phytoplankton: biological and geochemical implications. Limnol Oceanogr 40:1404–1417Google Scholar
  265. Szabo O, Farkas E (2011) Characterization of Mn(II) and Mn(III) binding capability of natural siderophores desferrioxamine B and desferricoprogen as well as model hydroxamic acids. Inorg Chim Acta 376:500–508Google Scholar
  266. Tack FMG, Meers E (2010) Assisted phytoextraction: helping plants to help us. Elements 6:383–388Google Scholar
  267. Takagi SI, Kamei S, Yu MH (1988) Efficiency of iron extraction from soil by mugineic acid family phytosiderophores. J Plant Nutr 11:643–651Google Scholar
  268. Taylor RJ, May I, Wallwork AL, Denniss IS, Hill NJ, Galkin BY, Zilberman BY, Fedorov YS (1998) The applications of formo- and aceto-hydroxamic acids in nuclear fuel reprocessing. J Alloy Compd 271–273:534–537Google Scholar
  269. Tellez CM, Gaus KP, Graham DW, Arnold RG, Guzman RZ (1998) Isolation of copper biochelates from Methylosinus trichosporium OB3b and soluble methane monooxygenase mutants. Appl Environ Microbiol 64:1115–1122Google Scholar
  270. Thom VJ, Hosken GD, Hancock RD (1985) Anomalous metal ion size selectivity of tetraaza macrocycles. Inorg Chem 24:3378–3381Google Scholar
  271. Tinoco AD, Eames EV, Valentine AM (2008) Reconsideration of serum Ti(IV) transport: albumin and transferrin trafficking of Ti(IV) and its complexes. J Am Chem Soc 130:2262–2270Google Scholar
  272. Town RM, Filella M (2000) A comprehensive systematic compilation of complexation parameters reported for trace metals in natural waters. Aquat Sci 62:252–295Google Scholar
  273. Traxler MF, Seyedsayamdost MR, Clardy J, Kolter R (2012) Interspecies modulation of bacterial development through iron competition and siderophore piracy. Mol Microbiol 86:628–644Google Scholar
  274. Treeby M, Marschner H, Römheld V (1989) Mobilization of iron and other micronutrient cations from a calcareous soil by plant-borne, microbial and synthetic metal chelators. Plant Soil 114:217–226Google Scholar
  275. Trouwborst RE, Clement BG, Tebo BM, Glazer BT, Luther GW (2006) Soluble Mn(III) in suboxic zones. Science 313:1955–1957Google Scholar
  276. van Leeuwen HP, Town RM, Buffle J, Cleven R, Davison W, Puy J, van Riemsdijk WH, Sigg L (2005) Dynamic speciation analysis and bioavailability of metals in aquatic systems. Environ Sci Technol 39:8545–8556Google Scholar
  277. Van Nevel L, Mertens J, Oorts K, Verheyen K (2007) Phytoextraction of metals from soils: how far from practice? Environ Pollut 150:34–40Google Scholar
  278. Velasquez I, Nunn BL, Ibisanmi E, Goodlett DR, Hunter KA, Sander SG (2011) Detection of hydroxamate siderophores in coastal and sub-Antarctic waters off the South Eastern Coast of New Zealand. Marine Chem 126:97–107Google Scholar
  279. Villavicencio M, Neilands JB (1965) An inducible ferrichrome A-degrading peptidase from Pseudomonas FC1. Biochemistry 4:1092–1097Google Scholar
  280. Visca P, Colotti G, Serino L, Verzili D, Orsi N, Chiancone E (1992) Metal regulation of siderophore synthesis in Pseudomonas aeruginosa and functional effects of siderophore-metal complexes. Appl Environ Microbiol 58:2886–2893Google Scholar
  281. Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea—how can it occur. Biogeochemistry 13:87–115Google Scholar
  282. Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB, Sprent JI (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57:1–45Google Scholar
  283. von Wirén N, Romheld V, Morel JL, Guckert A, Marschner H (1993) Influence of microorganisms on iron acquisition in maize. Soil Biol Biochem 25:371–376Google Scholar
  284. Vorobev A, Jagadevan S, Baral BS, DiSpirito AA, Freemeier BC, Bergman BH, Bandow NL, Semrau JD (2013) Detoxification of mercury by methanobactin from methylosinus trichosporium OB3b. Appl Environ Microbiol 79:5918–5926Google Scholar
  285. Vraspir JM, Butler A (2009) Chemistry of marine ligands and siderophores. Annu Rev Marine Sci 1:43–63Google Scholar
  286. Weng L, Temminghoff EJM, van Riemsdijk WH (2001) Contribution of individual sorbents to the control of heavy metal activity in sandy soil. Environ Sci Technol 35:4436–4443Google Scholar
  287. Whisenhunt DW, Neu MP, Hou ZG, Xu J, Hoffman DC, Raymond KN (1996) Specific sequestering agents for the actinides. 29. Stability of the thorium(IV) complexes of desferrioxamine B (DFO) and three octadentate catecholate or hydroxypyridinonate DFO derivatives: DFOMTA, DFOCAMC, and DFO-1,2-HOPO. Comparative stability of the plutonium(IV) DFOMTA complex. Inorg Chem 35:4128–4136Google Scholar
  288. Wichard T, Bellenger JP, Loison A, Kraepiel AML (2008) Catechol siderophores control tungsten uptake and toxicity in the nitrogen-fixing bacterium Azotobacter vinelandii. Environ Sci Technol 42:2408–2413Google Scholar
  289. Wichard T, Bellenger JP, Morel FMM, Kraepiel AML (2009a) Role of the siderophore azotobactin in the bacterial acquisition of nitrogenase metal cofactors. Environ Sci Technol 43:7218–7224Google Scholar
  290. Wichard T, Mishra B, Myneni SCB, Bellenger JP, Kraepiel AML (2009b) Storage and bioavailability of molybdenum in soils increased by organic matter complexation. Nat Geosci 2:625–629Google Scholar
  291. Winkelmann G (2007) Ecology of siderophores with special reference to the fungi. Biometals 20:379–392Google Scholar
  292. Wolff-Boenisch D, Traina SJ (2007a) The effect of desferrioxamine B on the desorption of U(VI) from Georgia kaolinite KGa-1b and its ligand-promoted dissolution at pH 6 and 25 ºC. Chem Geol 242:278–287Google Scholar
  293. Wolff-Boenisch D, Traina SJ (2007b) The effect of desferrioxamine B, enterobactin, oxalic acid, and Na-alginate on the dissolution of uranyl-treated goethite at pH 6 and 25 ºC. Chem Geol 243:357–368Google Scholar
  294. Wurzburger N, Bellenger JP, Kraepiel AML, Hedin LO (2012) Molybdenum and phosphorus interact to constrain asymbiotic nitrogen fixation in tropical forests. Plos One 7:e33710Google Scholar
  295. Wuttig K, Heller MI, Croot PL (2013) Reactivity of inorganic Mn and Mn desferrioxamine B with O2, O2 , and H2O2 in seawater. Environ Sci Technol 47:10257–10265Google Scholar
  296. Xiong HC, Kakei Y, Kobayashi T, Guo XT, Nakazono M, Takahashi H, Nakanishi H, Shen HY, Zhang FS, Nishizawa NK, Zuo YM (2013) Molecular evidence for phytosiderophore-induced improvement of iron nutrition of peanut intercropped with maize in calcareous soil. Plant Cell Environ 36:1888–1902Google Scholar
  297. Xu C, Santschi PH, Zhong JY, Hatcher PG, Francis AJ, Dodge CJ, Roberts KA, Hung C-C, Honeyman BD (2008) Colloidal cutin-like substances cross-linked to siderophore decomposition products mobilizing plutonium from contaminated soils. Environ Sci Technol 42:8211–8217Google Scholar
  298. Xue HB, Sigg L (1999) Comparison of the complexation of Cu and Cd by humic or fulvic acids and by ligands observed in lake waters. Aquat Geochem 5:313–335Google Scholar
  299. Xue HB, Oestreich A, Kistler D, Sigg L (1996) Free cupric ion concentrations and Cu complexation in selected Swiss lakes and rivers. Aquat Sci 58:69–87Google Scholar
  300. Xue HB, Jansen S, Prasch A, Sigg L (2001) Nickel speciation and complexation kinetics in freshwater by ligand exchange and DPCSV. Environ Sci Technol 35:539–546Google Scholar
  301. Yehuda Z, Shenker M, Hadar Y, Chen YN (2000) Remedy of chlorosis induced by iron deficiency in plants with the fungal siderophore rhizoferrin. J Plant Nutr 23:1991–2006Google Scholar
  302. Yoshimura E, Kohdr H, Mori S, Hider R (2011) The binding of aluminum to mugineic acid and related compounds as studied by potentiometric titration. Biometals 24:723–727Google Scholar
  303. Zahn JA, DiSpirito AA (1996) Membrane-associated methane monooxygenase from Methylococcus capsulatus (Bath). J Bacteriol 178:1018–1029Google Scholar
  304. Zaya N, Roginsky A, Williams J, Castignetti D (1998) Evidence that a desferrioxamine B degrading enzyme is a serine protease. Can J Microbiol 44:521–527Google Scholar
  305. Zhong L, Yang J, Liu L, Li X (2013) Desferrioxamine-B promoted dissolution of an Oxisol and the effect of low-molecular-weight organic acids. Biol Fertil Soils 49:1077–1083Google Scholar
  306. Zuo YM, Zhang FS (2008) Effect of peanut mixed cropping with gramineous species on micronutrient concentrations and iron chlorosis of peanut plants grown in a calcareous soil. Plant Soil 306:23–36Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Stephan M. Kraemer
    • 1
  • Owen W. Duckworth
    • 2
  • James M. Harrington
    • 3
  • Walter D. C. Schenkeveld
    • 1
  1. 1.Department of Environmental GeosciencesUniversity of ViennaViennaAustria
  2. 2.Department of Soil ScienceNorth Carolina State UniversityRaleighUSA
  3. 3.Trace Inorganics Department, Technologies for Industry and the EnvironmentRTI InternationalDurhamUSA

Personalised recommendations