BioMetals

, 22:573 | Cite as

Multiple roles of siderophores in free-living nitrogen-fixing bacteria

  • A. M. L. Kraepiel
  • J. P. Bellenger
  • T. Wichard
  • F. M. M. Morel
Article

Abstract

Free-living nitrogen-fixing bacteria in soils need to tightly regulate their uptake of metals in order to acquire essential metals (such as the nitrogenase metal cofactors Fe, Mo and V) while excluding toxic ones (such as W). They need to do this in a soil environment where metal speciation, and thus metal bioavailability, is dependent on a variety of factors such as organic matter content, mineralogical composition, and pH. Azotobacter vinelandii, a ubiquitous gram-negative soil diazotroph, excretes in its external medium catechol compounds, previously identified as siderophores, that bind a variety of metals in addition to iron. At low concentrations, complexes of essential metals (Fe, Mo, V) with siderophores are taken up by the bacteria through specialized transport systems. The specificity and regulation of these transport systems are such that siderophore binding of excess Mo, V or W effectively detoxifies these metals at high concentrations. In the topsoil (leaf litter layer), where metals are primarily bound to plant-derived organic matter, siderophores extract essential metals from natural ligands and deliver them to the bacteria. This process appears to be a key component of a mutualistic relationship between trees and soil diazotrophs, where tree-produced leaf litter provides a living environment rich in organic matter and micronutrients for nitrogen-fixing bacteria, which in turn supply new nitrogen to the ecosystem.

Keywords

Azotobacter vinelandii Metalophore Metal uptake Molybdenum Vanadium Tungsten 

References

  1. Alloway BJ (1995) Heavy metals in soils. Blackie Academic and Professional, GlasgowGoogle Scholar
  2. Andrews SC, Robinson AK, Rodriguez-Quinones F (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27:215–237. doi:10.1016/S0168-6445(03)00055-X PubMedCrossRefGoogle Scholar
  3. Barron AR, Wurzberger N, Bellenger JP, Wright SJ, Kraepiel AML, Hedin LO (2009) Molybdenum limits nitrogen fixation in tropical forest soils. Nat Geosci 2:42–45. doi:10.1038/NGEO366 CrossRefGoogle Scholar
  4. Bellenger J-P, 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 12:367–376. doi:10.1007/s00775-006-0194-6 PubMedCrossRefGoogle Scholar
  5. Bellenger J-P, Wichard T, Kraepiel AML (2008a) Vanadium requirements and uptake kinetics in the dinitrogen-fixing bacterium Azotobacter vinelandii. Appl Environ Microbiol 74:1478–1484. doi:10.1128/AEM.02236-07 PubMedCrossRefGoogle Scholar
  6. Bellenger J-P, Wichard T, Kustka AB, Kraepiel AML (2008b) Nitrogen fixing soil bacterium uses catechol siderophores for molybdenum and vanadium acquisition. Nat Geosci 1:243–246. doi:10.1038/ngeo161 CrossRefGoogle Scholar
  7. Bishop PE, Premakumar R, Dean DR, Jacobson MR, Chnisnell JR, Rizzo TM, Kopczynski J (1986) Nitrogen fixation by Azotobacter vinelandii strains having deletions in structural genes for nitrogenase. Science 232:92–94PubMedCrossRefGoogle Scholar
  8. Burgess BK, Lowe DJ (1996) Mechanism of molybdenum nitrogenase. Chem Rev 96:2983–3011. doi:10.1021/cr950055x PubMedCrossRefGoogle Scholar
  9. 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. doi:10.1016/S0009-2541(02)00421-7 CrossRefGoogle Scholar
  10. Cornish AS, Page WJ (1995) Production of the tricatecholate siderophore protochelin by Azotobacter vinelandii. Biometals 8:332–338. doi:10.1007/BF00141607 CrossRefGoogle Scholar
  11. Cornish AS, Page WJ (1998) The catecholate siderophores of Azotobacter vinelandii: their affinity for iron and role in oxygen stress management. Microbiology 144:1747–1754CrossRefGoogle Scholar
  12. Cornish AS, Page WJ (2000) Role of molybdate and other transition metals in the accumulation of protochelin by Azotobacter vinelandii. Appl Environ Microbiol 66:1580–1586. doi:10.1128/AEM.66.4.1580-1586.2000 PubMedCrossRefGoogle Scholar
  13. 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 3:520–526. doi:10.1007/s007750050263 CrossRefGoogle Scholar
  14. 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 8:1645–1652. doi:10.1039/b300431g CrossRefGoogle Scholar
  15. Goldberg S, Forster HS, Godfrey CL (1996) Molybdenum adsorption on oxydes, clay minerals, and soils. Soil Sci Soc Am J 60:425–432Google Scholar
  16. Grunden AM, Shanmugan KT (1997) Molybdate transport and regulation in bacteria. Arch Microbiol 168:345–354. doi:10.1007/s002030050508 PubMedCrossRefGoogle Scholar
  17. Gustafsson JP (2003) Modelling molybdate and tungstate adsorption to ferrihydrite. Chem Geol 200:105–115. doi:10.1016/S0009-2541(03)00161-X CrossRefGoogle Scholar
  18. Hudson RJM, Morel FMM (1992) Trace metal transport by marine microorganisms: implications of metal coordination kinetics. Deep Sea Res Part I Oceanogr Res Pap 40:129–150. doi:10.1016/0967-0637(93)90057-A CrossRefGoogle Scholar
  19. Hungate BA, Stiling PD, Dijkstra P, Johnson DW, Ketterer ME, Hymus GJ, Hinkle CR, Drake BG (2004) CO2 elicits long-term decline in nitrogen fixation. Science 304:1291. doi:10.1126/science.1095549 PubMedCrossRefGoogle Scholar
  20. Joerger RD, Jacobson MR, Premakumar R, Wolfinger ED, Bishop PE (1989) Nucleotide sequence and mutational analysis of the structural genes (anfHDGK) for the second alternative nitrogenase from Azotobacter vinelandii. J Bacteriol 171:1075–1086PubMedGoogle Scholar
  21. Keeler RF, Varner JE (1957) Tungstate as an antagonist of molybdate in Azotobacter vinelandii. Arch Biochem Biophys 70:585–590. doi:10.1016/0003-9861(57)90146-7 PubMedCrossRefGoogle Scholar
  22. Konigsberger LC, Konigsberger E, May PM, Hefter GT (2000) Complexation of iron(III) and iron(II) by citrate. Implications for iron speciation in blood plasma. J Inorg Biochem 78:175–184. doi:10.1016/S0162-0134(99)00222-6 PubMedCrossRefGoogle Scholar
  23. Kraemer SM (2004) Iron oxide dissolution and solubility in the presence of siderophores. Aquat Sci 66:3–18. doi:10.1007/s00027-003-0690-5 CrossRefGoogle Scholar
  24. Kula RJ, Rabenstein DL (1966) Solution equilibria and structures of Molybdenum(VI) complexes chelates. (Ethylenedinitrilo)tetraacetic acid. Anal Chem 38:1581–1584. doi:10.1021/ac60243a032 CrossRefGoogle Scholar
  25. Kustka AB, Sanudo-Wilhelmy SE, Carpenter EJ, Capone D, Burns J, Sunda WG (2003) Iron requirements for Dinitrogen- and Ammonium-supported growth in cultures of Trichodesmium (IMS 101): comparison with nitrogen fixation rates and iron: carbon ratios of field populations. Limnol Oceanogr 48:1869–1884Google Scholar
  26. Lang F, Kaupenjohann M (2000) Molybdenum at German Norway spruce sites: contents and mobility. Can J Res 30:1034–1040. doi:10.1139/cjfr-30-7-1034 CrossRefGoogle Scholar
  27. Page WJ, von-Tigerstrom M (1988) Aminochelin, a catecholamine siderophore produced by Azotobacter vinelandii. J Gen Microbiol 134:453–460Google Scholar
  28. Pau RN, Lawson DM (2002) Transport, homeostasis, regulation, and binding of molybdate and tungstate to proteins. In: Sigel A, Sigel H (eds) Metal ions in biological systems: molybdenum and tungsten: their roles in biological processes. Dekker Inc., BaselGoogle Scholar
  29. Perakis SS, Hedin LO (2002) Nitrogen loss from unpolluted South American forests mainly via dissolved organic compounds. Nature 415:416–419. doi:10.1038/415416a PubMedCrossRefGoogle Scholar
  30. Pratte BS, Thiel T (2006) High-affinity vanadate transport system in the cyanobacterium Anabaena variabilis ATCC 29413. J Bacteriol 188:464–468. doi:10.1128/JB.188.2.464-468.2006 PubMedCrossRefGoogle Scholar
  31. Premakumar R, Jacobitz S, Ricke SC, Bishop PE (1996) Phenotypic characterization of a tungsten-tolerant mutant of Azotobacter vinelandii. J Bacteriol 178:691–696PubMedGoogle Scholar
  32. Przyborowski VL, Schwarenbach G, Zimmermann T (1965) Komplexe XXVII. Die EDTA-Konplexe des Vanadiums (V). Helv Chim Acta 48:1556–1565. doi:10.1002/hlca.19650480716 CrossRefGoogle Scholar
  33. Reichard PU, Kretzschmar R, Kraemer SM (2007) Dissolution mechanisms of goethite in the presence of siderophores and organic acids. Geochim Cosmochim Acta 71:5635–5650. doi:10.1016/j.gca.2006.12.022 CrossRefGoogle Scholar
  34. Schalk IJ (2008) Metal trafficking via siderophores in gram-negative bacteria: specificities and characteristics of the pyoverdine pathway. J Inorg Biochem 102:1159–1169. doi:10.1016/j.jinorgbio.2007.11.017 PubMedCrossRefGoogle Scholar
  35. Self WT, Grunden AM, Hasona A, Shanmugam KT (2001) Molybdate transport. Res Microbiol 152:311–321. doi:10.1016/S0923-2508(01)01202-5 PubMedCrossRefGoogle Scholar
  36. Serrat FB, Morell GB (1994) Colorimetric method for the determination of vanadium with tannic acid in water and oils. Fresenius J Anal Chem 349:717. doi:10.1007/BF00325645 CrossRefGoogle Scholar
  37. Siemann S, Schneider K, Oley M, Muller A (2003) Characterization of a tungsten-substituted nitrogenase isolated from Rhodobacter capsulatus. Biochemistry 42:3846–3857. doi:10.1021/bi0270790 PubMedCrossRefGoogle Scholar
  38. Silvester WB (1989) Molybdenum limitation of asymbiotic nitrogen fixation in forests of Pacific Northwest America. Soil Biol Biochem 21:283–289. doi:10.1016/0038-0717(89)90106-5 CrossRefGoogle Scholar
  39. Sprencel C, Cao Z, Qi Z, Scott DC, Montague MA, Ivanoff N, Xu J, Raymond KM, Newton SMC, Klebba PE (2000) Binding of ferric enterobactin by the Escherichia coli periplasmic protein FepB. J Bacteriol 182:5359–5364. doi:10.1128/JB.182.19.5359-5364.2000 PubMedCrossRefGoogle Scholar
  40. Stiefel EI, Watt GD (1979) Azotobacter cytochrome b 557 is a bacterioferritin. Nature 279:81–83. doi:10.1038/279081a0 PubMedCrossRefGoogle Scholar
  41. Stumm W, Morgan JJ (1995) Aquatic chemistry. Wiley-Interscience Publication, New YorkGoogle Scholar
  42. Tindale AE, Mehrotra M, Ottem D, Page WJ (2000) Dual regulation of catecholate siderophore biosynthesis in Azotobacter vinelandii by iron and oxidative stress. Microbiology 146:1617–1626PubMedGoogle Scholar
  43. Wedepohl KH (1995) The composition of the continental crust. Geochim Cosmochim Acta 59:1217–1232. doi:10.1016/0016-7037(95)00038-2 CrossRefGoogle Scholar
  44. Werber T, Allard T, Tipping E, Benedetti MF (2006) Modeling Iron bonding to organic matter. Environ Sci Technol 40:7488–7493. doi:10.1021/es0607077 CrossRefGoogle Scholar
  45. Wichard T, Mishra B, Kraepiel AML, Myneni SCB (2008a) Molybdenum speciation and bioavailability in soils. Geochim Cosmochim Acta 72:A1019–A1019Google Scholar
  46. Wichard T, Bellenger J-P, Loison A, Kraepiel AML (2008b) Catechols siderophores control tungsten uptake and toxicity in the nitrogen-fixer bacterium Azotobacter vinelandii. Environ Sci Technol 42:2408–2413. doi:10.1021/es702651f PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC. 2009

Authors and Affiliations

  • A. M. L. Kraepiel
    • 1
  • J. P. Bellenger
    • 2
  • T. Wichard
    • 2
  • F. M. M. Morel
    • 2
  1. 1.Chemistry Department, Princeton Environmental Institute, Guyot HallPrinceton UniversityPrincetonUSA
  2. 2.Department of Geosciences, Princeton Environmental Institute, Guyot HallPrinceton UniversityPrincetonUSA

Personalised recommendations