Skip to main content

Advertisement

SpringerLink
Log in

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

  • Published:
BioMetals Aims and scope Submit manuscript

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.

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

  • Alloway BJ (1995) Heavy metals in soils. Blackie Academic and Professional, Glasgow

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 232:92–94

    Article  PubMed  CAS  Google Scholar 

  • Burgess BK, Lowe DJ (1996) Mechanism of molybdenum nitrogenase. Chem Rev 96:2983–3011. doi:10.1021/cr950055x

    Article  PubMed  CAS  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. doi:10.1016/S0009-2541(02)00421-7

    Article  CAS  Google Scholar 

  • Cornish AS, Page WJ (1995) Production of the tricatecholate siderophore protochelin by Azotobacter vinelandii. Biometals 8:332–338. doi:10.1007/BF00141607

    Article  CAS  Google Scholar 

  • Cornish AS, Page WJ (1998) The catecholate siderophores of Azotobacter vinelandii: their affinity for iron and role in oxygen stress management. Microbiology 144:1747–1754

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Goldberg S, Forster HS, Godfrey CL (1996) Molybdenum adsorption on oxydes, clay minerals, and soils. Soil Sci Soc Am J 60:425–432

    CAS  Google Scholar 

  • Grunden AM, Shanmugan KT (1997) Molybdate transport and regulation in bacteria. Arch Microbiol 168:345–354. doi:10.1007/s002030050508

    Article  PubMed  CAS  Google Scholar 

  • Gustafsson JP (2003) Modelling molybdate and tungstate adsorption to ferrihydrite. Chem Geol 200:105–115. doi:10.1016/S0009-2541(03)00161-X

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 171:1075–1086

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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 48:1869–1884

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Page WJ, von-Tigerstrom M (1988) Aminochelin, a catecholamine siderophore produced by Azotobacter vinelandii. J Gen Microbiol 134:453–460

    CAS  Google Scholar 

  • 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., Basel

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Premakumar R, Jacobitz S, Ricke SC, Bishop PE (1996) Phenotypic characterization of a tungsten-tolerant mutant of Azotobacter vinelandii. J Bacteriol 178:691–696

    PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Self WT, Grunden AM, Hasona A, Shanmugam KT (2001) Molybdate transport. Res Microbiol 152:311–321. doi:10.1016/S0923-2508(01)01202-5

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Stiefel EI, Watt GD (1979) Azotobacter cytochrome b 557 is a bacterioferritin. Nature 279:81–83. doi:10.1038/279081a0

    Article  PubMed  CAS  Google Scholar 

  • Stumm W, Morgan JJ (1995) Aquatic chemistry. Wiley-Interscience Publication, New York

    Google Scholar 

  • Tindale AE, Mehrotra M, Ottem D, Page WJ (2000) Dual regulation of catecholate siderophore biosynthesis in Azotobacter vinelandii by iron and oxidative stress. Microbiology 146:1617–1626

    PubMed  CAS  Google Scholar 

  • Wedepohl KH (1995) The composition of the continental crust. Geochim Cosmochim Acta 59:1217–1232. doi:10.1016/0016-7037(95)00038-2

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Wichard T, Mishra B, Kraepiel AML, Myneni SCB (2008a) Molybdenum speciation and bioavailability in soils. Geochim Cosmochim Acta 72:A1019–A1019

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from the NSF (CHE-0221978, Center for Environmental Bioinorganic Chemistry) and by a fellowship from the Camille and Henry Dreyfus Postdoctoral Program in Environmental Chemistry to T.W.

Author information

Authors and Affiliations

  1. Chemistry Department, Princeton Environmental Institute, Guyot Hall, Princeton University, Princeton, NJ, 08544, USA

    A. M. L. Kraepiel

  2. Department of Geosciences, Princeton Environmental Institute, Guyot Hall, Princeton University, Princeton, NJ, 08544, USA

    J. P. Bellenger, T. Wichard & F. M. M. Morel

Authors
  1. A. M. L. Kraepiel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. P. Bellenger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T. Wichard
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. F. M. M. Morel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. M. L. Kraepiel.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kraepiel, A.M.L., Bellenger, J.P., Wichard, T. et al. Multiple roles of siderophores in free-living nitrogen-fixing bacteria. Biometals 22, 573–581 (2009). https://doi.org/10.1007/s10534-009-9222-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10534-009-9222-7

Keywords

Search

Navigation