Complexation of oxoanions and cationic metals by the biscatecholate siderophore azotochelin

  • Jean-Philippe Bellenger
  • Françoise Arnaud-Neu
  • Zouhair Asfari
  • Satish C. B. Myneni
  • Edward I. Stiefel
  • Anne M. L. Kraepiel
Original Paper

Abstract

Azotochelin is a biscatecholate siderophore produced by the nitrogen-fixing soil bacterium Azotobacter vinelandii. The complexation properties of azotochelin with a series of oxoanions [Mo(VI), W(VI) and V(V)] and divalent cations [Cu(II), Zn(II), Co(II) and Mn(II)] were investigated by potentiometry, UV–vis and X-ray spectroscopy. Azotochelin forms a strong 1:1 complex with molybdate (log K =  7.6 ± 0.4) and with tungstate and vanadate; the stability of the complexes increases in the order Mo < V < W (log KappMo = 7.3 ± 0.4; log KappV = 8.8 ± 0.4 and log KappW = 9.0 ± 0.4 at pH 6.6). The Mo atom in the 1:1 Mo–azotochelin complex is bound to two oxo groups in a cis position and to the two catecholate groups of azotochelin, resulting in a slightly distorted octahedral configuration. Below pH 5, azotochelin appears to form polynuclear complexes with Mo in addition to the 1:1 complex. Azotochelin also forms strong complexes with divalent metals. Of the metals studied, Cu(II) binds most strongly to azotochelin \({(\log \beta_{{{\text{CuLH}}^{{2 -}}}}=-12.9\pm 0.1)}\), followed by Zn(II) \({(\log \beta _{{{\text {ZnL}}^{{3 -}}}} =-24.1\pm 0.14, \log \beta _{{{\text {ZnLH}}^{{2 -}}}} =-17.83\pm 0.09)}\), Mn(II) \({(\log \beta _{{{\text {MnL}}^{{3 -}}}} = -29, \log\beta_{{{\text {MnLH}}^{{2-}}}}=-18.6\pm 0.8, \log \beta _{{{\text {MnLH}}_{2} ^{-}}} =-11.5\pm 0.7)}\) and Co(II) \({(\log \beta _{{{\text {CoLH}}^{{2 -}}}}= -23.0\pm0.3, \log \beta _{{{\text {CoLH}}_{2} ^{-}}}=-13.5\pm 0.2)}\). Since very few organic ligands are known to bind strongly to oxoanions (and particularly molybdate) at circumneutral pH, the unusual properties of azotochelin may be used for the separation and concentration of oxoanions in the laboratory and in the field. In addition, azotochelin may prove useful for the investigation of the biogeochemistry of Mo, W and V in aquatic and terrestrial systems.

Keywords

Molybdenum Vanadium Tungsten N,N-di(2,3-dihydroxybenzoyl)-l-lysine l-LysineCAM 

Notes

Acknowledgements

The authors wish to thank Norbert Clauer for his help throughout this work. This study was supported by grants from the NSF (CHE-0221978, Center for Environmental Bioinorganic Chemistry) and the French Department of Research, as well as a fellowship from the French Department of Education to J.P.B.

Supplementary material

References

  1. 1.
    Stiefel EI (2002) In: Sigel A, Sigel H (eds) Molybdenum and tungsten. Their roles in biological processes, vol 39. Dekker, New York, pp 1–30Google Scholar
  2. 2.
    Kimblin C, Bu XH, Butler A (2002) Inorg Chem 41:161–163PubMedCrossRefGoogle Scholar
  3. 3.
    Carter-Franklin JN, Butler A (2004) J Am Chem Soc 126:15060–15066PubMedCrossRefGoogle Scholar
  4. 4.
    Bishop PE, Premakumar R, Dean DR, Jacobson MR, Chisnell JR, Rizzo TM, Kopczynski J (1986) Science 232:92–94CrossRefPubMedGoogle Scholar
  5. 5.
    Hemrika W, Renirie R, Macedo-Ribeiro S, Messerschmidt A, Wever R (1999) J Biol Chem 274:23820–23827PubMedCrossRefGoogle Scholar
  6. 6.
    Messerschmidt A, Wever R (1996) Proc Natl Acad Sci USA 93:392–396PubMedCrossRefGoogle Scholar
  7. 7.
    Eady RR (2003) Coord Chem Rev 237:23–30CrossRefGoogle Scholar
  8. 8.
    Kletzin A, Adams MWW (1996) FEMS Microbiol Rev 18:5–63PubMedCrossRefGoogle Scholar
  9. 9.
    Chan MK, Mukund S, Kletzin A, Adams MWW, Rees DC (1995) Science 267:1463–1469PubMedCrossRefGoogle Scholar
  10. 10.
    Keeler RF, Varner JE (1957) Arch Biochem Biophys 70:585–590PubMedCrossRefGoogle Scholar
  11. 11.
    Benemann JR, Smith GM, Kostel PJ, McKenna CE (1973) FEBS Lett 29:219–221PubMedCrossRefGoogle Scholar
  12. 12.
    Hales BJ, Case EE (1987) J Biol Chem 262:16205–16211PubMedGoogle Scholar
  13. 13.
    Siemann S, Schneider K, Oley M, Müller A (2003) Biochemistry 42:3846–3857PubMedCrossRefGoogle Scholar
  14. 14.
    Hallenbeck PC, Benemann JR (1980) FEMS Microbiol Lett 9:121–124CrossRefGoogle Scholar
  15. 15.
    Kahn D, Hawkins M, Eady RR (1982) J Gen Microbiol 128:779–787Google Scholar
  16. 16.
    Lei S, Pulakat L, Gavini N (1999) Biochem Biophys Res Commun 264:186–190PubMedCrossRefGoogle Scholar
  17. 17.
    Jacobson MR, Premakumar R, Bishop PE (1986) J Bacteriol 167:480–486PubMedGoogle Scholar
  18. 18.
    Stintzi A, Barnes C, Xu J, Raymond KN (2000) Proc Natl Acad Sci USA 97:10691–10696PubMedCrossRefGoogle Scholar
  19. 19.
    Page WJ, von Tigerstrom M (1982) J Bacteriol 151:237–242PubMedGoogle Scholar
  20. 20.
    Patel U, Baxi MD, Modi VV (1988) Curr Microbiol 17:179–182CrossRefGoogle Scholar
  21. 21.
    Saxena B, Vithlani L, Modi VV (1989) Curr Microbiol 19:291–295CrossRefGoogle Scholar
  22. 22.
    Duhme AK, Hider RC, Naldrett MJ, Pau RN (1998) J Biol Inorg Chem 3:520–526CrossRefGoogle Scholar
  23. 23.
    Cornish AS, Page WJ (2000) Appl Environ Microbiol 66:1580–1586PubMedCrossRefGoogle Scholar
  24. 24.
    Chimiak A, Neilands JB (1984) Struct Bonding 58:89–96CrossRefGoogle Scholar
  25. 25.
    Merz KW, Fink J (1956) Arch Pharm 289:347–358CrossRefGoogle Scholar
  26. 26.
    Tkachev VV, Atovmyan LO (1975) Sov J Coord Chem Engl Transl 1:715–720Google Scholar
  27. 27.
    Griffith WP, Pumphrey CA, Rainey TA (1986) J Chem Soc Dalton Trans 6:1125–1128CrossRefGoogle Scholar
  28. 28.
    Westall JC, Zachary JL, Morel FMM (1976) Technical Report 18. MIT, CambridgeGoogle Scholar
  29. 29.
    Westall JC (1982) Report 82–02. Department of Chemistry, Oregon St University, CorvallisGoogle Scholar
  30. 30.
    Herbelin AL, Westall JC (1999) Report 99-01. Department of Chemistry, Oregon St University, CorvallisGoogle Scholar
  31. 31.
    Vetrogon VI, Lukyanenko NG, Schwing-Weill MJ, Arnaud-Neu F (1994) Talanta 41:2105–2112CrossRefPubMedGoogle Scholar
  32. 32.
    Gans P, Sabatini A, Vacca A (1996) Talanta 43:1739–1753CrossRefPubMedGoogle Scholar
  33. 33.
    Martell AE, Smith RM (1974–1989) Critical stability constants. Plenum, New YorkGoogle Scholar
  34. 34.
    Cruywagen JJ (2000) Adv Inorg Chem 49:127–182Google Scholar
  35. 35.
    Cruywagen JJ, Draaijer AG, Heyns JBB, Rohwer EA (2002) Inorg Chim Acta 331:322–329CrossRefGoogle Scholar
  36. 36.
    Ressler T (1998) J Synchrotron Radiat 5:118–122PubMedCrossRefGoogle Scholar
  37. 37.
    Farkas E, Csoka H, Gama S, Santos MA (2000) Talanta 57:935–943CrossRefGoogle Scholar
  38. 38.
    Lu X, Liu S, Mao X, Bu X (2001) J Mol Struct 562:89–94CrossRefGoogle Scholar
  39. 39.
    Atovmyan LO, Sokolova Y, Tkachev VV (1970) Dokl Phys Chem Sect 195:1355–1356Google Scholar
  40. 40.
    Duhme AK (1997) J Chem Soc Dalton Trans 773–778Google Scholar
  41. 41.
    Torreggiani A, Trinchero A, Tamba M, Taddei P (2005) J Raman Spectrosc 36:380–388CrossRefGoogle Scholar
  42. 42.
    Cornish AS, Page WJ (1998) Microbiology 144:1747–1754CrossRefGoogle Scholar
  43. 43.
    Boukhalfa H, Crumbliss AL (2002) BioMetals 15:325–339PubMedCrossRefGoogle Scholar
  44. 44.
    Hou Z, Raymond KN, O‘Sullivan B, Esker TW, Nishio T (1998) Inorg Chem 37:6630–6637PubMedCrossRefGoogle Scholar
  45. 45.
    Carrano CJ, Cooper SR, Raymond KN (1979) J Am Chem Soc 101:599–604CrossRefGoogle Scholar
  46. 46.
    Eady RR, Robson RL, Richardson TH, Miller RW, Hawkins M (1987) Biochem J 244:197–207PubMedGoogle Scholar
  47. 47.
    Eady RR, Robson RL (1984) Biochem J 224:853–862PubMedGoogle Scholar
  48. 48.
    Bishop PE, Jarlenski DML, Hetherington DR (1982) J Bacteriol 150:1244–1251PubMedGoogle Scholar
  49. 49.
    Lei S, Pulakat L, Gavini N (2000) FEBS Lett 482:149–153PubMedCrossRefGoogle Scholar
  50. 50.
    Self WT, Grunden AM, Hasona A, Shanmugam KT (2001) Res Microbiol 152:311–321PubMedCrossRefGoogle Scholar
  51. 51.
    Anderson MA, Morel FMM (1982) Limnol Oceanogr 27:789–813CrossRefGoogle Scholar
  52. 52.
    Sunda WG, Huntsman SA (1997) Nature 390:389–392CrossRefGoogle Scholar
  53. 53.
    Sunda WG, Huntsman SA (1995) Mar Chem 50:189–206CrossRefGoogle Scholar
  54. 54.
    Sunda WG, Swift DG, Huntsman SA (1991) Nature 351:55–57CrossRefGoogle Scholar
  55. 55.
    Timmermans KR, Stolte W, de Baar HJW (1994) Mar Biol 121:389–396CrossRefGoogle Scholar
  56. 56.
    Wilhelm SW, Trick CG (1994) Limnol Oceanogr 39:1979–1984CrossRefGoogle Scholar
  57. 57.
    Page WJ (1995) BioMetals 8:30–36Google Scholar
  58. 58.
    Duhme AK, Hider RC, Khodr HH (1997) Chem Ber/Recueil 130:969–973Google Scholar
  59. 59.
    Knosp O, von Tigerstrom M, Page WJ (1984) J Bacteriol 159:341–347PubMedGoogle Scholar

Copyright information

© SBIC 2006

Authors and Affiliations

  • Jean-Philippe Bellenger
    • 1
    • 2
  • Françoise Arnaud-Neu
    • 3
  • Zouhair Asfari
    • 3
  • Satish C. B. Myneni
    • 2
  • Edward I. Stiefel
    • 4
  • Anne M. L. Kraepiel
    • 5
  1. 1.UMR 7517 (CNRS-ULP), EOSTStrasbourg CedexFrance
  2. 2.Department of Geosciences, Guyot HallPrinceton UniversityPrincetonUSA
  3. 3.UMR 7512 (CNRS-ULP), ECPMStrasbourg Cedex 02France
  4. 4.Chemistry Department, 101 Hoyt LaboratoryPrinceton UniversityPrincetonUSA
  5. 5.Chemistry Department, PEI, Guyot HallPrinceton UniversityPrincetonUSA

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