BioMetals

, Volume 25, Issue 2, pp 393–412 | Cite as

Trace metal complexation by the triscatecholate siderophore protochelin: structure and stability

  • James M. Harrington
  • John R. Bargar
  • Andrzej A. Jarzecki
  • James G. Roberts
  • Leslie A. Sombers
  • Owen W. Duckworth
Article

Abstract

Although siderophores are generally viewed as biological iron uptake agents, recent evidence has shown that they may play significant roles in the biogeochemical cycling and biological uptake of other metals. One such siderophore that is produced by A. vinelandii is the triscatecholate protochelin. In this study, we probe the solution chemistry of protochelin and its complexes with environmentally relevant trace metals to better understand its effect on metal uptake and cycling. Protochelin exhibits low solubility below pH 7.5 and degrades gradually in solution. Electrochemical measurements of protochelin and metal–protochelin complexes reveal a ligand half-wave potential of 200 mV. The Fe(III)Proto3− complex exhibits a salicylate shift in coordination mode at circumneutral to acidic pH. Coordination of Mn(II) by protochelin above pH 8.0 promotes gradual air oxidation of the metal center to Mn(III), which accelerates at higher pH values. The Mn(III)Proto3− complex was found to have a stability constant of log β110 = 41.6. Structural parameters derived from spectroscopic measurements and quantum mechanical calculations provide insights into the stability of the Fe(III)Proto3−, Fe(III)H3Proto, and Mn(III)Proto3− complexes. Complexation of Co(II) by protochelin results in redox cycling of Co, accompanied by accelerated degradation of the ligand at all solution pH values. These results are discussed in terms of the role of catecholate siderophores in environmental trace metal cycling and intracellular metal release.

Keywords

Siderophores Catechol Iron Manganese Cobalt Complexation 

Supplementary material

10534_2011_9513_MOESM1_ESM.doc (666 kb)
Supplementary material 1 (DOC 667 kb)

References

  1. Abergel RJ, Warner JA, Shuh DK, Raymond KN (2006) Enterobactin protonation and iron release: structural characterization of the salicylate coordination shift in ferric enterobactin. J Am Chem Soc J128:8920–8931CrossRefGoogle Scholar
  2. Abergel RJ, Zawadzka AM, Hoette TM, Raymond KN (2009) Enzymatic hydrolysis of trilactone siderophores: where chiral recognition occurs in enterobactin and bacillibactin iron transport. J Am Chem Soc 131(35):12682–12692PubMedCrossRefGoogle Scholar
  3. Ahrland S, Dahlgren A, Persson I (1990) Stabilities and hydrolysis of some iron(II) and manganese(III) complexes with chelating ligands. Acta Agric Scand 40:101–111CrossRefGoogle Scholar
  4. Albrecht-Gary AM, Crumbliss AL (1998) Coordination chemistry of siderophores: thermodynamics and kinetics of iron chelation and release. In: Sigel A, Sigel H (eds) Metal ions in biological systems. M. Dekker, New YorkGoogle Scholar
  5. Bath BD, Michael DJ, Trafton BJ, Joseph JD, Runnels PL, Wightman RM (2000) Subsecond adsorption and desorption of dopamine at carbon-fiber microelectrodes. Anal Chem 72(24):5994–6002PubMedCrossRefGoogle Scholar
  6. Becke AD (1993) Density-functional thermochemistry. III. The role of exact exchange. J Chem Phys 98:5648–5652CrossRefGoogle Scholar
  7. 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(3):367–376. doi:10.1007/s00775-006-0194-6 PubMedCrossRefGoogle Scholar
  8. Bellenger JP, Wichard T, Kraepiel AML (2008a) Vanadium requirements and uptake kinetics in the dinitrogen-fixing bacterium Azotobacter vinelandii. Appl Environ Microbiol 74(5):1478–1484. doi:10.1128/aem.02236-07 PubMedCrossRefGoogle Scholar
  9. 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(4):243–246. doi:10.1038/Ngeo161 CrossRefGoogle Scholar
  10. 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(6):1395–1411. doi:10.1111/j.1462-2920.2011.02440.x PubMedCrossRefGoogle Scholar
  11. Bodini M, Osorio C, Valle MAd, Aranciba V, Munoz G (1995) Redox chemistry of 3,4-dihydroxy-2-benzoic acid, its oxidation products and their interaction with manganese(II) and manganese(III). Polyhedron 14(20–21):2933–2936CrossRefGoogle Scholar
  12. Boukhalfa H, Reilly SD, Smith WH, Neu MP (2004) EDTA and mixed-ligand complexes of tetravalent and trivalent plutonium. Inorg Chem 43:5816PubMedCrossRefGoogle Scholar
  13. 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 46:1018PubMedCrossRefGoogle Scholar
  14. Buerge IJ, Hug SJ (1998) Influence of organic ligands on chromium(VI) reduction by iron(II). Environ Sci Technol 32:2092–2099CrossRefGoogle Scholar
  15. 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 analogs. Inorg Chem 35:6429–6436Google Scholar
  16. Clarke ET, Tari LW, Vogel HJ (2001) Structural biology of bacterial iron uptake systems. Curr Top Med Chem 1:7PubMedCrossRefGoogle Scholar
  17. Cornish AS, Page WJ (1995) Production of the Triscatecholate Siderophore Protochelin by Azotobacter vinelandii. Biometals 8(4):332–338CrossRefGoogle Scholar
  18. Cornish AS, Page WJ (2000) Role of molybdate and other transition metals in the accumulation of protochelin by Azotobacter vinelandii. Appl Environ Microbiol 66(4):1580–1586PubMedCrossRefGoogle Scholar
  19. Crumbliss AL, Harrington JM (2009) Iron sequestration by small molecules: thermodynamic and kinetic studies of natural siderophores and synthetic model compounds. In: van Eldik R (ed) Advance in inorganic chemistry, vol 61. Elsevier, Amsterdam, pp 179–250Google Scholar
  20. Dahlheimer SR, Neal CR, Fein JB (2007) Potential mobilization of platinum-group elements by siderophores in surface environments. Environ Sci Technol 41(3):870–875PubMedCrossRefGoogle Scholar
  21. Devlin HR, Harris IJ (1984) Mechanism of the oxidation of aqueous phenol with dissolved oxygen. Ind Eng Chem Fundam 23:387–392CrossRefGoogle Scholar
  22. Downward L, Booth CH, Lukens WW, Bridges FA (2006) Variation of the F-test for determining statistical relevance of particular parameters in EXAFS fits. In: Hedman B, Pianetta P (eds) 13th international conference on X-Ray absorption fine structure. Stanford Synchrotron Radiation Laboratory, StanfordGoogle Scholar
  23. Duckworth OW, Sposito G (2005) Siderophore–manganese(III) interactions I. Air-oxidation of manganese(II) promoted by desferrioxamine B. Environ Sci Technol 39:6037–6044PubMedCrossRefGoogle Scholar
  24. 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 72:3371–3380CrossRefGoogle Scholar
  25. Duckworth OW, Bargar JR, Sposito G (2009a) Quantitative structure–activity relationships for aqueous metal–siderophore complexes. Environ Sci Technol 43:343–349PubMedCrossRefGoogle Scholar
  26. Duckworth OW, Holmström SJM, Pena J, Sposito G (2009b) Biogeochemistry of iron oxidation in a circumneutral freshwater habitat. Chem Geol 260(3–4):149–158CrossRefGoogle Scholar
  27. Duckworth OW, Jarzecki AA, Bargar JR, Oyerinde O, Spiro TG, Sposito G (2009c) An exceptionally stable cobalt(III)–desferrioxamine B complex. Mar Chem 113:114–122CrossRefGoogle Scholar
  28. Duhme AK, Hider RC, Khodr HH (1997) Synthesis and iron-binding properties of protochelin, the tris(catecholamide) siderophore of Azotobacter vinelandii. Chem Ber Recueil 130:969–973CrossRefGoogle Scholar
  29. 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(5):520–526CrossRefGoogle Scholar
  30. Essén SA, Bylund D, Holmström SJA (2006) Quantification of hydroxamate siderophores in soil solutions of podzolic soil profiles in Sweden. Biometals 19(3):269–282PubMedCrossRefGoogle Scholar
  31. Frazier SW, Kretzschmar K, Kraemer SM (2005) Bacterial siderophores promote dissolution of UO2 under reducing conditions. Environ Sci Technol 39(15):5709–5715PubMedCrossRefGoogle Scholar
  32. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Scalmani G, Barone V, Mennucci B, Petersson GA, Nakatsuji H, Caricato M, Li X, Hratchian HP, Izmaylov AF, Bloino J, Zheng G, Sonnenberg JL, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Vreven T, Montgomery J, A J, Peralta JE, Ogliaro F, Bearpark M, Heyd JJ, Brothers E, Kudin KN, Staroverov VN, Kobayashi R, Normand J, Raghavachari K, Rendell A, Burant JC, Iyengar SS, Tomasi J, Cossi M, Rega N, Millam NJ, Klene M, Knox JE, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Martin RL, Morokuma K, Zakrzewski VG, Voth GA, Salvador P, Dannenberg JJ, Daniels S, Dapprich AD, Farkas Ö, Foresman JB, Ortiz JV, Cioslowski J, Fox DJ (2009) Gaussian 09. B, 1st edn. Gaussian Inc., WallingfordGoogle Scholar
  33. Gans P, Sabatini A, Vacca A (1996) Investigation of equilibria in solution. Determination of equilibrium constants with HYPERQUAD suite of programs. Talanta 43(10):1739–1753PubMedCrossRefGoogle Scholar
  34. Hamilton WC (1965) Significance tests on the crystallographic R factor. Acta Crystallogr 18:502–510CrossRefGoogle Scholar
  35. Harrington JM, Park H, Ying Y, Hong J, Crumbliss AL (2011a) Characterization of Fe(III) sequestration by an analog of the cytotoxic siderophore brasilibactin A: implications for the iron transport mechanism in mycobacteria. Metallomics 3:464–471PubMedCrossRefGoogle Scholar
  36. Harrington JM, Parker DL, Jarzecki AA, Bargar JR, Tebo BM, Duckworth OW (2011b) Structural dependence of manganese chelation by siderophores: Donor group dependence of complex stability and reactivity. Geochim Cosmochim Acta (inpress)Google Scholar
  37. Harris WR, Carrano CJ, Raymond KN (1979a) Coordination chemistry of microbial iron transport compounds. 16. Isolation, characterization, and formation constants of ferric aerobactin. J Am Chem Soc 101:2722CrossRefGoogle Scholar
  38. Harris WR, Carrano CR, Cooper SR, Sofen SR, Avdeef AE, McArdle JV, Raymond KN (1979b) Coordination chemistry of microbial iron transport compounds. 19. Stability constants and electrochemical behavior of ferric enterobactin and model complexes. J Am Chem Soc 101:6097–6104CrossRefGoogle Scholar
  39. Harris WR, Amin SA, Kuepper FC, Green DH, Carrano CJ (2007) Borate binding to siderophores: structure and stability. J Am Chem Soc 129:12263PubMedCrossRefGoogle Scholar
  40. Hay BP, Dixon DA, Vargas R, Garza J, Raymond KN (2001) Structural criteria for the rational design of selective ligands. 3. Quantitative structure–stability relationship for Iron(III) complexation by tris-catecholamide siderophores. Inorg Chem 40:3922–3935PubMedCrossRefGoogle Scholar
  41. Heien M, Johnson MA, Wightman RM (2004) Resolving neurotransmitters detected by fast-scan cyclic voltammetry. Anal Chem 76(19):5697–5704. doi:10.1021/ac0491509 PubMedCrossRefGoogle Scholar
  42. 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
  43. Hewkin DJ, Prince RH (1970) The mechanism of octahedral complex formation by labile metal ions. Coord Chem Rev 5:45–73CrossRefGoogle Scholar
  44. Hider RC, Kong X (2010) Chemistry and biology of siderophores. Nat Prod Rep 27:637–657PubMedCrossRefGoogle Scholar
  45. Holmström SJA, Lundstrom US, Finlay RD, Van Hees PAW (2004) Siderophores in forest soil solution. Biogeochemistry 71(2):247–258CrossRefGoogle Scholar
  46. Hou Z, Stack TDP, Sunderland CJ, Raymond KN (1997) Enhanced iron(III) chelation through ligand predisposition: syntheses, structures and stability of tris-catecholate enterobactin analogs. Inorg Chim Acta 263:341–355CrossRefGoogle Scholar
  47. Kelly SD, Hesterberg D, Ravel B (2008) Analysis of soils and minerals using X-ray absorption spectroscopy. In: Ulery AL, Drees LR (eds) Methods of soil analysis. Soil Science Society of America, MadisonGoogle Scholar
  48. 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(7–8):891–896. doi:10.1007/s00775-002-0375-x PubMedGoogle Scholar
  49. Kohler T, Armbruster T, Libowitzky E (1997) Hydrogen bonding and Jahn–Teller distortion in groutite, α-MnOOH, and manganite, γ-MnOOH, and their relations to the manganese dioxides ramsdellite and pyrolusite. J Solid State Chem 133:486–500CrossRefGoogle Scholar
  50. Kraemer SM (2004) Iron oxide dissolution and solubility in the presence of siderophores. Aquat Sci 66:3–18CrossRefGoogle Scholar
  51. 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, vol 5. Mineralogical Society of America, ChantillyGoogle Scholar
  52. Kraepiel AML, Bellenger JP, Wichard T, Morel FMM (2009) Multiple roles of siderophores in free-living nitrogen-fixing bacteria. Biometals 22(4):573–581. doi:10.1007/s10534-009-9222-7 PubMedCrossRefGoogle Scholar
  53. Lee C, Yang W, Parr RG (1988) Development of the Colle–Salvetti correlation-energy formula into a functional of the electron density. Phys Rev B 37:785–789CrossRefGoogle Scholar
  54. Levina A, Armstrong RS, Lay PA (2005) Three-dimensional structure determination using multiple-scattering analysis of XAFS: applications to metalloproteins and coordination chemistry. Coord Chem Rev 249:141–160CrossRefGoogle Scholar
  55. Loomis LD, Raymond KN (1991) Solution equilibria of enterobactin and metal–enterobactin complexes. Inorg Chem 30:906–911CrossRefGoogle Scholar
  56. Marschner H, Romheld V, Kissel M (1986) Different strategies in higher plants inmobilization and uptake of iron. J Plant Nutr 9:695–713CrossRefGoogle Scholar
  57. Martell AE, Smith RM (2003) Critical stability constant database. National Institute of Science and Technology (NIST), GaithersburgGoogle Scholar
  58. Mawji E, Gledhill M, Milton JA, Tarran GA, Ussher S, Thompson A, Wolff GA, Worsfold PJ, Achterbeg EP (2008) Hydroxamate siderophores: occurrence and importance in the Atlantic Ocean. Environ Sci Technol 42(23):8675–8680PubMedCrossRefGoogle Scholar
  59. 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(1):94–100PubMedCrossRefGoogle Scholar
  60. Mucha P, Rekowski P, Kosakowska A, Kupryszewski G (1999) Separation of siderophores by capillary electrophoresis. J Chromatogr A 830(1):183–189CrossRefGoogle Scholar
  61. Neu MP, Icopini GA, Boukhalfa H (2005) Plutonium speciation affected by environmental bacteria. Radiochim Acta 93:705CrossRefGoogle Scholar
  62. Newville M (2001) IFEFFIT: interactive XAFS analysis and FEFF fitting. J Synchrotron Rad 8:322–324CrossRefGoogle Scholar
  63. Parker DL, Sposito G, Tebo BM (2004) Manganese(III) binding to a pyoverdine siderophore produced by a manganese(II)-oxidizing bacterium. Geochim Cosmochim Acta 68:4809–4820CrossRefGoogle Scholar
  64. 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(III)-oxidizing bacterial cultures. Geochim Cosmochim Acta 71:5672CrossRefGoogle Scholar
  65. Raymond KN, Dertz EA (2004) Biochemical and physical properties of siderophores. In: Crosa JH, Rey AR, Payne SM (eds) Iron transport in bacteria. ASM, Washington, p 3Google Scholar
  66. Rehr JJ, Kas JJ, Prange MP, Sorini AP, Takimoto Y, Vila F (2009) Ab initio theory and calculations of X-ray spectra. C R Phys 10(6):548–559CrossRefGoogle Scholar
  67. Renshaw JC, Robson GD, Trinci APJ, Wiebe MG, Livens FR, Collison D, Taylor RJ (2002) Fungal siderophores: structures, functions and applications. Mycol Res 106:1123CrossRefGoogle Scholar
  68. Roberts JG, Moody BP, McCarty GS, Sombers LA (2010) Specific oxygen-containing functional groups on the carbon surface underlie an enhanced sensitivity to dopamine at electrochemically pretreated carbon fiber microelectrodes. Langmuir 26(11):9116–9122. doi:10.1021/la9048924 PubMedCrossRefGoogle Scholar
  69. Rodgers SJ, Lee CW, Ng CY, Raymond KN (1987) Ferric ion sequestering agents. 15. Synthesis, solution chemistry, and electrochemistry of a new cationic analogue of enterobactin. Inorg Chem 26:1622–1625CrossRefGoogle Scholar
  70. Sanford AL, Morton SW, Whitehouse KL, Oara HM, Lugo-Morales LZ, Roberts JG, Sombers LA (2010) Voltammetric detection of hydrogen peroxide at carbon fiber microelectrodes. Anal Chem 82:5205–5210PubMedCrossRefGoogle Scholar
  71. Schwarzenbach G, Schwarzenbach K (1963) Hydroxamatkomplexe I. Die Stabilität der Eisen(III)-Komplexe einfacher Hydroxamsäuren und des Ferrioxamins B. Helv Chim Acta 46:1390–1400CrossRefGoogle Scholar
  72. Schweigert N, Zehnder AJB, Eggen RIL (2001) Chemical properties of catechols and their molecular modes of toxic action in cells, from microorganisms to mammals. Environ Microbiol 3(2):81–91PubMedCrossRefGoogle Scholar
  73. Selig H, Keinath TM, Weber WJ (2003) Sorption and manganese-induced oxidative coupling of hydroxylated aromatic compounds by natural geosorbents. Environ Sci Technol 37:4122–4127PubMedCrossRefGoogle Scholar
  74. Shannon RD (1976) Revised effective ionic radii and systematic studies of interatomic distances in halides and chalcogenides. Acta Crystallogr A32:751–767Google Scholar
  75. Strathmann TJ, Stone AT (2002) Reduction of the pesticides oxamyl and methomyl by Fe(II): effect of pH and inorganic ligands. Environ Sci Technol 36:653–661PubMedCrossRefGoogle Scholar
  76. 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 376:500–508CrossRefGoogle Scholar
  77. Taraz K, Ehlert G, Geisen K, Budzikiewicz H, Korth H, Pulverer Z (1990) Chemicals from bacteria. 40. Protocheline-A catecholate siderophore from a bacterium (DMS no. 5746). Z Naturforsch 45b:1327–1332Google Scholar
  78. Tebo BM, Johnson HA, McCarthy JK, Templeton AS (2005) Geomicrobiology of manganese(II) oxidation. Trends Microbiol 13(9):421–428PubMedCrossRefGoogle Scholar
  79. Tomasi J, Mennucci B, Cammi R (2005) Quantum mechanical continuum solvation models. Chem Rev 105:2999–3094PubMedCrossRefGoogle Scholar
  80. Webb SM (2005) SIXPACK: a graphical user interface for XAS analysis using IFEFFIT. Phys Scr T115:1011–1014CrossRefGoogle Scholar
  81. Webb SM, Dick GJ, Bargar JR, Tebo BM (2005a) Evidence for the presence of Mn(III) intermediates in the bacterial oxidation of Mn(II). Proc Natl Acad Sci USA 102(15):5558–5563PubMedCrossRefGoogle Scholar
  82. Webb SM, Tebo BM, Bargar JR (2005b) Structural characterization of biogenic Mn oxides produced in seawater by the marine bacillus sp. strain SG-1. Am Min 90(8–9):1342–1357CrossRefGoogle Scholar
  83. 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(7):2408–2413. doi:10.1021/Es702651f PubMedCrossRefGoogle Scholar
  84. Winkelmann G (2004) Ecology of Siderophores. In: Crosa JH, Rey AR, Payne SM (eds) Iron transport in bacteria. ASM, Washington, p 437Google Scholar
  85. Winkelmann G (2007) Ecology of siderophores with special reference to the fungi. Biometals 20:379–392PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC. 2011

Authors and Affiliations

  • James M. Harrington
    • 1
    • 5
  • John R. Bargar
    • 2
  • Andrzej A. Jarzecki
    • 3
  • James G. Roberts
    • 4
  • Leslie A. Sombers
    • 4
  • Owen W. Duckworth
    • 1
  1. 1.Soil Science DepartmentNorth Carolina State UniversityRaleighUSA
  2. 2.Stanford Synchrotron Radiation LightsourceMenlo ParkUSA
  3. 3.Chemistry DepartmentThe Brooklyn College and the Graduate School of the City University of New YorkBrooklynUSA
  4. 4.Chemistry DepartmentNorth Carolina State UniversityRaleighUSA
  5. 5.U.S. Environmental Protection AgencyNational Exposure Research LaboratoryResearch Triangle ParkUSA

Personalised recommendations