1fdd › Citations

Azotobacter vinelandii ferredoxin I. Aspartate 15 facilitates proton transfer to the reduced [3Fe-4S] cluster.

Shen B, Martin LL, Butt JN, Armstrong FA, Stout CD, Jensen GM, Stephens PJ, La Mar GN, Gorst CM, Burgess BK
J Biol Chem 268 25928-39 (1993)
Cited: 24 times
EuropePMC logo PMID: 8245026

Abstract

The [3Fe-4S]+/0 cluster of Azotobacter vinelandii ferredoxin I (AvFdI) has an unusually low and strongly pH-dependent reduction potential (E'0). The reduced cluster exists in two forms, depending upon pH, that exhibit substantially different magnetic circular dichroism (MCD) spectra. Recent studies have established that the MCD changes observed on decreasing the pH from 8.3 (alkaline form) to 6.0 (acid form) cannot be explained either by a change in spin state of the cluster (Stephens, P.J., Jensen, G.M., Devlin, F.J., Morgan, T.V., Stout, C. D., Martin, A.E., and Burgess, B.K. (1991) Biochemistry 30, 3200-3209) or by a major structural change (e.g. ligand exchange) (Stout, C.D. (1993) J. Biol. Chem. 268, 25920-25927). Here, we have examined the influence of aspartate 15 on the pH dependence of the spectroscopic and electrochemical properties of AvFdI by construction of a D15N mutant. Aspartate 15, which is salt-bridged to lysine 84 at the protein surface, is the closest ionizable residue to the [3Fe-4S] cluster. The results show that replacement of aspartate by asparagine results in an approximately 20-mV increase in E'0 for the [3Fe-4S]+/0 cluster at high pH concomitant with an approximately 0.8-pH unit decrease in the pK of the reduced form. The major pH dependence of E'0 is preserved as is the effect observed by MCD. These data eliminate the possibility that the MCD change is due to the presence of Asp-15 and support the conclusion that it originates in direct protonation of the [3Fe-4S]0 cluster, probably on a sulfide ion. Voltammetric studies show that interconversion between [3Fe-4S]+ and [3Fe-4S]0 at acidic pH involves rapid electron transfer followed by proton transfer (for reduction) and then proton transfer followed by electron transfer (for oxidation). Ionized aspartate 15 facilitates proton transfer. Thus, protonation and deprotonation are much slower for D15N relative to the native protein at pH > 5.5. Proton transfer reactions necessary for further reduction of the [3Fe-4S]0 cluster to the [3Fe-4S]- and [3Fe-4S]2- states are also retarded in D15N. The results suggest that the carboxylate-ammonium salt bridge afforded by Asp-15-Lys-84 conducts protons between the cluster and solvent H2O molecules. Overproduction of D15N FdI, but not native FdI, in A. vinelandii has a negative effect on the growth rate of the organism, suggesting that the rate of protonation or deprotonation of the [3Fe-4S]0 cluster may be important in vivo.

Articles - 1fdd mentioned but not cited (1)

  1. Theoretical investigations on Azotobacter vinelandii ferredoxin I: effects of electron transfer on protein dynamics. Meuwly M, Karplus M. Biophys J 86 1987-2007 (2004)


Reviews citing this publication (3)

  1. Metalloproteins containing cytochrome, iron-sulfur, or copper redox centers. Liu J, Chakraborty S, Hosseinzadeh P, Yu Y, Tian S, Petrik I, Bhagi A, Lu Y. Chem Rev 114 4366-4469 (2014)
  2. The structure of iron-sulfur proteins. Sticht H, Rösch P. Prog Biophys Mol Biol 70 95-136 (1998)
  3. Electron Transfer in Nitrogenase. Rutledge HL, Tezcan FA. Chem Rev 120 5158-5193 (2020)

Articles citing this publication (20)

  1. Atomically defined mechanism for proton transfer to a buried redox centre in a protein. Chen K, Hirst J, Camba R, Bonagura CA, Stout CD, Burgess BK, Armstrong FA. Nature 405 814-817 (2000)
  2. Proton-coupled electron transfer in Fe-superoxide dismutase and Mn-superoxide dismutase. Miller AF, Padmakumar K, Sorkin DL, Karapetian A, Vance CK. J Inorg Biochem 93 71-83 (2003)
  3. High-Resolution ENDOR Spectroscopy Combined with Quantum Chemical Calculations Reveals the Structure of Nitrogenase Janus Intermediate E4(4H). Hoeke V, Tociu L, Case DA, Seefeldt LC, Raugei S, Hoffman BM. J Am Chem Soc 141 11984-11996 (2019)
  4. Identification of the iron-sulfur clusters in a ferredoxin from the archaeon Sulfolobus acidocaldarius. Evidence for a reduced [3Fe-4S] cluster with pH-dependent electronic properties. Breton JL, Duff JL, Butt JN, Armstrong FA, George SJ, Pétillot Y, Forest E, Schäfer G, Thomson AJ. Eur J Biochem 233 937-946 (1995)
  5. Formation and characterization of an all-ferrous Rieske cluster and stabilization of the [2Fe-2S]0 core by protonation. Leggate EJ, Bill E, Essigke T, Ullmann GM, Hirst J. Proc Natl Acad Sci U S A 101 10913-10918 (2004)
  6. Direct electrochemistry of Megasphaera elsdenii iron hydrogenase. Definition of the enzyme's catalytic operating potential and quantitation of the catalytic behaviour over a continuous potential range. Butt JN, Filipiak M, Hagen WR. Eur J Biochem 245 116-122 (1997)
  7. Structure of Azotobacter vinelandii 7Fe ferredoxin at 1.35 A resolution and determination of the [Fe-S] bonds with 0.01 A accuracy. Stout CD, Stura EA, McRee DE. J Mol Biol 278 629-639 (1998)
  8. Identification of an Fe protein residue (Glu146) of Azotobacter vinelandii nitrogenase that is specifically involved in FeMo cofactor insertion. Ribbe MW, Bursey EH, Burgess BK. J Biol Chem 275 17631-17638 (2000)
  9. Formation and properties of a stable 'high-potential' copper-iron-sulphur cluster in a ferredoxin. Butt JN, Niles J, Armstrong FA, Breton J, Thomson AJ. Nat Struct Biol 1 427-433 (1994)
  10. Influence of electrochemical properties in determining the sensitivity of [4Fe-4S] clusters in proteins to oxidative damage. Tilley GJ, Camba R, Burgess BK, Armstrong FA. Biochem J 360 717-726 (2001)
  11. Site-directed mutagenesis of Azotobacter vinelandii ferredoxin I: cysteine ligation of the [4Fe-4S] cluster with protein rearrangement is preferred over serine ligation. Shen B, Jollie DR, Diller TC, Stout CD, Stephens PJ, Burgess BK. Proc Natl Acad Sci U S A 92 10064-10068 (1995)
  12. Entropies of redox reactions between proteins and mediators: the temperature dependence of reversible electrode potentials in aqueous buffers. Liu Y, Seefeldt LC, Parker VD. Anal Biochem 250 196-202 (1997)
  13. Electrochemical behaviour of human adrenodoxin on a pyrolytic graphite electrode. Johnson D, Norman S, Tuckey RC, Martin LL. Bioelectrochemistry 59 41-47 (2003)
  14. Protonation of bridging sulfur in cubanoid Fe4S4 clusters causes large geometric changes: the theory of geometric and electronic structure. Dance I. Dalton Trans 44 4707-4717 (2015)
  15. Voltammetric studies of the reactions of iron-sulphur clusters ([3Fe-4S] or [M3Fe-4S]) formed in Pyrococcus furiosus ferredoxin. Fawcett SE, Davis D, Breton JL, Thomson AJ, Armstrong FA. Biochem J 335 ( Pt 2) 357-368 (1998)
  16. A mediated thin-layer voltammetry method for the study of redox protein electrochemistry. Parker VD, Seefeldt LC. Anal Biochem 247 152-157 (1997)
  17. The influence of promoter and of electrode material on the cyclic voltammetry of Pisum sativum plastocyanin. Johnson DL, Maxwell CJ, Losic D, Shapter JG, Martin LL. Bioelectrochemistry 58 137-147 (2002)
  18. Water-assisted proton transfer in ferredoxin I. Lutz S, Tubert-Brohman I, Yang Y, Meuwly M. J Biol Chem 286 23679-23687 (2011)
  19. An extrusion strategy for the FeMo cofactor from nitrogenase. Towards synthetic iron-sulfur proteins. Martin LL, West LC, Wu B. Eur J Biochem 268 5676-5686 (2001)
  20. Some fundamental insights into biological redox catalysis from the electrochemical characteristics of enzymes attached directly to electrodes. Armstrong FA. Electrochim Acta 390 138836 (2021)


Related citations provided by authors (12)

  1. Crystallographic Analysis of Two Site-Directed Mutants of Azotobacter Vinelandii Ferredoxin. Soman J, Iismaa S, Stout CD J. Biol. Chem. 266 21558- (1991)
  2. Site-Directed Mutagenesis of Azotobacter Vinelandii Ferredoxin I. (Fe-S) Cluster-Driven Protein Rearrangement. Martin AE, Burgess BK, Stout CD, Cash VL, Dean DR, Jensen GM, Stephens PJ Proc. Natl. Acad. Sci. U.S.A. 87 598- (1990)
  3. Refinement of the 7 Fe Ferredoxin from Azotobacter at 1.9 Angstroms Resolution. Stout CD J. Mol. Biol. 205 545- (1989)
  4. 7-Iron Ferredoxin Revisited. Stout CD J. Biol. Chem. 263 9256- (1988)
  5. (4Fe-4S)-Cluster-Depleted Azotobacter Vinelandii Ferredoxin I. A New 3Fe Iron-Sulfur Protein. Stephens PJ, Morgan TV, Devlin F, Penner-Hahn JE, Hodgson KO, Scott RA, Stout CD, Burgess BK Proc. Natl. Acad. Sci. U.S.A. 82 5661- (1985)
  6. Structure of Azotobacter Vinelandii 7Fe Ferredoxin. Amino Acid Sequence and Electron Density Maps of Residues. Howard JB, Lorsbach TW, Ghosh D, Melis K, Stout CD J. Biol. Chem. 258 508- (1983)
  7. Iron-Sulfur Clusters and Protein Structure of Azotobacter Ferredoxin at 2.0 Angstroms Resolution. Ghosh D, O'Donnell S, Fureyjunior W, Robbins AH, Stout CD J. Mol. Biol. 158 73- (1982)
  8. Structure of a 7Fe Ferredoxin from Azotobacter Vinelandii. Ghosh D, Fureyjunior W, O'Donnell S, Stout CD J. Biol. Chem. 256 4185- (1981)
  9. Iron-Sulfur Clusters in Azotobacter Ferredoxin at 2.5 Angstroms Resolution. Stout CD, Ghosh D, Pattabhi V, Robbins AH J. Biol. Chem. 255 1797- (1980)
  10. Structure of the Iron-Sulfur Clusters in Azotobacter Ferredoxin at 4.0 Angstroms Resolution. Stout CD Am. Cryst. Assoc. Abstr. Papers (Annual Meeting) 6 97- (1979)
  11. Two Crystal Forms of Azotobacter Ferredoxin. Stout CD J. Biol. Chem. 254 3598- (1979)
  12. Structure of the Iron-Sulphur Clusters in Azotobacter Ferredoxin at 4.0 Angstroms Resolution. Stout CD Nature 279 83- (1979)

Quick links