Substrate Interactions with Nitrogenase: Fe versus Mo

Biochemistry

Volumn 43, Issue 6, 2004, Pages 1401-1409

  Seefeldt, Lance C ^a   Dance, Ian G ^b   Dean, Dennis R ^c  

^a UTAH STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

^c VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CATALYSIS; NITROGEN; ORGANOMETALLICS; REDUCTION;

METALLOCLUSTERS;

ENZYME KINETICS;

CITRIC ACID; HOMOCITRATE; IRON; MOLYBDENUM; NITROGEN; NITROGENASE; UNCLASSIFIED DRUG;

BINDING SITE; BIOPHYSICS; CALCULATION; CATALYSIS; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME KINETICS; ENZYME MECHANISM; ENZYME METABOLISM; ENZYME SUBSTRATE; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; REDUCTION; REVIEW; THEORY;

BACTERIAL PROTEINS; BINDING, COMPETITIVE; ENZYME INHIBITORS; IRON; MODELS, CHEMICAL; MOLYBDENUM; MOLYBDOFERREDOXIN; NITROGENASE; SUBSTRATE SPECIFICITY;

EID: 1142275465     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi036038g     Document Type: Review

References (86)

1. Smil, V. (2001) Enriching the Earth: Fritz Haber, Carl Bosch, and the Transformation of World Food Production, MIT Press, Cambridge, MA.
2. Burgess, B. K., and Lowe, D. J. (1996) The mechanism of molybdenum nitrogenase, Chem. Rev. 96, 2983-3011.
3. Rees, D. C., and Howard, J. B. (2000) Nitrogenase: standing at the crossroads, Curr. Opin. Chem. Biol. 4, 559-566.
4. Georgiadis, M. M., Komiya, H., Chakrabarti, P., Woo, D., Kornuc, J. J., and Rees, D. C. (1992) Crystallographic structure of the nitrogenase iron protein from Azotobacter vinelandii, Science 257, 1653-1659.
5. Seefeldt, L. C., and Dean, D. R. (1997) Role of nucleotides in nitrogenase catalysis, Acc. Chem. Res. 30, 260-266.
6. Howard, J. B., and Rees, D. C. (1994) Nitrogenase: A nucleotide-dependent molecular switch, Annu. Rev. Biochem. 63, 235-264.
7. Kim, J., and Rees, D. C. (1992) Crystallographic structure and functional implications of the nitrogenase molybdenum iron protein from Azotobacter vinelandii, Nature 360, 553-560.
8. 4-stabilized nitrogenase complex and its implications for signal transduction, Nature 387, 370-376.
9. Chiu, H.-J., Peters, J. W., Lanzilotta, W. N., Ryle, M. J., Seefeldt, L. C., Howard, J. B., and Rees, D. C. (2001) MgATP-bound and nucleotide-free structures of a nitrogenase protein complex between the Leu 127-Delta-Fe-protein and the MoFe-protein, Biochemistry 40, 641-650.
10. Einsle, O., Tezcan, F. A., Andrade, S. L. A., Schmid, B., Yoshida, M., Howard, J. B., and Rees, D. C. (2002) Nitrogenase MoFe-protein at 1.16 angstrom resolution: A central ligand in the FeMo-cofactor, Science 297, 1696-1700.
11. Dance, I. (2003) The consequences of an interstitial N atom in the FeMo cofactor of nitrogenase, Chem. Commun., 324-325.
12. Lee, H. I., Benton, P. M., Laryukhin, M., Igarashi, R. Y., Dean, D. R., Seefeldt, L. C., and Hoffman, B. M. (2003) The interstitial atom of the nitrogenase FeMo-cofactor: ENDOR and ESEEM show it is not an exchangeable nitrogen, J. Am. Chem. Soc. 125, 5604-5605.
13. Lovell, T., Liu, T., Case, D. A., and Noodleman, L. (2003) Structural, spectroscopic, and redox consequences of a central ligand in the FeMoco of nitrogenase: A density functional theoretical study, J. Am. Chem. Soc. 125, 8377-8383.
14. Hinnemann, B., and Norskov, J. K. (2003) Modeling a central ligand in the nitrogenase FeMo cofactor, J. Am. Chem. Soc. 125, 1466-1467.
15. McLean, P. A., and Dixon, R. A. (1981) Requirement of nifV gene for production of wild-type nitrogenase enzyme in Klebsiella pneumoniae, Nature 292, 655-656.
16. Shah, V. K., and Brill, W. J. (1977) Isolation of an iron-molybdenum cofactor from nitrogenase, Proc. Natl. Acad. Sci. U.S.A. 74, 3249-3253.
17. Jang, S. B., Seefeldt, L. C., and Peters, J. W. (2000) Insights into nucleotide signal transduction in nitrogenase: Structure of an iron protein with MgADP bound, Biochemistry 39, 14745-14752.
18. Mayer, S. M., Lawson, D. M., Gormal, C. A., Roe, S. M., and Smith, B. E. (1999) New insights into structure-function relationships in nitrogenase: A 1.6 Å resolution X-ray crystallographic study of Klebsiella pneumoniae MoFe-protein, J. Mol. Biol. 292, 871-891.
19. Thorneley, R. N. F., and Lowe, D. J. (1985) Kinetics and mechanisms of the nitrogenase enzyme system, in Molybdenum Enzymes (Spiro, T. G., Ed.) pp 221-284, Wiley, New York.
20. Kim, J., and Rees, D. C. (1992) Structural models for the metal centers in the nitrogenase molybdenum-iron protein, Science 257, 1677-1682.
21. Kim, J., Woo, D., and Rees, D. C. (1993) X-ray crystal structure of the nitrogenase molybdenum-iron protein from Clostridium pasteurianum at 3. 0-Å resolution, Biochemistry 32, 7104-7115.
22. Orme-Johnson, W. H., Hamilton, W. D., Jones, T. L., Tso, M. Y. W., Burris, R. H., Shah, V. K., and Brill, W. J. (1972) Electron paramagnetic resonance of nitrogenase and nitrogenase components from Clostridium pasteurianum W5 and Azotobacter vinelandii OP, Proc. Natl. Acad. Sci. U.S.A. 69, 3142-3145.
23. Lindahl, P. A., Papaefthymiou, V., Orme-Johnson, W. H., and Münck, E. (1988) Mössbauer studies of solid thionin-oxidized MoFe protein of nitrogenase, J. Biol. Chem. 263, 19412-19418.
24. Zimmermann, R., Münck, E., Brill, W. J., Shah, V. K., Henzl, M. T., Rawlings, J., and Orme-Johnson, W. H. (1978) Nitrogenase X: Mössbauer and EPR studies on reversibly oxidized MoFe protein from Azotobacter vinelandii OP: Nature of the iron centers, Biochim. Biophys. Acta 537, 185-207.
25. Schultz, F. A., Gheller, S. F., and Newton, W. E. (1988) Iron molybdenum cofactor of nitrogenase: electrochemical determination of the electron stoichiometry of the oxidized semi-reduced couple, Biochem. Biophys. Res. Commun. 152, 629-635.
26. O'Donnell, M. J., and Smith, B. E. (1978) Electron paramagnetic resonance studies on the redox properties of the molybdenum iron protein of nitrogenase between +50 and -450 mV, Biochem. J. 173, 831-839.
27. Huynh, B. H., Henzl, M. T., Christner, J. A., Zimmermann, R., Orme-Johnson, W. H., and Münck, E. (1980) Nitrogenase XII: Mössbauer studies of the MoFe protein from Clostridium pasteurianum W5, Biochim. Biophys. Acta 623, 124-138.
28. 57Fe enrichment of the M-centers, J. Am. Chem. Soc. 122, 4926-4936.
29. Watt, G. D., Burns, A., Lough, S., and Tennent, D. L. (1980) Redox and spectroscopic properties of oxidized MoFe protein from Azotobacter vinelandii, Biochemistry 19, 4926-4932.
30. DeRose, V. J., Kim, C. H., Newton, W. E., Dean, D. R., and Hoffman, B. M. (1995) Electron-spin-echo envelope modulation spectroscopic analysis of altered nitrogenase MoFe proteins from Azotobacter vinelandii, Biochemistry 34, 2809-2814.
31. Smith, B. E., Durrant, M. C., Fairhurst, S. A., Gormal, C. A., Gronberg, K. L. C., Henderson, R. A., Ibrahim, S. K., Le Gall, T., and Pickett, C. J. (1999) Exploring the reactivity of the isolated iron-molybdenum cofactor of nitrogenase, Coord. Chem. Rev. 185-186, 669-687.
32. Simpson, F. B., and Burris, R. H. (1984) A nitrogen pressure of 50 atmospheres does not prevent evolution of hydrogen by nitrogenase, Science 224, 1095-1097.
33. Dilworth, M. J. (1966) Acetylene reduction by nitrogen-fixing prepartions from Clostridium pasteurianum, Biochim. Biophys. Acta 127, 285-294.
34. Davis, L. C., Henzl, M. T., Burris, R. H., and Orme-Johnson, W. H. (1979) Iron-sulfur clusters in the molybdenum-iron protein component of nitrogenase. Electron paramagnetic resonance of the carbon monoxide inhibited state, Biochemistry 18, 4860-4869.
35. Rivera-Ortiz, J. M., and Burris, R. H. (1975) Interactions among substrates and inhibitors of nitrogenase, J. Bacteriol. 123, 537-545.
36. 2 on the distribution of electrons to alternative substrates, Biochim. Biophys. Acta 403, 67-78.
37. 2 on HD formation by various nitrogenases, Biochemistry 22, 4472-4480.
38. 2, Biochemistry 22, 5111-5122.
39. Shen, J., Dean, D. R., and Newton, W. E. (1997) Evidence for multiple substrate-reduction sites and distinct inhibitor-binding sites from an altered Azotobacter vinelandii nitrogenase MoFe protein, Biochemistry 36, 4884-4894.
40. Kim, C. H., Newton, W. E., and Dean, D. R. (1995) Role of the MoFe protein alpha-subunit histidine-195 residue in FeMo-cofactor binding and nitrogenase catalysis, Biochemistry 34, 2798-2808.
41. Fisher, K., Dilworth, M. J., Kim, C. H., and Newton, W. E. (2000) Azotobacter vinelandii nitrogenases containing altered MoFe proteins with substitutions in the FeMo-cofactor environment: effects on the catalyzed reduction of acetylene and ethylene, Biochemistry 39, 2970-2979.
42. Christiansen, J., Seefeldt, L. C., and Dean, D. R. (2000) Competitive substrate and inhibitor interactions at the physiologically relevant active site of nitrogenase, J. Biol. Chem. 275, 36104-36107.
43. Chatt, J., Dilworth, J. R., and Richards, R. L. (1978) Recent advances in the chemistry of nitrogen fixation, Chem. Rev. 78, 589-625.
44. Barriere, F. (2003) Modeling of the molybdenum center in the nitrogenase FeMo-cofactor, Coord. Chem. Rev. 236, 71-89.
45. Pickett, C. J. (1996) The Chatt cycle and the mechanism of enzymic reduction of molecular nitrogen, J. Biol. Inorg. Chem. 1, 601-606.
46. 4-polycarboxylate clusters. Possible relevance regarding the function of the molybdenum-coordinated homocitrate in nitrogenase, Inorg. Chem. 35, 4038-4046.
47. Malinak, S. M., and Coucouvanis, D. (2001) The chemistry of synthetic Fe-Mo-S clusters and their relevance to the structure and function of the Fe-Mo-S center in nitrogenase, Prog. Inorg. Chem. 49, 599-662.
48. Yandulov, D. V., and Schrock, R. R. (2003) Catalytic reduction of dinitrogen to ammonia at a single molybdenum center, Science 301, 76-78.
49. Schrock, R. R. (2003) Catalytic reduction of dinitrogen under mild conditions, Chem. Commun., 2389-2391.
50. Hoover, T. R., Imperial, J., Ludden, P. W., and Shah, V. K. (1988) Dinitrogenase with altered substrate specificity results from the use of homocitrate analogues for in vitro synthesis of the iron-molybdenum cofactor, Biochemistry 27, 3647-3652.
51. Madden, M. S., Paustian, T. D., Ludden, P. W., and Shah, V. K. (1991) Effects of homocitrate, homocitrate lactone, and fluorochomocitrate on nitrogenase in nifV-mutants of Azotobacter vinelandii, J. Bacteriol. 173, 5403-5405.
52. Hawkes, T. R., McLean, P. A., and Smith, B. E. (1984) Nitrogenase from nifV mutants of Klebsiella pneumoniae contains an altered form of the iron-molybdenum cofactor, Biochem. J. 217, 317-321.
53. Mayer, S. M., Gormal, C. A., Smith, B. E., and Lawson, D. M. (2002) Crystallographic analysis of the MoFe protein of nitrogenase from a nifV mutant of Klebsiella pneumoniae identifies citrate as a ligand to the molybdenum of iron molybdenum cofactor (FeMoco), J. Biol. Chem. 277, 35263-35266.
54. Gronberg, K. L. C., Gormal, C. A., Durrant, M. C., Smith, B. E., and Henderson, R. A. (1998) Why R-homocitrate is essential to the reactivity of FeMo-cofactor of nitrogenase: Studies on NifV-(-)-extracted FeMo-cofactor, J. Am. Chem. Soc. 120, 10613-10621.
55. Imperial, J., Hoover, T. R., Madden, M. S., Ludden, P. W., and Shah, V. K. (1989) Substrate reduction properties of dinitrogenase activated in vitro are dependent upon the presence of homocitrate or its analogues during iron-molybdenum cofactor synthesis, Biochemistry 28, 7796-7799.
56. Scott, D. J., Dean, D. R., and Newton, W. E. (1992) Nitrogenase-catalyzed ethane production and CO-sensitive hydrogen evolution from MoFe proteins having amino acid substitutions in an α-subunit FeMo cofactor-binding domain, J. Biol. Chem. 267, 20002-20010.
57. Eady, R. R., Robson, R. L., and Smith, B. E. (1988) Alternative and conventional nitrogenases, in The Nitrogen and Sulfur Cycles (Cole, J. A., and Ferguson, S., Eds.) pp 363-382, University Press, Cambridge, MA.
58. Eady, R. R. (1996) Structure-function relationships of alternative nitrogenases, Chem. Rev. 96, 3013-3030.
59. Durrant, M. C. (2001) A molybdenum-centered model for nitrogenase catalysis, Inorg. Chem. Commun. 4, 60-62.
60. Durrant, M. C. (2002) An atomic-level mechanism for molybdenum nitrogenase. Part 1. Reduction of dinitrogen, Biochemistry 41, 13934-13945.
61. Durrant, M. C. (2002) An atomic-level mechanism for molybdenum nitrogenase. Part 2. Proton reduction, inhibition of dinitrogen reduction by dihydrogen, and the HD formation reaction, Biochemistry 41, 13946-13955.
62. Szilagyi, R. K., Musaev, D. G., and Morokuma, K. (2001) Theoretical studies of biological nitrogen fixation. I. Density functional modeling of the Mo-site of the FeMo-cofactor, Inorg. Chem. 40, 766-775.
63. 3, J. Am. Chem. Soc. 112, 4831-4841.
64. 4′2-dianion of 2,2′ -bis[(2-mercaptophenyl)thio]diethylamine), Inorg. Chem. 31, 3711-3717.
65. Buys, I. E., Field, L. D., Hambley, T. W., and McQueen, A. E. D. (1993) Structure of bis[1,2-bis(diethylphosphino)ethane-P, P′ ]-hydrido(dinitrogen-N)iron(II) tetraphenylborate, Acta Crystallogr. C49, 1056-1059.
66. Albertin, G., Antoniutti, S., Bordignon, E., and Pattaro, S. (1997) Synthesis, characterization and reactivity of hydrazine complexes of iron(II), J. Chem. Soc., Dalton Trans., 4445-4454.
67. 2, Inorg. Chem. 41, 3491-3499.
68. Betley, T. A., and Peters, J. C. (2003) Dinitrogen chemistry from trigonally coordinated iron and cobalt platforms, J. Am. Chem. Soc. 125, 10782-10783.
69. Lehnert, N., Wiesler, B. E., Tuczek, F., Hennige, A., and Sellmann, D. (1997) Activation of diazene and the nitrogenase problem: an investigation of diazene-bridged Fe(II) centers with sulfur ligand sphere. 1. Electronic structure, J. Am. Chem. Soc. 119, 8869-8878.
70. 2 dependent HD formation: a model reaction and its significance for the FeMoco function, Coord. Chem. Rev. 200-202, 545-561.
71. Bozso, F., Ertl, G., and Weiss, M. (1977) Interaction of nitrogen with iron surfaces, J. Catal. 50, 519-529.
72. Dorr, M., Kassbohrer, J., Grunert, R., Kreisel, G., Brand, W. A., Werner, R. A., Geilmann, H., Apfel, C., Robl, C., and Weigand, W. (2003) A possible prebiotic formation of ammonia from dinitrogen on iron sulfide surfaces, Angew. Chem., Int. Ed., Engl. 42, 1540-1543.
73. Hwang, J. C., Chen, C. H., and Burris, R. H. (1973) Inhibition of nitrogenase-catalyzed reductions, Biochim. Biophys. Acta 292, 256-270.
74. 1H Q-band ENDOR investigation, J. Am. Chem. Soc. 119, 10121-10126.
75. 57Fe isotopomers, J. Am. Chem. Soc. 118, 8707-8709.
76. 1H ENDOR, J. Am. Chem. Soc. 122, 5582-5587.
77. Sørlie, M., Christiansen, J., Dean, D. R., and Hales, B. J. (1999) Detection of a new radical and FeMo-cofactor EPR signal during acetylene reduction by the α-H195Q mutant of nitrogenase, J. Am. Chem. Soc. 121, 9457-9458.
78. Ryle, M. J., Lee, H. I., Seefeldt, L. C., and Hoffman, B. M. (2000) Nitrogenase reduction of carbon disulfide: freeze-quench EPR and ENDOR evidence for three sequential intermediates with cluster-bound carbon moieties, Biochemistry 39, 1114-1119.
79. Christiansen, J., Cash, V. L., Seefeldt, L. C., and Dean, D. R. (2000) Isolation and characterization of an acetylene-resistant nitrogenase, J. Biol. Chem. 275, 11459-11464.
80. Mayer, S. M., Niehaus, W. G., and Dean, D. R. (2002) Reduction of short chain alkynes by a nitrogenase alpha-70Ala-substituted MoFe protein, J. Chem. Soc., Dalton Trans. 5, 802-807.
81. Benton, P. M. C., Laryukhin, M., Mayer, S. M., Hoffman, B. M., Dean, D. R., and Seefeldt, L. C. (2003) Localization of a substrate binding site on FeMo-cofactor in nitrogenase: trapping propargyl alcohol with an α-70-substituted MoFe protein, Biochemistry 42, 9102-9109.
82. Deeth, R. J., and Field, C. N. (1994) A computational study of metal-dinitrogen co-ordination, J. Chem. Soc., Dalton Trans., 1943-1948.
83. Siegbahn, P. E. M., Westerberg, J., Svensson, M., and Crabtree, R. H. (1998) Nitrogen fixation by nitrogenases: A quantum chemical study, J. Phys. Chem. B 102, 1615-1623.
84. Reiher, M., and Hess, B. A. (2002) A quantum-chemical study of dinitrogen reduction at mononuclear iron-sulfur complexes with hints to the mechanism of nitrogenase, Chem. Eur. J. 8, 5332-5339.
85. Rod, T. H., and Norskov, J. K. (2000) Modeling the nitrogenase FeMo cofactor, J. Am. Chem. Soc. 122, 12751-12763.
86. Fisher, K., Newton, W. E., and Lowe, D. J. (2001) Electron paramagnetic resonance analysis of different Azotobacter vinelandii nitrogenase MoFe-protein conformations generated during enzyme turnover: Evidence for S = 3/2 spin states from reduced MoFe-protein intermediates, Biochemistry 40, 3333-3339.