Assembly of nitrogenase MoFe protein

Biochemistry

Volumn 47, Issue 13, 2008, Pages 3973-3981

  Hu, Yilin ^a   Fay, Aaron W ^a   Chi, Chung Lee ^a   Yoshizawa, Janice ^a   Ribbe, Markus W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; CHARACTERIZATION;

BIOINORGANIC CHEMISTRY; FEMOCO BIOSYNTHESIS;

PROTEINS;

MOLYBDENUM IRON PROTEIN; NITROGENASE;

ALPHA CHAIN; BETA CHAIN; BIOSYNTHESIS; CRYSTAL STRUCTURE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; REVIEW;

ELECTROSTATICS; MODELS, MOLECULAR; MOLYBDOFERREDOXIN; PROTEIN CONFORMATION;

EID: 41449113502     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi7025003     Document Type: Review

References (72)

1. Burgess, B. K., and Lowe, D. J. (1996) Mechanism of molybdenum nitrogenase. Chem. Rev. 96, 2983-3012.
2. Howard, J. B., and Rees, D. C. (1996) Structural basis of biological nitrogen fixation. Chem. Rev. 96, 2965-2982.
3. Smith, B. E. (1999) Structure, function, and biosynthesis of the metallosulfur clusters in nitrogenases. Adv. Inorg. Chem. 47, 159-218.
4. Rees, D. C., Tezcan, F. A., Haynes, C. A., Walton, M. Y., Andrade, S., Einsle, O., and Howard, J. B. (2005) Structural basis of biological nitrogen fixation. Philos. Trans. R. Soc. London, Ser. A 363, 971-984.
5. 2? A mechanistic overview of biological nitrogen fixation. Proc. Natl. Acad. Sci U.S.A. 103, 17088-17093.
6. Peters, J. W., and Szilagyi, R. K. (2006) Exploring new frontiers of nitrogenase structure and mechanism. Curr. Opin. Chem. Biol. 10, 101-108.
7. 2 by a Mo-CO dehydrogenase. J. Biol. Chem. 272, 26627-26633.
8. Einsle, O., Tezcan, F. A., Andrade, S. L., Schmid, B., Yoshida, M., Howard, J. B., and Rees, D. C. (2002) Nitrogenase MoFe-protein at 1.16 Å resolution: A central ligand in the FeMo-cofactor. Science 297, 1696-1700.
9. 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.
10. Schindelin, H., Kisker, C., Schlessman, J. L., Howard, J. B., and Rees, D. C. (1997) Structure of ADP-AHV-stabilized nitrogenase complex and its implications for signal transduction. Nature 387, 370-376.
11. N clusters. Inorg. Chem. 46, 9192-9200.
12. z: Synthesis, structures, and electron transfer series. Inorg. Chem. 45, 1997-2007.
13. N-type clusters topologically related to the nitrogenase P-cluster. Inorg. Chem. 43, 674-682.
14. 8 double cubane. J. Am. Chem. Soc. 125, 3910-3920.
15. N cluster of nitrogenase. Inorg. Chem. 42, 4624-4631.
16. Ohki, Y., Ikagawa, Y., and Tatsumi, K. (2007) Synthesis of new [8Fe-7S] clusters: A topological link between the core structures of P-cluster, FeMo-co, and FeFe-co of nitrogenases. J. Am. Chem. Soc. 129, 10457-10465.
17. Ohki, Y., Sunada, Y., Honda, M., Katada, M., and Tatsumi, K. (2003) Synthesis of the P-cluster inorganic core of nitrogenases. J. Am. Chem. Soc. 125, 4052-4053.
18. Zimmermann, R., Orme-Johnson, W. H., Münck, E., Shah, V. K., Brill, W. I., Henzl, M. T., and Rawlings, J. (1978) Nitrogenase-X: Mössbauer and EPR studies on reversibly oxidized MoFe protein from Azotobacter vinelandii OP: Nature of iron centers. Biochim. Biophys. Acta 537, 185-207.
19. ox is a non-Kramers system with a nearly degenerate ground doublet. J. Am. Chem. Soc. 114, 8579-8590.
20. 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.
21. Pierik, A. J., Wassink, H., Haaker, H., and Hagen, W. R. (1993) Redox properties and EPR spectroscopy of the P-clusters of Azotobacter vinelandii MoFe Protein. Eur. J. Biochem. 212, 51-61.
22. Chan, M. K., Kim, J., and Rees, D. C. (1993) The nitrogenase FeMo-cofactor and P-cluster pair: 2.2 A resolution structures. Science 260, 792-794.
23. Peters, J. W., Stowell, M. H., Soltis, S. M., Finnegan, M. G., Johnson, M. K., and Rees, D. C. (1997) Redox-dependent structural changes in the nitrogenase P-cluster. Biochemistry 36, 1181-1187.
24. 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.
25. Burgess, B. K. (1990) The iron molybdenum cofactor of nitrogenase. Chem. Rev. 90, 1377-1406.
26. Hinnemann, B., and Norskov, J. K. (2003) Modeling a central ligand in the nitrogenase FeMo cofactor. J. Am. Chem. Soc. 125, 1466-1467.
27. Lovell, T., Liu, T. Q., Case, D. A., and Noodleman, L. (2003) Structural, spectroscopic, and redox consequences of central ligand in the FeMoco of nitrogenase: A density functional theoretical study. J. Am. Chem. Soc. 125, 8377-8383.
28. Dance, I. (2003) The consequences of an interstitial N atom in the FeMo cofactor of nitrogenase. Chem. Commun. 3, 324-325.
29. Vrajmasu, V., Münck, E., and Bominaar, E. L. (2003) Density functional study of the electric hyperfine interactions and the redox-structural correlations in the cofactor of nitrogenase. Analysis of general trends in Fe-57 isomer shifts. Inorg. Chem. 42, 5974-5988.
30. Yang, T. C., Maeser, N. K., Laryukhin, M., Lee, H. I., Dean, D. R., Seefeldt, L. C., and Hoffman, B. M. (2005) The interstitial atom of the nitrogenase FeMo-Cofactor: ENDOR and ESEEM evidence that it is not a nitrogen. J. Am. Chem. Soc. 127, 12804-12805.
31. Lee, H.-I., Hales, B. J., and Hoffman, B. M. (1997) Metal-ion valencies of the FeMo cofactor in CO-inhibited and resting state nitrogenase by Fe-57 Q-band ENDOR. J. Am. Chem. Soc. 119, 11395-11400.
32. 57 enrichment of the M-centers. J. Am. Chem. Soc. 122, 4926-4936.
33. Dos Santos, P. C., Dean, D. R., Hu, Y. L., and Ribbe, M. W. (2004) Formation and insertion of the nitrogenase iron-molybdenum cofactor. Chem. Rev. 104, 1159-1173.
34. Hu, Y., Corbett, M. C., Fay, A. W., Webber, J. A., Hodgson, K. O., Hedman, B., and Ribbe, M. W. (2006) FeMo cofactor maturation on NifEN. Proc. Natl. Acad. Sci. U.S.A. 103, 17119-17124.
35. Frazzon, J., and Dean, D. R. (2002) Biosynthesis of the nitrogenase iron-molybdenum-cofactor from Azotobacter vinelandii. Met. Ions Biol. Syst. 39, 163-186.
36. Yuvaniyama, P., Agar, J. N., Cash, V. L., Johnson, M. K., and Dean, D. R. (2000) NifS-directed assembly of a transient [2Fe-2S] cluster within the NifU protein. Proc. Natl. Acad. Sci. U.S.A. 97, 599-604.
37. Agar, J. N., Yuvaniyama, P., Jack, R. F., Cash, V. L., Smith, A. D., Dean, D. R., and Johnson, M. K. (2000) Modular organization and identification of a mononuclear iron-binding site within the NifU protein. J. Biol. Inorg. Chem. 5, 167-177.
38. Dos Santos, P. C., Smith, A. D., Frazzon, J., Cash, V. L., Johnson, M. K., and Dean, D. R. (2004) Iron-sulfur cluster assembly: NifU-directed activation of the nitrogenase Fe protein. J. Biol. Chem. 279, 19705-19711.
39. Smith, A. D., Jameson, G. N. L., Dos Santos, P. C., Agar, J. N., Naik, S., Krebs, C., Frazzon, J., Dean, D. R., Huynh, B. H., and Johnson, M. K. (2005) NifS-mediated assembly of [4Fe-4S] clusters in the N- and C-terminal domains of the NifU scaffold protein. Biochemistry 44, 12955-12969.
40. Allen, R. M., Chatterjee, R., Ludden, P. W., and Shah, V. K. (1995) Incorporation of iron and sulfur from NifB cofactor into the iron-molybdenum cofactor of dinitrogenase. J. Biol. Chem. 270, 26890-26896.
41. Roll, J. T., Shah, V. K., Dean, D. R., and Roberts, G. P. (1995) Characteristics of NifNE in Azotobacter vinelandii strains: Implications for the synthesis of the iron-molybdenum cofactor of dinitrogenase. J. Biol. Chem. 270, 4432-4437.
42. Goodwin, P. J., Agar, J. N., Roll, J. T., Roberts, G. P., Johnson, M. K., and Dean, D. R. (1998) The Azotobacter vinelandii NifEN complex contains two identical [4Fe-4S] clusters. Biochemistry 37, 10420-10428.
43. Hoover, T. R., Robertson, A. D., Cerny, R. L., Hayes, R. N., Imperial, J., Shah, V. K., and Ludden, P. W. (1987) Identification of the V-factor needed for synthesis of the iron-molybdenum cofactor of nitrogenase as homocitrate. Nature 329, 855-857.
44. Zheng, L. M., White, R. H., and Dean, D. R. (1997) Purification of the Azotobacter vinelandii nifV-encoded homocitrate synthase. J. Bacteriol. 179, 5963-5966.
45. Dean, D. R., and Jacobson, M. R. (1992) Biochemical genetics of Nitrogenase, in Biological Nitrogen Fixation (Stacey, G., Burris, R. H., and Evans, H. J., Eds.) pp 763-834, Chapman & Hall, New York.
46. Curatti, L., Hernandez, J. A., Igarashi, R. Y., Soboh, B., Zhao, D., and Rubio, L. M. (2007) In vitro synthesis of the iron-molybdenum cofactor of nitrogenase from iron, sulfur, molybdenum, and homocitrate using purified proteins. Proc. Natl. Acad. Sci. U.S.A. 104, 17626-17631.
47. Curatti, L., Ludden, P. W., and Rubio, L. M. (2006) NifB-dependent in vitro synthesis of the iron-molybdenum cofactor of nitrogenase. Proc. Natl. Acad. Sci. U.S.A. 103, 5297-5301.
48. Hu, Y., Fay, A. W., and Ribbe, M. W. (2005) Identification of a nitrogenase iron-molybdenum cofactor precursor on NifEN complex. Proc. Natl. Acad. Sci. U.S.A. 102, 3236-3241.
49. Brigle, K. E., Weiss, M. C., Newton, W. E., and Dean, D. R. (1987) Products of the iron-molybdenum cofactor-specific biosynthetic genes, nifE and nifN, are structurally homologous to the products of the nitrogenase molybdenum-iron protein genes, nifD and nifK. J. Bacteriol. 169, 1547-1553.
50. Corbett, M. C., Hu, Y., Fay, A. W., Ribbe, M. W., Hedman, B., and Hodgson, K. O. (2006) Structural insights into a protein-bound iron-molybdenum cofactor precursor. Proc. Natl. Acad. Sci. U.S.A. 103, 1238-1243.
51. George, S. J., Igarashi, R. Y., Piamonteze, C., Soboh, B., Cramer, S. P., and Rubio, L. M. (2007) Identification of a Mo-Fe-S cluster on NifEN by Mo K-edge extended X-ray absorption fine structure. J. Am. Chem. Soc. 129, 3060-3601.
52. Soboh, B., Igarashi, R. Y., Hernandez, J. A., and Rubio, L. M. (2006) Purification of a NifEN protein complex that contains bound molybdenum and a FeMo-Co precursor from an Azotobacter vinelandii ΔnifHDK strain. J. Biol. Chem. 281, 36701-36709.
53. Hu, Y., Corbett, M. C., Fay, A. W., Webber, J. A., Hodgson, K. O., Hedman, B., and Ribbe, M. W. (2006) Nitrogenase Fe protein: A moybdate/homocitrate insertase. Proc. Natl. Acad. Sci. U.S.A. 103, 17125-17130.
54. Homer, M. J., Paustian, T. D., Shah, V. K., and Roberts, G. P. (1993) The NifY product of Klebsiella pneumoniae is associated with apodinitrogenase and dissociates upon activation with the iron-molybdenum cofactor. J. Bacteriol. 175, 4907-4910.
55. White, T. C., Harris, G. S., and Orme-Johnson, W. (1992) Electrophoretic studies on the assembly of the nitrogenase molybdenum-iron protein from the Klebsiella pneumoniae nifD and nifK gene-products. J. Biol. Chem. 267, 24007-24016.
56. Homer, M. J., Dean, D. R., and Roberts, G. P. (1995) Characterization of the gamma-protein and its involvement in the metallocluster assembly and maturation of dinitrogenase from Azotobacter vinelandii. J. Biol. Chem. 270, 24745-24752.
57. Lukoyanov, D., Pelmenschikov, V., Maeser, N., Laryukhin, M., Yang, T. C., Noodleman, L., Dean, D. R., Case, D. A., Seefeldt, L. C., and Hoffman, B. M. (2007) Testing if the interstitial atom, X, of the nitrogenase molybdenum-iron cofactor is N or C: ENDOR, ESEEM, and DFT studies of the S = 3/2 resting state in multiple environments. Inorg. Chem. 46, 11437-11449.
58. Hernandez, J. A., Igarashi, R. Y., Soboh, B., Curatti, L., Dean, D. R., Ludden, P. W., and Rubio, L. M. (2007) NifX and NifEN exchange NifB cofactor and the VK-cluster, a newly isolated intermediate of the iron-molybdenum cofactor biosynthetic pathway. Mol. Microbiol. 63, 177-192.
59. Ribbe, M. W., and Burgess, B. K. (2001) The chaperone GroEL is required for the final assembly of the molybdenum-iron protein of nitrogenase. Proc. Natl. Acad. Sci. U.S.A. 98, 5521-5525.
60. Schmid, B., Ribbe, M. W., Einsle, O., Yoshida, M., Thomas, L. M., Dean, D. R., Rees, D. C., and Burgess, B. K. (2002) Structure of a cofactor-deficient nitrogenase MoFe protein. Science 296, 352-356.
61. Hu, Y., Fay, A. W., Schmid, B., Makar, B., and Ribbe, M. W. (2006) Molecular insights into nitrogenase FeMoco insertion: Trp 444 of MoFe protein α subunit locks FeMoco in its binding site. J. Biol. Chem. 281, 30534-30541.
62. Hu, Y., Fay, A. W., and Ribbe, M. W. (2007) Molecular insights into nitrogenase FeMoco insertion: The role of His362 of MoFe protein α subunit in FeMoco incorporation. J. Biol. Inorg. Chem. 12, 449-460.
63. Fay, A. W., Hu, Y., Schmid, B., and Ribbe, M. W. (2007) Molecular insights into nitrogenase FeMoco insertion: The role of His 274 and His 451 of MoFe protein α subunit. J. Inorg. Biochem. 101, 1630-1641.
64. Corbett, M. C., Hu, Y., Fay, A. W., Tsuruta, H., Ribbe, M. W., Hodgson, K. O., and Hedman, B. (2007) Conformational differences between Azotobacter vinelandii nitrogenase MoFe proteins as studied by small angle X-ray scattering. Biochemistry 46, 8066-8074.
65. Lee, S. C., and Holm, R. H. (2004) The clusters of nitrogenase: Synthetic methodology in the construction of weak-field clusters. Chem. Rev. 104, 1135-1158.
66. Ribbe, M. W., Hu, Y., Guo, M., Schmid, B., and Burgess, B. K. (2002) The FeMoco-deficient MoFe protein produced by a nifH- deletion strain of Azotobacter vinelandii shows unusual P-cluster features. J. Biol. Chem. 277, 23469-23476.
67. Corbett, M. C., Hu, Y., Naderi, F., Ribbe, M. W., Hedman, B., and Hodgson, K. O. (2004) Comparison of iron-molybdenum cofactor deficient nitrogenase MoFe proteins by X-ray absorption spectroscopy: Implications for P-cluster biosynthesis. J. Biol. Chem. 279, 28276-28282.
68. Broach, R. B., Rupnik, K., Hu, Y., Fay, A. W., Cotton, M., Ribbe, M. W., and Hales, B. J. (2006) VTVH-MCD spectroscopic study of the metal clusters in the ΔnifB and ΔnifH MoFe proteins of nitrogenase from Azotobacter vinelandii. Biochemistry 45, 15039-15048.
69. Tal, S., Chun, T. W., Gavini, N., and Burgess, B. K. (1991) The ΔnifB (or ΔnifE) FeMo cofactor-deficient MoFe protein is different from the ΔnifH protein. J. Biol. Chem. 266, 10654-10657.
70. Hu, Y., Corbett, M. C., Fay, A. W., Webber, J. A., Hedman, B., Hodgson, K. O., and Ribbe, M. W. (2005) Nitrogenase reactivity with P-cluster variants. Proc. Natl. Acad. Sci. U.S.A. 102, 13825-13830.
71. Hu, Y., Fay, A. W., Dos Santos, P. C., Naderi, F., and Ribbe, M. W. (2004) Characterization of Azotobacter vinelandii nifZ-deletion strains: Indication of stepwise MoFe protein assembly. J. Biol. Chem. 279, 54963-54971.
72. Hu, Y., Fay, A. W., Lee, C. C., and Ribbe, M. W. (2007) P-Cluster maturation on nitrogenase MoFe protein. Proc. Natl. Acad. Sci. U.S.A. 104, 10424-10429.