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Annual Review of Microbiology

Volume 62, 2008

Biosynthesis of the Iron-Molybdenum Cofactor of Nitrogenase

Abstract

The iron-molybdenum cofactor (FeMo-co), located at the active site of the molybdenum nitrogenase, is one of the most complex metal cofactors known to date. During the past several years, an intensive effort has been made to purify the proteins involved in FeMo-co synthesis and incorporation into nitrogenase. This effort is starting to provide insights into the structures of the FeMo-co biosynthetic intermediates and into the biochemical details of FeMo-co synthesis.

Keyword(s): FeMo-co, iron-sulfur, MoFe protein, nif, NifDK, nitrogen fixation
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2008-10-13
2024-04-16
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Literature Cited

  1. Agar JN, Yuvaniyama P, Jack RF, Cash VL, Smith AD et al.1.  2000. Modular organization and identification of a mononuclear iron-binding site within the NifU protein. J. Biol. Inorg. Chem. 5:167–77 [Google Scholar]
  2. Allen RM, Chatterjee R, Ludden PW, Shah VK. 2.  1995. Incorporation of iron and sulfur from NifB cofactor into the iron-molybdenum cofactor of dinitrogenase. J. Biol. Chem. 270:26890–96 [Google Scholar]
  3. Allen RM, Roll JT, Rangaraj P, Shah VK, Roberts GP, Ludden PW. 3.  1999. Incorporation of molybdenum into the iron-molybdenum cofactor of nitrogenase. J. Biol. Chem. 274:15869–74 [Google Scholar]
  4. Arnold W, Rump A, Klipp W, Priefer UB, Pühler A. 4.  1988. Nucleotide sequence of a 24,206-base-pair DNA fragment carrying the entire nitrogen fixation gene cluster of Klebsiella pneumoniae. J. Mol. Biol. 203:715–38 [Google Scholar]
  5. Barney BM, Igarashi RY, Dos Santos PC, Dean DR, Seefeldt LC. 5.  2004. Substrate interaction at an iron-sulfur face of the FeMo-cofactor during nitrogenase catalysis. J. Biol. Chem. 279:53621–24 [Google Scholar]
  6. Barney BM, Yang TC, Igarashi RY, Dos Santos PC, Laryukhin M et al.6.  2005. Intermediates trapped during nitrogenase reduction of N triple bond N, CH3-N NH, and H2N-NH2. J. Am. Chem. Soc. 127:14960–61 [Google Scholar]
  7. Bishop PE, Joerger RD. 7.  1990. Genetics and molecular biology of alternative nitrogen fixation systems. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41:109–25 [Google Scholar]
  8. Brigle KE, Weiss MC, Newton WE, Dean DR. 8.  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. 169:1547–53 [Google Scholar]
  9. Broach RB, Rupnik K, Hu Y, Fay AW, Cotton M et al.9.  2006. Variable-temperature, variable-field magnetic circular dichroism spectroscopic study of the metal clusters in the ΔnifB and ΔnifH MoFe proteins of nitrogenase from Azotobacter vinelandii. Biochemistry 45:15039–48 [Google Scholar]
  10. Bulen WA, LeComte JR. 10.  1966. The nitrogenase system from Azotobacter: two enzyme requirements for N2 reduction, ATP dependent H2 evolution and ATP hydrolysis. Proc. Natl. Acad. Sci. USA 56:979–86 [Google Scholar]
  11. Chan MK, Kim J, Rees DC. 11.  1993. The nitrogenase FeMo-cofactor and P-cluster pair: 2.2 A resolution structures. Science 260:792–94 [Google Scholar]
  12. Chen JS, Toth J, Kasap M. 12.  2001. Nitrogen-fixation genes and nitrogenase activity in Clostridium acetobutylicum and Clostridium beijerinckii. J. Ind. Microbiol. Biotechnol. 27:281–86 [Google Scholar]
  13. Corbett MC, Hu Y, Fay AW, Ribbe MW, Hedman B, Hodgson KO. 13.  2006. Structural insights into a protein-bound iron-molybdenum cofactor precursor. Proc. Natl. Acad. Sci. USA 103:1238–43 [Google Scholar]
  14. Curatti L, Brown CS, Ludden PW, Rubio LM. 14.  2005. Genes required for rapid expression of nitrogenase activity in Azotobacter vinelandii. Proc. Natl. Acad. Sci. USA 102:6291–96 [Google Scholar]
  15. Curatti L, Hernandez JA, Igarashi RY, Soboh B, Zhao D, Rubio LM. 15.  2007. In vitro synthesis of the iron-molybdenum cofactor of nitrogenase from iron, sulfur, molybdenum and homocitrate using purified proteins. Proc. Natl. Acad. Sci. USA 104:17626–31 [Google Scholar]
  16. Curatti L, Ludden PW, Rubio LM. 16.  2006. NifB-dependent in vitro synthesis of the iron-molybdenum cofactor of nitrogenase. Proc. Natl. Acad. Sci. USA 103:5297–301 [Google Scholar]
  17. Dos Santos PC, Dean DR, Hu Y, Ribbe MW. 17.  2004. Formation and insertion of the nitrogenase iron-molybdenum cofactor. Chem. Rev. 104:1159–74 [Google Scholar]
  18. Dos Santos PC, Johnson DC, Ragle BE, Unciuleac MC, Dean DR. 18.  2007. Controlled expression of nif and isc iron-sulfur protein maturation components reveals target specificity and limited functional replacement between the two systems. J. Bacteriol. 189:2854–62 [Google Scholar]
  19. Dos Santos PC, Smith AD, Frazzon J, Cash VL, Johnson MK, Dean DR. 19.  2004. Iron-sulfur cluster assembly: NifU-directed activation of the nitrogenase Fe protein. J. Biol. Chem. 279:19705–11 [Google Scholar]
  20. Dyer DH, Rubio LM, Thoden JB, Holden HM, Ludden PW, Rayment I. 20.  2003. The three-dimensional structure of the core domain of NafY from Azotobacter vinelandii determined at 1.8-A resolution. J. Biol. Chem. 278:32150–56 [Google Scholar]
  21. Einsle O, Tezcan FA, Andrade SL, Schmid B, Yoshida M et al.21.  2002. Nitrogenase MoFe-protein at 1.16 A resolution: a central ligand in the FeMo-cofactor. Science 297:1696–700 [Google Scholar]
  22. Fenske D, Gnida M, Schneider K, Meyer-Klaucke W, Schemberg J et al.22.  2005. A new type of metalloprotein: The Mo storage protein from Azotobacter vinelandii contains a polynuclear molybdenum-oxide cluster. ChemBioChem 6:405–13 [Google Scholar]
  23. Fu W, Jack RF, Morgan TV, Dean DR, Johnson MK. 23.  1994. nifU gene product from Azotobacter vinelandii is a homodimer that contains two identical [2Fe-2S] clusters. Biochemistry 33:13455–63 [Google Scholar]
  24. Gavini N, Burgess BK. 24.  1992. FeMo cofactor synthesis by a nifH mutant with altered Mg⋅ ATP reactivity. J. Biol. Chem. 267:21179–86 [Google Scholar]
  25. George SJ, Igarashi RY, Piamonteze C, Soboh B, Cramer SP, Rubio LM. 25.  2007. Identification of a Mo-Fe-S cluster on NifEN by Mo K-edge extended X-ray absorption fine structure. J. Am. Chem. Soc. 129:3060–61 [Google Scholar]
  26. George SJ, Igarashi RY, Xiao Y, Hernandez JA, Demuez M et al.26.  2008. EXAFS and NRVS reveal that NifB-co, a FeMo-co precursor, comprises a 6 Fe core with an interstitial light atom. J. Am. Chem Soc. In press [Google Scholar]
  27. Georgiadis MM, Komiya H, Chakrabarti P, Woo D, Kornuc JJ, Rees DC. 27.  1992. Crystallographic structure of the nitrogenase iron protein from Azotobacter vinelandii. Science 257:1653–59 [Google Scholar]
  28. Goodwin PJ. 28.  1999. Biosynthesis of the nitrogenase FeMo-cofactor from Azotobacter vinelandii: involvement of the NifNE complex, NifX and the Fe protein PhD thesis Virginia Tech.210pp. [Google Scholar]
  29. Goodwin PJ, Agar JN, Roll JT, Roberts GP, Johnson MK, Dean DR. 29.  1998. The Azotobacter vinelandii NifEN complex contains two identical [4Fe-4S] clusters. Biochemistry 37:10420–28 [Google Scholar]
  30. Grunden AM, Shanmugam KT. 30.  1997. Molybdate transport and regulation in bacteria. Arch. Microbiol. 168:345–54 [Google Scholar]
  31. Hageman RV, Burris RH. 31.  1978. Nitrogenase and nitrogenase reductase associate and dissociate with each catalytic cycle. Proc. Natl. Acad. Sci. USA 75:2699–702 [Google Scholar]
  32. Hernandez JA, Igarashi RY, Soboh B, Curatti L, Dean DR et al.32.  2007. NifX and NifEN exchange NifB cofactor and the VK-cluster, a newly isolated intermediate of the iron-molybdenum cofactor biosynthetic pathway. Mol. Microbiol. 63:177–92 [Google Scholar]
  33. Homer MJ, Dean DR, Roberts GP. 33.  1995. Characterization of the γ protein and its involvement in the metallocluster assembly and maturation of dinitrogenase from Azotobacter vinelandii. J. Biol. Chem. 270:24745–52 [Google Scholar]
  34. Hoover TR, Imperial J, Ludden PW, Shah VK. 34.  1988. Homocitrate cures the NifV-phenotype in Klebsiella pneumoniae. J. Bacteriol. 170:1978–79 [Google Scholar]
  35. Hoover TR, Robertson AD, Cerny RL, Hayes RN, Imperial J et al.35.  1987. Identification of the V factor needed for synthesis of the iron-molybdenum cofactor of nitrogenase as homocitrate. Nature 329:855–57 [Google Scholar]
  36. Hu Y, Corbett MC, Fay AW, Webber JA, Hodgson KO et al.36.  2006. FeMo cofactor maturation on NifEN. Proc. Natl. Acad. Sci. USA 103:17119–24 [Google Scholar]
  37. Hu Y, Fay AW, Ribbe MW. 37.  2005. Identification of a nitrogenase FeMo cofactor precursor on NifEN complex. Proc. Natl. Acad. Sci. USA 102:3236–41 [Google Scholar]
  38. Hu YL, Corbettt MC, Fay AW, Webber JA, Hodgson KO et al.38.  2006. Nitrogenase Fe protein: a molybdate/homocitrate insertase. Proc. Natl. Acad. Sci. USA 103:17125–30 [Google Scholar]
  39. Igarashi RY, Seefeldt LC. 39.  2003. Nitrogen fixation: the mechanism of the Mo-dependent nitrogenase. Crit. Rev. Biochem. Mol. Biol. 38:351–84 [Google Scholar]
  40. Imperial J, Hoover TR, Madden MS, Ludden PW, Shah VK. 40.  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 28:7796–99 [Google Scholar]
  41. Imperial J, Ugalde RA, Shah VK, Brill WJ. 41.  1984. Role of the nifQ gene product in the incorporation of molybdenum into nitrogenase in Klebsiella pneumoniae. J. Bacteriol. 158:187–94 [Google Scholar]
  42. Jacobson MR, Brigle KE, Bennett LT, Setterquist RA, Wilson MS et al.42.  1989. Physical and genetic map of the major nif gene cluster from Azotobacter vinelandii. J. Bacteriol. 171:1017–27 [Google Scholar]
  43. Jacobson MR, Cash VL, Weiss MC, Laird NF, Newton WE, Dean DR. 43.  1989. Biochemical and genetic analysis of the nifUSVWZM cluster from Azotobacter vinelandii. Mol. Gen. Genet. 219:49–57 [Google Scholar]
  44. Joerger RD, Bishop PE. 44.  1988. Nucleotide sequence and genetic analysis of the nifB-nifQ region from Azotobacter vinelandii. J. Bacteriol. 170:1475–87 [Google Scholar]
  45. Johnson DC, Dean DR, Smith AD, Johnson MK. 45.  2005. Structure, function, and formation of biological iron-sulfur clusters. Annu. Rev. Biochem. 74:247–81 [Google Scholar]
  46. Johnson DC, Dos Santos PC, Dean DR. 46.  2005. NifU and NifS are required for the maturation of nitrogenase and cannot replace the function of isc-gene products in Azotobacter vinelandii. Biochem. Soc. Trans. 33:90–93 [Google Scholar]
  47. Kim J, Rees DC. 47.  1992. Crystallographic structure and functional implications of the nitrogenase molybdenum-iron protein from Azotobacter vinelandii. Nature 360:553–60 [Google Scholar]
  48. Lanzilotta WN, Fisher K, Seefeldt LC. 48.  1996. Evidence for electron transfer from the nitrogenase iron protein to the molybdenum-iron protein without Mg⋅ ATP hydrolysis: characterization of a tight protein-protein complex. Biochemistry 35:7188–96 [Google Scholar]
  49. Lanzilotta WN, Parker VD, Seefeldt LC. 49.  1998. Electron transfer in nitrogenase analyzed by Marcus theory: evidence for gating by Mg⋅ ATP. Biochemistry 37:399–407 [Google Scholar]
  50. Ludden PW, Rangaraj P, Rubio LM. 50.  2004. Biosynthesis of the iron-molybdenum and iron-vanadium cofactors of the nif- and vnf-encoded nitrogenases. Catalysts for Nitrogen Fixation: Nitrogenases, Relevant Chemical Models, and Commercial Processes BE Smith, RL Richards, WE Newton 219–53 Dordretch, The Neth.: Kluwer [Google Scholar]
  51. MacNeil T, MacNeil D, Roberts GP, Supiano MA, Brill WJ. 51.  1978. Fine-structure mapping and complementation analysis of nif (nitrogen fixation) genes in Klebsiella pneumoniae. J. Bacteriol. 136:253–66 [Google Scholar]
  52. Martinez-Argudo I, Little R, Shearer N, Johnson P, Dixon RA. 52.  2004. The NifL-NifA system: a multidomain transcriptional regulatory complex that integrates environmental signals. J. Bacteriol. 186:601–10 [Google Scholar]
  53. Masepohl B, Schneider K, Drepper T, Muller A, Klipp W. 53.  2002. Alternative nitrogenases. Nitrogen Fixation at the Millenium GJ Leigh 191–222 Amsterdam: Elsevier [Google Scholar]
  54. Mayer SM, Gormal CA, Smith BE, Lawson DM. 54.  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. 277:35263–66 [Google Scholar]
  55. McLean PA, Smith BE, Dixon RA. 55.  1983. Nitrogenase of Klebsiella pneumoniae nifV mutants.. Biochem. J 211:589–97 [Google Scholar]
  56. Paustian TD, Shah VK, Roberts GP. 56.  1989. Purification and characterization of the nifN and nifE gene products from Azotobacter vinelandii mutant UW45. Proc. Natl. Acad. Sci. USA 86:6082–86 [Google Scholar]
  57. Rangaraj P, Ludden PW. 57.  2002. Accumulation of 99Mo-containing iron-molybdenum cofactor precursors of nitrogenase on NifNE, NifH, and NifX of Azotobacter vinelandii. J. Biol. Chem. 277:40106–11 [Google Scholar]
  58. Rangaraj P, Ruttimann-Johnson C, Shah VK, Ludden PW. 58.  2001. Accumulation of 55Fe-labeled precursors of the iron-molybdenum cofactor of nitrogenase on NifH and NifX of Azotobacter vinelandii. J. Biol. Chem. 276:15968–74 [Google Scholar]
  59. Rangaraj P, Ryle MJ, Lanzilotta WN, Goodwin PJ, Dean DR et al.59.  1999. Inhibition of iron-molybdenum cofactor biosynthesis by L127Δ NifH and evidence for a complex formation between L127Δ NifH and NifNE. J. Biol. Chem. 274:29413–19 [Google Scholar]
  60. Rangaraj P, Ryle MJ, Lanzilotta WN, Ludden PW, Shah VK. 60.  1999. In vitro biosynthesis of iron-molybdenum cofactor and maturation of the nif-encoded apodinitrogenase. Effect of substitution for NifH with site-specifically altered forms of NifH. J. Biol. Chem. 274:19778–84 [Google Scholar]
  61. Rangaraj P, Shah VK, Ludden PW. 61.  1997. ApoNifH functions in iron-molybdenum cofactor synthesis and apodinitrogenase maturation. Proc. Natl. Acad. Sci. USA 94:11250–55 [Google Scholar]
  62. Raymond J, Siefert JL, Staples CR, Blankenship RE. 62.  2004. The natural history of nitrogen fixation. Mol. Biol. Evol. 21:541–54 [Google Scholar]
  63. Ribbe MW, Hu Y, Guo M, Schmid B, Burgess BK. 63.  2002. The FeMoco-deficient MoFe protein produced by a nifH deletion strain of Azotobacter vinelandii shows unusual P-cluster features.. J. Biol. Chem. 277:23469–76 [Google Scholar]
  64. Roberts GP, MacNeil T, MacNeil D, Brill WJ. 64.  1978. Regulation and characterization of protein products coded by the nif (nitrogen fixation) genes of Klebsiella pneumoniae. J. Bacteriol. 136:267–79 [Google Scholar]
  65. Rodríguez-Quiñones F, Bosch R, Imperial J. 65.  1993. Expression of the nifBfdxNnifOQ region of Azotobacter vinelandii and its role in nitrogenase activity.. J. Bacteriol. 175:2926–35 [Google Scholar]
  66. Roll JT, Shah VK, Dean DR, Roberts GP. 66.  1995. Characteristics of NIFNE in Azotobacter vinelandii strains. Implications for the synthesis of the iron-molybdenum cofactor of dinitrogenase. J. Biol. Chem. 270:4432–37 [Google Scholar]
  67. Rubio LM, Ludden PW. 67.  2002. The gene products of the nif regulon.. Nitrogen Fixation at the Millenium GJ Leigh 101–36 Amsterdam: Elsevier [Google Scholar]
  68. Rubio LM, Ludden PW. 68.  2005. Maturation of nitrogenase: a biochemical puzzle. J. Bacteriol. 187:405–14 [Google Scholar]
  69. Rubio LM, Rangaraj P, Homer MJ, Roberts GP, Ludden PW. 69.  2002. Cloning and mutational analysis of the γ gene from Azotobacter vinelandii defines a new family of proteins capable of metallocluster-binding and protein stabilization. J. Biol. Chem. 277:14299–305 [Google Scholar]
  70. Rubio LM, Singer SW, Ludden PW. 70.  2004. Purification and characterization of NafY (apodinitrogenase γ subunit) from Azotobacter vinelandii. J. Biol. Chem. 279:19739–46 [Google Scholar]
  71. Ruttimann-Johnson C, Rubio LM, Dean DR, Ludden PW. 71.  2003. VnfY is required for full activity of the vanadium-containing dinitrogenase in Azotobacter vinelandii. J. Bacteriol. 185:2383–86 [Google Scholar]
  72. Shah VK, Allen JR, Spangler NJ, Ludden PW. 72.  1994. In vitro synthesis of the iron-molybdenum cofactor of nitrogenase. Purification and characterization of NifB cofactor, the product of NIFB protein. J. Biol. Chem. 269:1154–58 [Google Scholar]
  73. Shah VK, Brill WJ. 73.  1977. Isolation of an iron-molybdenum cofactor from nitrogenase. Proc. Natl. Acad. Sci. USA 74:3249–53 [Google Scholar]
  74. Shah VK, Imperial J, Ugalde RA, Ludden PW, Brill WJ. 74.  1986. In vitro synthesis of the iron-molybdenum cofactor of nitrogenase. Proc. Natl. Acad. Sci. USA 83:1636–40 [Google Scholar]
  75. Shah VK, Stacey G, Brill WJ. 75.  1983. Electron transport to nitrogenase. Purification and characterization of pyruvate:flavodoxin oxidoreductase. The nifJ gene product. J. Biol. Chem. 258:12064–68 [Google Scholar]
  76. Simpson FB, Burris RH. 76.  1984. A nitrogen pressure of 50 atmospheres does not prevent evolution of hydrogen by nitrogenase. Science 224:1095–97 [Google Scholar]
  77. Smith AD, Jameson GN, Dos Santos PC, Agar JN, Naik S et al.77.  2005. NifS-mediated assembly of [4Fe-4S] clusters in the N- and C-terminal domains of the NifU scaffold protein. Biochemistry 44:12955–69 [Google Scholar]
  78. Soboh B, Igarashi RY, Hernandez JA, Rubio LM. 78.  2006. Purification of a NifEN protein complex that contains bound Mo and a FeMo-co precursor from an Azotobacter vinelandii ΔnifHDK strain. J. Biol. Chem. 281:36701–9 [Google Scholar]
  79. Sofia HJ, Chen G, Hetzler BG, Reyes-Spindola JF, Miller NE. 79.  2001. Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods. Nucleic Acids Res. 29:1097–106 [Google Scholar]
  80. Ugalde RA, Imperial J, Shah VK, Brill WJ. 80.  1984. Biosynthesis of iron-molybdenum cofactor in the absence of nitrogenase. J. Bacteriol. 159:888–93 [Google Scholar]
  81. Ugalde RA, Imperial J, Shah VK, Brill WJ. 81.  1985. Biosynthesis of the iron-molybdenum cofactor and the molybdenum cofactor in Klebsiella pneumoniae: effect of sulfur source. J. Bacteriol. 164:1081–87 [Google Scholar]
  82. Wang SC, Frey PA. 82.  2007. S-adenosylmethionine as an oxidant: the radical SAM superfamily. Trends Biochem. Sci. 32:101–10 [Google Scholar]
  83. Yuvaniyama P, Agar JN, Cash VL, Johnson MK, Dean DR. 83.  2000. NifS-directed assembly of a transient [2Fe-2S] cluster within the NifU protein. Proc. Natl. Acad. Sci. USA 97:599–604 [Google Scholar]
  84. Zhao D, Curatti L, Rubio LM. 84.  2007. Evidence for nifU and nifS participation in the biosynthesis of the iron-molybdenum cofactor of nitrogenase. J. Biol. Chem. 282:37016–25 [Google Scholar]
  85. Zheng L, Cash VL, Flint DH, Dean DR. 85.  1998. Assembly of iron-sulfur clusters. Identification of an iscSUA-hscBA-fdx gene cluster from Azotobacter vinelandii. J. Biol. Chem. 273:13264–72 [Google Scholar]
  86. Zheng L, White RH, Cash VL, Dean DR. 86.  1994. Mechanism for the desulfurization of l-cysteine catalyzed by the nifS gene product. Biochemistry 33:4714–20 [Google Scholar]
  87. Zheng L, White RH, Cash VL, Jack RF, Dean DR. 87.  1993. Cysteine desulfurase activity indicates a role for NIFS in metallocluster biosynthesis. Proc. Natl. Acad. Sci. USA 90:2754–58 [Google Scholar]
  88. Zheng L, White RH, Dean DR. 88.  1997. Purification of the Azotobacter vinelandii nifV-encoded homocitrate synthase. J. Bacteriol. 179:5963–66 [Google Scholar]
/content/journals/10.1146/annurev.micro.62.081307.162737
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Biosynthesis of the Iron-Molybdenum Cofactor of Nitrogenase
Annual Review of Microbiology 62, 93 (2008); https://doi.org/10.1146/annurev.micro.62.081307.162737
/content/journals/10.1146/annurev.micro.62.081307.162737
/content/journals/10.1146/annurev.micro.62.081307.162737
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