Assembly of nitrogenase MoFe protein.

Assembly of nitrogenase MoFe protein is arguably one of the most complex processes in the field of bioinorganic chemistry, requiring, at least, the participation of nifS, nifU, nifB, nifE, nifN, nifV, nifQ, nifZ, nifH, nifD, and nifK gene products. Previous genetic studies have identified factors involved in MoFe protein assembly; however, the exact functions of these factors and the precise sequence of events during the process have remained unclear until the recent characterization of a number of assembly-related intermediates that provided significant insights into this biosynthetic "black box". This review summarizes the recent advances in elucidation of the mechanism of FeMoco biosynthesis in four aspects: (1) the ex situ assembly of FeMoco on NifEN, (2) the incorporation of FeMoco into MoFe protein, (3) the in situ assembly of P-cluster on MoFe protein, and (4) the stepwise assembly of MoFe protein.

[1]  K. Hodgson,et al.  Stepwise formation of P-cluster in nitrogenase MoFe protein , 2009, Proceedings of the National Academy of Sciences.

[2]  R. Mendel,et al.  Molybdenum cofactors, enzymes and pathways , 2009, Nature.

[3]  K. Hodgson,et al.  Optimization of FeMoco maturation on NifEN. , 2009, Journal of the American Chemical Society.

[4]  K. Rupnik,et al.  VTVH-MCD study of the Delta nifB Delta nifZ MoFe protein from Azotobacter vinelandii. , 2009, Journal of the American Chemical Society.

[5]  D. Case,et al.  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. , 2007, Inorganic chemistry.

[6]  L. Curatti,et al.  In vitro synthesis of the iron–molybdenum cofactor of nitrogenase from iron, sulfur, molybdenum, and homocitrate using purified proteins , 2007, Proceedings of the National Academy of Sciences.

[7]  Yilin Hu,et al.  MOLECULAR INSIGHTS INTO NITROGENASE FeMoco INSERTION – THE ROLE OF His 274 and His 451 OF MoFe PROTEIN α SUBUNIT , 2007 .

[8]  R. Staples,et al.  Hydroxide-promoted core conversions of molybdenum-iron-sulfur edge-bridged double cubanes: oxygen-ligated topological PN clusters. , 2007, Inorganic chemistry.

[9]  Y. Ohki,et al.  Synthesis of new [8Fe-7S] clusters: a topological link between the core structures of P-cluster, FeMo-co, and FeFe-co of nitrogenases. , 2007, Journal of the American Chemical Society.

[10]  Yilin Hu,et al.  P-cluster maturation on nitrogenase MoFe protein , 2007, Proceedings of the National Academy of Sciences.

[11]  K. Hodgson,et al.  Conformational differences between Azotobacter vinelandii nitrogenase MoFe proteins as studied by small-angle X-ray scattering. , 2007, Biochemistry.

[12]  S. George,et al.  Identification of a Mo-Fe-S cluster on NifEN by Mo K-edge extended X-ray absorption fine structure. , 2007, Journal of the American Chemical Society.

[13]  L. Curatti,et al.  NifX and NifEN exchange NifB cofactor and the VK‐cluster, a newly isolated intermediate of the iron‐molybdenum cofactor biosynthetic pathway , 2007, Molecular microbiology.

[14]  Yilin Hu,et al.  Molecular insights into nitrogenase FeMo cofactor insertion: the role of His 362 of the MoFe protein α subunit in FeMo cofactor incorporation , 2007, JBIC Journal of Biological Inorganic Chemistry.

[15]  L. M. Rubio,et al.  Purification of a NifEN Protein Complex That Contains Bound Molybdenum and a FeMo-Co Precursor from an Azotobacter vinelandii ΔnifHDK Strain* , 2006, Journal of Biological Chemistry.

[16]  K. Rupnik,et al.  Variable-temperature, variable-field magnetic circular dichroism spectroscopic study of the metal clusters in the DeltanifB and DeltanifH mofe proteins of nitrogenase from Azotobacter vinelandii. , 2006, Biochemistry.

[17]  Mary C. Corbett,et al.  FeMo cofactor maturation on NifEN , 2006, Proceedings of the National Academy of Sciences.

[18]  Mary C. Corbett,et al.  Nitrogenase Fe protein: A molybdate/homocitrate insertase , 2006, Proceedings of the National Academy of Sciences.

[19]  D. Rees,et al.  How many metals does it take to fix N2? A mechanistic overview of biological nitrogen fixation , 2006, Proceedings of the National Academy of Sciences.

[20]  Molecular Insights into Nitrogenase FeMoco Insertion , 2006, Journal of Biological Chemistry.

[21]  NifB-dependent in vitro synthesis of the iron-molybdenum cofactor of nitrogenase. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[22]  J. W. Peters,et al.  Exploring new frontiers of nitrogenase structure and mechanism. , 2006, Current opinion in chemical biology.

[23]  C. Berlinguette,et al.  Precursors to clusters with the topology of the P(N) cluster of nitrogenase: edge-bridged double cubane clusters [(Tp)2Mo2Fe6S8L4]z: synthesis, structures, and electron transfer series. , 2006, Inorganic chemistry.

[24]  Mary C. Corbett,et al.  Structural insights into a protein-bound iron-molybdenum cofactor precursor , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[25]  C. Krebs,et al.  NifS-mediated assembly of [4Fe-4S] clusters in the N- and C-terminal domains of the NifU scaffold protein. , 2005, Biochemistry.

[26]  Mary C. Corbett,et al.  Nitrogenase reactivity with P-cluster variants. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[27]  L. Seefeldt,et al.  The interstitial atom of the nitrogenase FeMo-cofactor: ENDOR and ESEEM evidence that it is not a nitrogen. , 2005, Journal of the American Chemical Society.

[28]  Yilin Hu,et al.  Identification of a nitrogenase FeMo cofactor precursor on NifEN complex. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[29]  D. Rees,et al.  Structural Basis of Biological Nitrogen Fixation. , 1996, Chemical reviews.

[30]  Yilin Hu,et al.  Characterization of Azotobacter vinelandii nifZ Deletion Strains , 2004, Journal of Biological Chemistry.

[31]  Mary C. Corbett,et al.  Comparison of Iron-Molybdenum Cofactor-deficient Nitrogenase MoFe Proteins by X-ray Absorption Spectroscopy , 2004, Journal of Biological Chemistry.

[32]  J. Frazzon,et al.  Iron-Sulfur Cluster Assembly , 2004, Journal of Biological Chemistry.

[33]  R. H. Holm,et al.  The clusters of nitrogenase: synthetic methodology in the construction of weak-field clusters. , 2004, Chemical reviews.

[34]  Yilin Hu,et al.  Formation and insertion of the nitrogenase iron-molybdenum cofactor. , 2004, Chemical reviews.

[35]  Yugen Zhang,et al.  Structural conversions of molybdenum-iron-sulfur edge-bridged double cubanes and P(n)-type clusters topologically related to the nitrogenase P-cluster. , 2004, Inorganic chemistry.

[36]  J. Zuo,et al.  Vanadium-iron-sulfur clusters containing the cubane-type [VFe3S4] core unit: synthesis of a cluster with the topology of the PN cluster of nitrogenase. , 2003, Inorganic chemistry.

[37]  D. Case,et al.  Structural, spectroscopic, and redox consequences of a central ligand in the FeMoco of nitrogenase: a density functional theoretical study. , 2003, Journal of the American Chemical Society.

[38]  Y. Ohki,et al.  Synthesis of the P-cluster inorganic core of nitrogenases. , 2003, Journal of the American Chemical Society.

[39]  Yugen Zhang,et al.  Synthesis of a molecular Mo2Fe6S9 cluster with the topology of the PN cluster of nitrogenase by rearrangement of an edge-bridged Mo2Fe6S8 double cubane. , 2003, Journal of the American Chemical Society.

[40]  I. Dance.  The consequences of an interstitial N atom in the FeMo cofactor of nitrogenase. , 2003, Chemical communications.

[41]  J. Nørskov,et al.  Modeling a central ligand in the nitrogenase FeMo cofactor. , 2003, Journal of the American Chemical Society.

[42]  D. Rees,et al.  Nitrogenase MoFe-Protein at 1.16 Å Resolution: A Central Ligand in the FeMo-Cofactor , 2002, Science.

[43]  M. Guo,et al.  The FeMoco-deficient MoFe Protein Produced by a nifHDeletion Strain of Azotobacter vinelandii Shows Unusual P-cluster Features* , 2002, The Journal of Biological Chemistry.

[44]  D. Rees,et al.  Structure of a Cofactor-Deficient Nitrogenase MoFe Protein , 2002, Science.

[45]  J. Frazzon,et al.  Biosynthesis of the nitrogenase iron-molybdenum-cofactor from Azotobacter vinelandii. , 2002, Metal ions in biological systems.

[46]  B. Burgess,et al.  The chaperone GroEL is required for the final assembly of the molybdenum-iron protein of nitrogenase , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[47]  B. Burgess,et al.  Mössbauer Study of the MoFe Protein of Nitrogenase from Azotobacter vinelandii Using Selective 57Fe Enrichment of the M-Centers , 2000 .

[48]  J. Agar,et al.  Modular organization and identification of a mononuclear iron-binding site within the NifU protein , 2000, JBIC Journal of Biological Inorganic Chemistry.

[49]  J. Agar,et al.  NifS-directed assembly of a transient [2Fe-2S] cluster within the NifU protein. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[50]  Barry E. Smith.  Structure, Function, and Biosynthesis of the Metallosulfur Clusters in Nitrogenases , 1999 .

[51]  J. Agar,et al.  The Azotobacter vinelandii NifEN complex contains two identical [4Fe-4S] clusters. , 1998, Biochemistry.

[52]  B. Hoffman,et al.  Metal-Ion Valencies of the FeMo Cofactor in CO-Inhibited and Resting State Nitrogenase by 57Fe Q-Band ENDOR , 1997 .

[53]  R. White,et al.  Purification of the Azotobacter vinelandii nifV-encoded homocitrate synthase , 1997, Journal of bacteriology.

[54]  D. Rees,et al.  Structure of ADP·AIF4 –-stabilized nitrogenase complex and its implications for signal transduction , 1997, Nature.

[55]  J. W. Peters,et al.  Redox-dependent structural changes in the nitrogenase P-cluster. , 1997, Biochemistry.

[56]  B. Burgess,et al.  Mechanism of Molybdenum Nitrogenase. , 1996, Chemical reviews.

[57]  P. Ludden,et al.  Incorporation of Iron and Sulfur from NifB Cofactor into the Iron-Molybdenum Cofactor of Dinitrogenase (*) , 1995, The Journal of Biological Chemistry.

[58]  G. Roberts,et al.  Characterization of the γ Protein and Its Involvement in the Metallocluster Assembly and Maturation of Dinitrogenase from Azotobacter vinelandii(*) , 1995, The Journal of Biological Chemistry.

[59]  G. Roberts,et al.  Characteristics of NIFNE in Azotobacter vinelandii Strains , 1995, The Journal of Biological Chemistry.

[60]  G. Roberts,et al.  The nifY product of Klebsiella pneumoniae is associated with apodinitrogenase and dissociates upon activation with the iron-molybdenum cofactor , 1993, Journal of bacteriology.

[61]  D. Rees,et al.  The nitrogenase FeMo-cofactor and P-cluster pair: 2.2 A resolution structures. , 1993, Science.

[62]  W. Hagen,et al.  Redox properties and EPR spectroscopy of the P clusters of Azotobacter vinelandii MoFe protein. , 1993, European journal of biochemistry.

[63]  D. C. Rees,et al.  Crystallographic structure and functional implications of the nitrogenase molybdenum–iron protein from Azotobacter vinelandii , 1992, Nature.

[64]  T. White,et al.  Electrophoretic studies on the assembly of the nitrogenase molybdenum-iron protein from the Klebsiella pneumoniae nifD and nifK gene products. , 1992, The Journal of biological chemistry.

[65]  W. Orme-Johnson,et al.  Moessbauer and integer-spin EPR of the oxidized P-clusters of nitrogenase: POX is a non-Kramers system with a nearly degenerate ground doublet , 1992 .

[66]  M. Weiss,et al.  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 , 1987, Journal of bacteriology.

[67]  A. D. Robertson,et al.  Identification of the V factor needed for synthesis of the iron-molybdenum cofactor of nitrogenase as homocitrate , 1987, Nature.

[68]  R. Dixon,et al.  The Iron-Molybdenum Cofactor of Nitrogenase , 1985 .

[69]  D. Tennent,et al.  Redox and spectroscopic properties of oxidized MoFe protein from Azotobacter vinelandii. , 1980, Biochemistry.

[70]  W. Brill,et al.  Nitrogenase X: Mössbauer and EPR studies on reversibly oxidized MoFe protein from Azotobacter vinelandii OP. Nature of the iron centers. , 1978, Biochimica et biophysica acta.

[71]  W. Brill,et al.  Isolation of an iron-molybdenum cofactor from nitrogenase. , 1977, Proceedings of the National Academy of Sciences of the United States of America.