Molybdenum trafficking for nitrogen fixation.

The molybdenum nitrogenase is responsible for most biological nitrogen fixation, a prokaryotic metabolic process that determines the global biogeochemical cycles of nitrogen and carbon. Here we describe the trafficking of molybdenum for nitrogen fixation in the model diazotrophic bacterium Azotobacter vinelandii. The genes and proteins involved in molybdenum uptake, homeostasis, storage, regulation, and nitrogenase cofactor biosynthesis are reviewed. Molybdenum biochemistry in A. vinelandii reveals unexpected mechanisms and a new role for iron-sulfur clusters in the sequestration and delivery of molybdenum.

[1]  L. Seefeldt,et al.  Mechanism of Mo-dependent nitrogenase. , 2009, Annual review of biochemistry.

[2]  M. Romão Molybdenum and tungsten enzymes: a crystallographic and mechanistic overview. , 2009, Dalton transactions.

[3]  Jian Sun,et al.  Genome Sequence of Azotobacter vinelandii , an Obligate Aerobe Specialized To Support Diverse Anaerobic Metabolic Processes † , 2009 .

[4]  F. Morel,et al.  Multiple roles of siderophores in free-living nitrogen-fixing bacteria , 2009, BioMetals.

[5]  R. D. Britt,et al.  Metal trafficking for nitrogen fixation: NifQ donates molybdenum to NifEN/NifH for the biosynthesis of the nitrogenase FeMo-cofactor , 2008, Proceedings of the National Academy of Sciences.

[6]  D. Dean,et al.  A newly discovered role for iron-sulfur clusters , 2008, Proceedings of the National Academy of Sciences.

[7]  Yan Zhang,et al.  Molybdoproteomes and evolution of molybdenum utilization. , 2008, Journal of molecular biology.

[8]  Zhanglin Lin,et al.  Nitrogen fixation island and rhizosphere competence traits in the genome of root-associated Pseudomonas stutzeri A1501 , 2008, Proceedings of the National Academy of Sciences.

[9]  Yuming Xiao,et al.  Extended X-ray absorption fine structure and nuclear resonance vibrational spectroscopy reveal that NifB-co, a FeMo-co precursor, comprises a 6Fe core with an interstitial light atom. , 2008, Journal of the American Chemical Society.

[10]  E. Herrero,et al.  Chloroplast monothiol glutaredoxins as scaffold proteins for the assembly and delivery of [2Fe–2S] clusters , 2008, The EMBO journal.

[11]  Thomas Wichard,et al.  Uptake of molybdenum and vanadium by a nitrogen-fixing soil bacterium using siderophores , 2008 .

[12]  K. Schneider,et al.  Azotobacter vinelandii Metal Storage Protein: “Classical” Inorganic Chemistry Involved in Mo/W Uptake and Release Processes , 2008, Chembiochem : a European journal of chemical biology.

[13]  Thomas Wichard,et al.  Catechol siderophores control tungsten uptake and toxicity in the nitrogen-fixing bacterium Azotobacter vinelandii. , 2008, Environmental science & technology.

[14]  L. Curatti,et al.  Evidence for nifU and nifS Participation in the Biosynthesis of the Iron-Molybdenum Cofactor of Nitrogenase* , 2007, Journal of Biological Chemistry.

[15]  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.

[16]  E. Warkentin,et al.  Towards biological supramolecular chemistry: a variety of pocket-templated, individual metal oxide cluster nucleations in the cavity of a mo/w-storage protein. , 2007, Angewandte Chemie.

[17]  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.

[18]  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.

[19]  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.

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

[21]  F. Bittner,et al.  Cell biology of molybdenum. , 2006, Biochimica et biophysica acta.

[22]  L. Curatti,et al.  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.

[23]  K. Rajagopalan,et al.  High-resolution EXAFS of the active site of human sulfite oxidase: comparison with density functional theory and X-ray crystallographic results. , 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]  A. Anbar,et al.  Production of a molybdophore during metal-targeted dissolution of silicates by soil bacteria , 2005 .

[26]  D. Dean,et al.  Structure, function, and formation of biological iron-sulfur clusters. , 2005, Annual review of biochemistry.

[27]  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.

[28]  K. Schneider,et al.  A New Type of Metalloprotein: The Mo Storage Protein from Azotobacter vinelandii Contains a Polynuclear Molybdenum–Oxide Cluster , 2005, Chembiochem : a European journal of chemical biology.

[29]  Paul Dijkstra,et al.  CO2 Elicits Long-Term Decline in Nitrogen Fixation , 2004, Science.

[30]  S. Singer,et al.  Purification and Characterization of NafY (Apodinitrogenase γ Subunit) from Azotobacter vinelandii* , 2004, Journal of Biological Chemistry.

[31]  R. H. Holm,et al.  Synthetic analogues and reaction systems relevant to the molybdenum and tungsten oxotransferases. , 2004, Chemical reviews.

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

[33]  L. Seefeldt,et al.  Substrate interactions with nitrogenase: Fe versus Mo. , 2004, Biochemistry.

[34]  David J Studholme,et al.  A DNA element recognised by the molybdenum-responsive transcription factor ModE is conserved in Proteobacteria, green sulphur bacteria and Archaea , 2003, BMC Microbiology.

[35]  W. Page,et al.  The csbX gene of Azotobacter vinelandii encodes an MFS efflux pump required for catecholate siderophore export. , 2003, FEMS microbiology letters.

[36]  S. Andrews,et al.  Bacterial iron homeostasis. , 2003, FEMS microbiology reviews.

[37]  A. Müller,et al.  Characterization of a tungsten-substituted nitrogenase isolated from Rhodobacter capsulatus. , 2003, Biochemistry.

[38]  W. Hunter,et al.  Crystal structure of activated ModE reveals conformational changes involving both oxyanion and DNA-binding domains. , 2003, Journal of molecular biology.

[39]  P. Ludden,et al.  Accumulation of 99Mo-containing Iron-Molybdenum Cofactor Precursors of Nitrogenase on NifNE, NifH, and NifX ofAzotobacter vinelandii * , 2002, The Journal of Biological Chemistry.

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

[41]  R. Gunsalus,et al.  The Molybdate-Responsive Escherichia coli ModE Transcriptional Regulator Coordinates Periplasmic Nitrate Reductase (napFDAGHBC) Operon Expression with Nitrate and Molybdate Availability , 2002, Journal of bacteriology.

[42]  G. Roberts,et al.  Cloning and Mutational Analysis of the γ Gene fromAzotobacter vinelandii Defines a New Family of Proteins Capable of Metallocluster Binding and Protein Stabilization* , 2002, The Journal of Biological Chemistry.

[43]  H. Sigel,et al.  Molybdenum and tungsten : their roles in biological processes , 2002 .

[44]  N. C. Price,et al.  Oxyanion Binding Alters Conformation and Quaternary Structure of the C-terminal Domain of the Transcriptional Regulator ModE , 2001, The Journal of Biological Chemistry.

[45]  D. Lawson,et al.  Two crystal structures of the cytoplasmic molybdate-binding protein ModG suggest a novel cooperative binding mechanism and provide insights into ligand-binding specificity. , 2001, Journal of molecular biology.

[46]  W. Page,et al.  Dual regulation of catecholate siderophore biosynthesis in Azotobacter vinelandii by iron and oxidative stress. , 2000, Microbiology.

[47]  R. Pau,et al.  Extended X-ray absorption fine structure studies on periplasmic and intracellular molybdenum-binding proteins , 1999, JBIC Journal of Biological Inorganic Chemistry.

[48]  K. Shanmugam,et al.  An Analysis of the Binding of Repressor Protein ModE tomodABCD (Molybdate Transport) Operator/Promoter DNA ofEscherichia coli * , 1999, The Journal of Biological Chemistry.

[49]  G. Roberts,et al.  Incorporation of Molybdenum into the Iron-Molybdenum Cofactor of Nitrogenase* , 1999, The Journal of Biological Chemistry.

[50]  D. Hall,et al.  The high‐resolution crystal structure of the molybdate‐dependent transcriptional regulator (ModE) from Escherichia coli: a novel combination of domain folds , 1999, The EMBO journal.

[51]  K. Shanmugam,et al.  Molybdate-dependent transcription of hyc and nar operons of Escherichia coli requires MoeA protein and ModE-molybdate. , 1998, FEMS microbiology letters.

[52]  R. Gunsalus,et al.  Functional Dissection of the Molybdate-Responsive Transcription Regulator, ModE, from Escherichia coli , 1998, Journal of bacteriology.

[53]  E. Stiefel Transition metal sulfur chemistry and its relevance to molybdenum and tungsten enzymes , 1998 .

[54]  R. Gunsalus,et al.  Anaerobic regulation of the Escherichia coli dmsABC operon requires the molybdate‐responsive regulator ModE , 1998, Molecular microbiology.

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

[56]  O. Meyer,et al.  N2 Fixation by Streptomyces thermoautotrophicus Involves a Molybdenum-Dinitrogenase and a Manganese-Superoxide Oxidoreductase That Couple N2Reduction to the Oxidation of Superoxide Produced from O2by a Molybdenum-CO Dehydrogenase* , 1997, The Journal of Biological Chemistry.

[57]  K. Shanmugam,et al.  Molybdate transport and regulation in bacteria , 1997, Archives of Microbiology.

[58]  D. Rees,et al.  Crystal structure of the molybdate binding protein ModA , 1997, Nature Structural Biology.

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

[60]  Paul G. Falkowski,et al.  Evolution of the nitrogen cycle and its influence on the biological sequestration of CO2 in the ocean , 1997, Nature.

[61]  R. Hille The Mononuclear Molybdenum Enzymes. , 1997, Chemical reviews.

[62]  R. Gunsalus,et al.  Characterization of the ModE DNA‐binding sites in the control regions of modABCD and moaABCDE of Escherichia coli , 1997, Molecular microbiology.

[63]  C. Pickett The Chatt cycle and the mechanism of enzymic reduction of molecular nitrogen , 1996, JBIC Journal of Biological Inorganic Chemistry.

[64]  R. Eady Structure−Function Relationships of Alternative Nitrogenases , 1996 .

[65]  R. Hille Structure and function of mononuclear molybdenum enzymes , 1996, JBIC Journal of Biological Inorganic Chemistry.

[66]  M. E. Leonowicz,et al.  Synthesis, reactivity and redox properties of dinuclear molybdenum-sulfur complexes , 1996 .

[67]  B. Howes,et al.  Evidence favoring molybdenum-carbon bond formation in xanthine oxidase action: 17Q- and 13C-ENDOR and kinetic studies. , 1996, Biochemistry.

[68]  K. Shanmugam,et al.  Repression of the Escherichia coli modABCD (molybdate transport) operon by ModE , 1996, Journal of bacteriology.

[69]  Robert Huber,et al.  Crystal Structure of the Xanthine Oxidase-Related Aldehyde Oxido-Reductase from D. gigas , 1995, Science.

[70]  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.

[71]  S. Cramer,et al.  FE AND MO EXAFS OF AZOTOBACTER VINELANDII NITROGENASE IN PARTIALLY OXIDIZED AND SINGLY REDUCED FORMS , 1995 .

[72]  R. Pau,et al.  Mutational analysis of genes of the mod locus involved in molybdenum transport, homeostasis, and processing in Azotobacter vinelandii , 1995, Journal of bacteriology.

[73]  K. Shanmugam,et al.  Genetic analysis of the modABCD (molybdate transport) operon of Escherichia coli , 1995, Journal of bacteriology.

[74]  R. Gunsalus,et al.  Regulation of the molybdate transport operon, modABCD, of Escherichia coli in response to molybdate availability , 1995, Journal of bacteriology.

[75]  Jeffrey R. Allen,et al.  In vitro synthesis of the iron-molybdenum cofactor of nitrogenase. Purification and characterization of NifB cofactor, the product of NIFB protein. , 1994, The Journal of biological chemistry.

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

[77]  W. Klipp,et al.  Characterization of Rhodobacter capsulatus genes encoding a molybdenum transport system and putative molybdenum-pterin-binding proteins , 1993, Journal of bacteriology.

[78]  F. Rodríguez-Quiñones,et al.  Expression of the nifBfdxNnifOQ region of Azotobacter vinelandii and its role in nitrogenase activity , 1993, Journal of bacteriology.

[79]  F. Armstrong,et al.  Investigation of metal ion uptake reactivities of [3Fe-4S] clusters in proteins : voltammetry of co-adsorbed ferredoxin-aminocyclitol films at graphite electrodes and spectroscopic identification of transformed clusters , 1991 .

[80]  M. Weiss,et al.  Biochemical and genetic analysis of the nifUSVWZM cluster from Azotobacter vinelandii , 1989, Molecular and General Genetics MGG.

[81]  R. Prince,et al.  Structure of the active site of sulfite oxidase. X-ray absorption spectroscopy of the Mo(IV), Mo(V), and Mo(VI) oxidation states. , 1989, Biochemistry.

[82]  R. Setterquist,et al.  Physical and genetic map of the major nif gene cluster from Azotobacter vinelandii , 1989, Journal of bacteriology.

[83]  P. Bishop,et al.  Nucleotide sequence and genetic analysis of the nifB-nifQ region from Azotobacter vinelandii , 1988, Journal of bacteriology.

[84]  W. Page,et al.  Aminochelin, a Catecholamine Siderophore Produced by Azotobacter vinelandii , 1988 .

[85]  M. Eldridge,et al.  Nitrogenase of Klebsiella pneumoniae. Rhodanese-catalysed restoration of activity of the inactive 2Fe species of the Fe protein. , 1987, The Biochemical journal.

[86]  W. Brill,et al.  Biosynthesis of the Iron-Molybdenum Cofactor and the Molybdenum Cofactor in Klebsiella pneumoniae: Effect of Sulfur Source , 1986, Journal of bacteriology.

[87]  S. Pagani,et al.  Enzymic synthesis of the iron-sulfur cluster of spinach ferredoxin. , 1984, European journal of biochemistry.

[88]  W. Brill,et al.  Role of the nifQ gene product in the incorporation of molybdenum into nitrogenase in Klebsiella pneumoniae , 1984, Journal of bacteriology.

[89]  W. Brill,et al.  Molybdenum accumulation and storage in Klebsiella pneumoniae and Azotobacter vinelandii , 1981, Journal of bacteriology.

[90]  D. Lowe,et al.  Electron-paramagnetic-resonance studies on nitrogenase of Klebsiella pneumoniae. Evidence for acetylene- and ethylene-nitrogenase transient complexes. , 1978, The Biochemical journal.

[91]  K. Hodgson,et al.  The molybdenum site of nitrogenase. Preliminary structural evidence from x-ray absorption spectroscopy , 1978 .

[92]  W. Brill,et al.  Molybdenum cofactors from molybdoenzymes and in vitro reconstitution of nitrogenase and nitrate reductase. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[93]  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.

[94]  D. Werner,et al.  Reduction of acetylene and hydrazine with a molybdenum-glutathione complex. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[95]  M. Losada,et al.  185W-labelled nitrate reductase from Chlorella , 1972 .

[96]  G. Schrauzer,et al.  Chemical evolution of a nitrogenase model. I. Reduction of acetylene and other substrates by a molybdenum-thiol catalyst system , 1970 .

[97]  Alexander R. Barron,et al.  Molybdenum limitation of asymbiotic nitrogen fixation in tropical forest soils , 2009 .

[98]  Thomas Wichard,et al.  Molybdenum speciation and bioavailability in soils , 2008 .

[99]  J. Gallon,et al.  Genetics and regulation of nitrogen fixation in free-living bacteria , 2005 .

[100]  R. Pau Molybdenum Uptake and Homeostasis , 2004 .

[101]  K. Shanmugam,et al.  Molybdate transport. , 2001, Research in microbiology.

[102]  F. Albert Cotton,et al.  Advanced Inorganic Chemistry , 1999 .

[103]  R. Hernández-Molina,et al.  Chalcogenide-bridged cuboidal clusters with M4Q4 (M = Mo, W; Q = S, Se, Te) cores , 1999 .

[104]  K. Jones,et al.  Other less abundant elements of potential environmental significance , 1995 .

[105]  T. Ho,et al.  Molecules, clusters, solids and catalysts in early transition metal sulphide systems , 1989 .

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

[107]  B. Hoffman,et al.  ENDOR of the resting state of nitrogenase molybdenum―iron proteins from Azotobacter vinelandii, Klebsiella pneumoniae, and Clostridium pasteurianum: 1H, 57Fe, 95Mo, and 33S studies , 1986 .

[108]  W. Brill,et al.  Molybdenum in nitrogenase. , 1984, Annual review of biochemistry.

[109]  J. Neilands Microbial iron compounds. , 1981, Annual review of biochemistry.

[110]  M. T. Pope,et al.  A Comparison between the Chemistry and Biochemistry of Molybdenum and Related Elements , 1980 .