SCIENTIA SINICA Chimica, Volume 44, Issue 12: 1849-1864(2014) https://doi.org/10.1360/N032014-00215

Catalytic site of nitrogenases and its chemical simulations

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  • AcceptedOct 9, 2014
  • PublishedDec 18, 2014


Nitrogenase catalyzes the reduction of dinitrogen to ammonia in the process of biological nitrogen fixation. In the past few decades, its catalytic mechanism and chemical simulation have been widely studied. The high resolution X-ray structural analysis of the MoFe protein in nitrogenase reveals the iron molybdenum cofactor (FeMo-co) as a cage structure, MoFe7S9C(R-homocit). The molybdenum atom is coordinated by three sulfur atoms, a nitrogen atom from histidine residue and two oxygen atoms from R-homocitrate. Recently, the model has been modified as a protonated structure of MoFe7S9C(R-Hhomocit). Homocitrate and imidazole sidechain may play important roles in delivering proton and stabilizing the MoFe7S9C cluster in the process of N2 reduction. However the mechanism of N2 reduction remains unclear. In this review, the chemistry of molybdenum with homocitrate and imidazole is discussed, including the iron molybdenum sulfur complexes, which will be helpful to understand the coordination environment of molybdenum atom in iron molybdenum cofactor.


[1] Burgess BK, Lowe DJ. Mechanism of molybdenum nitrogenase. Chem Rev, 1996, 96: 2983-3011

[2] Howard JB, Rees DC. Structural basis of biological nitrogen fixation. Chem Rev, 1996, 96: 2965-2982

[3] Thorneley RNF, Lowe DJ. Nitrogenase: substrate binding and activation. J Biol Inorg Chem, 1996, 1: 576-580

[4] Christiansen J, Dean DR, Seefeldt LC. Mechanistic features of the Mo-containing nitrogenase. Annu Rev Plant Physiol Plant Mol Biol, 2001, 52: 269-295

[5] Seefeldt LC, Hoffman BM, Dean DR. Mechanism of Mo-dependent nitrogenase. Annu Rev Biochem, 2009, 78: 701-722

[6] Lee CC, Hu Y, Ribbe MW. Vanadium nitrogenase reduces CO. Science, 2010, 329: 642

[7] Kim JS, Rees DC. Crystallographic structure and functional implications of the nitrogenase molybdenum iron protein from Azotobacter-vinelandii. Nature, 1992, 360: 553-560

[8] Kim JS, Rees DC. Structural models for the metal centers in the nitrogenase molybdenum-iron protein. Science, 1992, 257: 1677-1682

[9] Georgiadis MM, Komiya H, Chakrabarti P, Woo D, Kornuc JJ, Rees DC. Crystallographic structure of the nitrogenase iron protein from Azotobacter-vinelandii. Science, 1992, 257: 1653-1659

[10] Peters JW, Stowell MHB, Soltis SM, Finnegan MG, Johnson MK, Rees DC. Redox-dependent structural changes in the nitrogenase P-cluster. Biochemistry, 1997, 36: 1181-1187

[11] Mayer SM, Lawson DM, Gormal CA, Roe SM, Smith BE. New insights into structure-function relationships in nitrogenase: a 1.6 angstrom resolution X-ray crystallographic study of Klebsiella pneumoniae MoFe-protein. J Mol Biol, 1999, 292: 871-891

[12] Einsle O, Tezcan FA, Andrade SLA, Schmid B, Yoshida M, Howard JB, Rees DC. Nitrogenase MoFe-protein at 1.16 angstrom resolution: a central ligand in the FeMo-cofactor. Science, 2002, 297: 1696-1700

[13] Spatzal T, Aksoyoglu M, Zhang LM, Andrade SLA, Schleicher E, Weber S, Rees DC, Einsle O. Evidence for interstitial carbon in nitrogenase FeMo cofactor. Science, 2011, 334: 940

[14] Lancaster KM, Roemelt M, Ettenhuber P, Hu YL, Ribbe MW, Neese F, Bergmann U, DeBeer S. X-ray emission spectroscopy evidences a central carbon in the nitrogenase iron-molybdenum cofactor. Science, 2011, 334: 974-977

[15] Chen CY, Chen ML, Chen HB, Wang HX, Cramer SP, Zhou ZH. a-Hydroxy coordination of mononuclear vanadyl citrate, malate and S-citramalate with N-heterocycle ligand, implying a new protonation pathway of iron-vanadium cofactor in nitrogenase. J Inorg Biochem, 2014, 141: 114-120

[16] Christiansen J, Goodwin PJ, Lanzilotta WN, Seefeldt LC, Dean DR. Catalytic and biophysical properties of a nitrogenase apo-MoFe protein produced by a nifB-deletion mutant of Azotobacter vinelandii. Biochemistry, 1998, 37: 12611-12623

[17] Imperial J, Hoover TR, Madden MS, Ludden PW, Shah VK. Substrate reduction properties of dinitrogenase activated in vitro are dependent upon the presence of homocitrate or its analogues during iron-molybdenum cofactor synthesis. Biochemistry, 1989, 28: 7796-7799

[18] Madden MS, Paustian TD, Ludden PW, Shah VK. Effects of homocitrate, homocitrate lactone, and fluorohomocitrate on nitrogenase in NifV-mutants of Azotobacter vinelandii. J Bacteriol, 1991, 173: 5403-5405

[19] Pollock RC, Lee HI, Cameron LM, Derose VJ, Hales BJ, Ormejohnson WH, Hoffman BM. Investigation of CO bound to inhibited forms of nitrogenase mofe protein by C-13 ENDOR. J Am Chem Soc, 1995, 117: 8686-8687

[20] Christie PD, Lee HI, Cameron LM, Hales BJ, OrmeJohnson WH, Hoffman BM. Identification of the CO-binding cluster in nitrogenase MoFe protein by ENDOR of Fe-57 isotopomers. J Am Chem Soc, 1996, 118: 8707-8709

[21] Lee HI, Cameron LM, Hales BJ, Hoffman BM. CO binding to the FeMo cofactor of CO-inhibited nitrogenase: (CO)-C-13 and H-1 Q-band ENDOR investigation. J Am Chem Soc, 1997, 119: 10121-10126

[22] Yang ZY, Seefeldt LC, Dean DR, Cramer SP, George SJ. Steric control of the Hi-CO MoFe nitrogenase complex revealed by stopped-flow infrared spectroscopy. Angew Chem, 2011, 123: 286-289

[23] Dos Santos PC, Igarashi RY, Lee HI, Hoffman BM, Seefeldt LC, Dean DR. Substrate interactions with the nitrogenase active site. Acc Chem Res, 2005, 38: 208-214

[24] Dance I. The consequences of an interstitial N atom in the FeMo cofactor of nitrogenase. Chem Commun, 2003, 3: 324-325

[25] Lovell T, Liu TQ, Case DA, Noodleman L. Structural, spectroscopic, and redox consequences of central ligand in the FeMoco of nitrogenase: a density functional theoretical study. J Am Chem Soc, 2003, 125: 8377-8383

[26] Schimpl J, Petrilli HM, Blochl PE. Nitrogen binding to the FeMo-cofactor of nitrogenase. J Am Chem Soc, 2003, 125: 15772-15778

[27] Huniar U, Ahlrichs R, Coucouvanis D. Density functional theory calculations and exploration of a possible mechanism of N-2 reduction by nitrogenase. J Am Chem Soc, 2004, 126: 2588-2601

[28] Dance I. The hydrogen chemistry of the FeMo-co active site of nitrogenase. J Am Chem Soc, 2005, 127: 10925-10942

[29] Dance I. Mechanistic significance of the preparatory migration of hydrogen atoms around the FeMo-co active site of nitrogenase. Biochemistry, 2006, 45: 6328-6340

[30] Dance I. Elucidating the coordination chemistry and mechanism of biological nitrogen fixation. Chem-Asian J, 2007, 2: 936-946

[31] Dance I. The chemical mechanism of nitrogenase: calculated details of the intramolecular mechanism for hydrogenation of η2-N2 on FeMo-co to NH3. Dalton Trans, 2008: 5977-5991

[32] Dance I. The chemical mechanism of nitrogenase: hydrogen tunneling and further aspects of the intramolecular mechanism for hydrogenation of η2-N2 on FeMo-co to NH3. Dalton Trans, 2008: 5992-5998

[33] Pelmenschikov V, Case DA, Noodleman L. Ligand-bound S=1/2 FeMo-cofactor of nitrogenase: hyperfine interaction analysis and implication for the central ligand X identity. Inorg Chem, 2008, 47: 6162-6172

[34] Dance I. Ramifications of C-centering rather than N-centering of the active site FeMo-co of the enzyme nitrogenase. Dalton Trans, 2012, 41: 4859-4865

[35] Wiig JA, Lee CC, Hu Y, Ribbe MW. Tracing the interstitial carbide of the nitrogenase cofactor during substrate turnover. J Am Chem Soc, 2013, 135: 4982-4983

[36] Lancaster KM, Hu Y, Bergmann U, Ribbe MW, DeBeer S. X-ray spectroscopic observation of an interstitial carbide in NifEN-bound FeMoco precursor. J Am Chem Soc, 2013, 135: 610-612

[37] Seefeldt LC, Dance IG, Dean DR. Substrate interactions with nitrogenase: Fe versus Mo. Biochemistry, 2004, 43: 1401-1409

[38] Hoover TR, Robertson AD, Cerny RL, Hayes RN, Imperial J, Shah VK, Ludden PW. Identification of the V factor needed for synthesis of the iron-molybdenum cofactor of nitrogenase as homocitrate. Nature, 1987, 329: 855-857

[39] Hawkes TR, McLean PA, Smith BE. Nitrogenase from nifV mutants of Klebsiella pneumoniae contains an altered form of the iron-molybdenum cofactor. Biochem J, 1984, 217: 317-321

[40] McLean PA, Smith BE, Dixon RA. Nitrogenase of Klebsiella pneumoniae nifV mutants. Biochem J, 1983, 211: 589-597

[41] Gronberg KLC, Gormal CA, Smith BE, Henderson RA. A new approach to identifying substrate binding sites on isolated FeMo-cofactor of nitrogenase. Chem Commun, 1997, 7: 713-714

[42] Gronberg KLC, Gormal CA, Durrant MC, Smith BE, Henderson RA. Why R-Homocitrate is essential to the reactivity of FeMo-cofactor of nitrogenase: studies on NifV--extracted FeMo-cofactor. J Am Chem Soc, 1998, 120: 10613-10621

[43] Hoover TR, Imperial J, Liang JH, Ludden PW, Shah VK. Dinitrogenase with altered substrate specificity results from the use of homocitrate analogs for in vitro synthesis of the iron-molybdenum cofactor. Biochemistry, 1988, 27: 3647-3652

[44] Hu YL, Ribbe MW. Biosynthesis of the iron-molybdenum cofactor of nitrogenase. J Biol Chem, 2013, 288: 13173-13177

[45] Ludden PW, Shah VK, Roberts GP, Homer M, Allen R, Paustian T, Roll J, Chatterjee R, Madden M, Allen J. Biosynthesis of the iron-molybdenum cofactor of nitrogenase. ACS Symp Ser, 1993, 535: 196-215

[46] Liang JH, Madden M, Shah VK, Burris RH. Citrate substitutes for homocitrate in nitrogenase of a nifV mutant of Klebsiella pneumoniae. Biochemistry, 1990, 29: 8577-8581

[47] Mayer SM, Gormal CA, Smith BE, Lawson DM. 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, 2002, 277: 35263-35266

[48] Igarashi RY, Seefeldt LC. Nitrogen fixation: the mechanism of the Mo-dependent nitrogenase. Crit Rev Biochem Mol Biol, 2003, 38: 351-384

[49] Hoffman BM, Dean DR, Seefeldt LC. Climbing nitrogenase: toward a mechanism of enzymatic nitrogen fixation. Acc Chem Res, 2009, 42: 609-619

[50] Hoffman BM, Lukoyanov D, Yang ZY, Dean DR, Seefeldt LC. Mechanism of nitrogen fixation by nitrogenase: the next stage. Chem Rev, 2014, 114: 4041-4062

[51] Wilson PE, Nyborg AC, Watt GD. Duplication and extension of the Thorneley and Lowe kinetic model for Klebsiella pneumoniae nitrogenase catalysis using a MATHEMATICA software platform. Biophys Chem, 2001, 91: 281-304

[52] Thorneley RNF, Lowe DJ. Kinetics and mechanism of the nitrogenase enzyme system. In: Spiro TG, ed. Molybdenum Enzymes. New York: John Wiley & Sons, 1985

[53] Tsai KR, Wan HL. On the structure-function relationship of nitrogenase M-cluster and P-cluster pairs. J Cluster Sci, 1995, 6: 485-501

[54] 万惠霖, 黄静伟, 张凤章, 周朝晖, 张鸿图, 许良树, 蔡启瑞. 化学探针方法研究固氮酶M-簇和P-簇对的结构与功能关系. 厦门大学学报(自然科学版), 1996, 35: 890-899

[55] Durrant MC. An atomic-level mechanism for molybdenum nitrogenase. Part 2. Proton reduction, inhibition of dinitrogen reduction by dihydrogen, and the HD formation reaction. Biochemistry, 2002, 41: 13946-13955

[56] Simpson FB, Burris RH. A nitrogen pressure of 50 atmospheres does not prevent evolution of hydrogen by nitrogenase. Science, 1984, 224: 1095-1097

[57] Dance I. The stereochemistry and dynamics of the introduction of hydrogen atoms onto FeMo-co, the active site of nitrogenase. Inorg Chem, 2013, 52: 13068-13077

[58] Dance I. Nitrogenase: a general hydrogenator of small molecules. Chem Commun, 2013, 49: 10893-10907

[59] Dance I. The mechanistically significant coordination chemistry of dinitrogen at FeMo-co, the catalytic site of nitrogenase. J Am Chem Soc, 2007, 129: 1076-1088

[60] Spatzal T, Perez KA, Einsle O, Howard JB, Rees DC. Ligand binding to the FeMo-cofactor: structures of CO-bound and reactivated nitrogenase. Science, 2014, 345: 1620-1623

[61] Chen Z, Lin GX, Cai SH, Xu X, Huang JW, Wan HL, Cai QR. H-1 NMR study on the products of the catalytic reduction of ethyne by nitrogenase in D2O. Acta Chim Sinica, 1999, 57: 907-913

[62] Dance I. The mechanism of nitrogenase. Computed details of the site and geometry of binding of alkyne and alkene substrates and intermediates. J Am Chem Soc, 2004, 126: 11852-11863

[63] Fisher K, Dilworth MJ, Kim CH, Newton WE. Azotobacter vinelandii nitrogenases containing altered MoFe proteins with substitutions in the FeMo-cofactor environment: effects on the catalyzed reduction of acetylene and ethylene. Biochemistry, 2000, 39: 2970-2979

[64] Bazhenova TA, Bardina NV, Petrova GN, Borovinskaya MA. Effect of the potential of an external electron donor on C2H2 reduction catalyzed by the nitrogenase active center (FeMoco) isolated from the enzyme. Russ Chem Bull, 2004, 53: 1646-1654

[65] Han JH, Newton WE. Differentiation of acetylene-reduction sites by stereoselective proton addition during Azotobacter vinelandii nitrogenase-catalyzed C2D2 reduction. Biochemistry, 2004, 43: 2947-2956

[66] Dance I. How does vanadium nitrogenase reduce CO to hydrocarbons. Dalton Trans, 2011, 40: 5516-5527

[67] Yan LF, Dapper CH, George SJ, Wang HX, Mitra D, Dong WB, Newton WE, Cramer SP. Photolysis of Hi-CO nitrogenase—observation of a plethora of distinct CO species using infrared spectroscopy. Eur J Inorg Chem, 2011, 2011: 2064-2074

[68] Yan LF, Pelmenschikov V, Dapper CH, Scott AD, Newton WE, Cramer SP. IR-monitored photolysis of CO-inhibited nitrogenase: a major EPR-silent species with coupled terminal CO ligands. Chemistry, 2012, 18: 16349-16357

[69] Seefeldt LC, Yang ZY, Duval S, Dean DR. Nitrogenase reduction of carbon-containing compounds. Biochim Biophys Acta, 2013, 1827: 1102-1111

[70] Yandulov DV, Schrock RR. Catalytic reduction of dinitrogen to ammonia at a single molybdenum center. Science, 2003, 301: 76-78

[71] Rodriguez MM, Bill E, Brennessel WW, Holland PL. N2 reduction and hydrogenation to ammonia by a molecular iron-potassium complex. Science, 2011, 334: 780-783

[72] Hernandez JA, Curatti L, Aznar CP, Perova Z, Britt RD, Rubio LM. Metal trafficking for nitrogen fixation: NifQ donates molybdenum to NifEN/NifH for the biosynthesis of the nitrogenase FeMo-cofactor. Proc Natl Acad Sci USA, 2008, 105: 11679-11684

[73] Rubio LM, Ludden PW. Biosynthesis of the iron-molybdenum cofactor of nitrogenase. Annul Rev Microbiol, 2008, 62: 93-111

[74] Yang JG, Xie XQ, Wang X, Dixon R, Wang YP. Reconstruction and minimal gene requirements for the alternative iron-only nitrogenase in Escherichia coli. Proc Natl Acad Sci USA, 2014, 111: E3718-E3725

[75] Ribbe MW, Hu YL, Hodgson KO, Hedman B. Biosynthesis of nitrogenase metalloclusters. Chem Rev, 2014, 114: 4063-4080

[76] Corbett MC, Hu YL, Fay AW, Ribbe MW, Hedman B, Hodgson KO. Structural insights into a protein-bound iron-molybdenum cofactor precursor. Proc Natl Acad Sci USA, 2006, 103: 1238-1243

[77] George SJ, Igarashi RY, Xiao Y, Hernandez JA, Demuez M, Zhao D, Yoda Y, Ludden PW, Rubio LM, Cramer SP. 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. J Am Chem Soc, 2008, 130: 5673-5680

[78] Kaiser JT, Hu Y, Wiig JA, Rees DC, Ribbe MW. Structure of precursor-bound NifEN: a nitrogenase FeMo cofactor maturase/insertase. Science, 2011, 331: 91-94

[79] Lee SC, Lo W, Holm RH. Developments in the biomimetic chemistry of cubane-type and higher nuclearity iron-sulfur clusters. Chem Rev, 2014, 114: 3579-3600

[80] Rao PV, Holm RH. Synthetic analogues of the active sites of iron-sulfur proteins. Chem Rev, 2004, 104: 527-559

[81] Wu AJ, Penner-Hahn JE, Pecoraro VL. Structural, spectroscopic, and reactivity models for the manganese catalases. Chem Rev, 2004, 104: 903-938

[82] Demadis KD, Campana CF, Coucouvanis D. Synthesis and structural characterization of the new Mo2Fe6S8(PR3)6(Cl4-cat)2 clusters-double clubanes containing 2 edge-linked MoFe3S42+ reduced cores. J Am Chem Soc, 1995, 117: 7832-7833

[83] Ye H, Rouault TA. Human iron-sulfur cluster assembly, cellular iron homeostasis, and disease. Biochemistry, 2010, 49: 4945-4956

[84] Ohki Y, Sunada Y, Tatsumi K. Synthesis of 2Fe-2S and 4Fe-4S clusters having terminal amide ligands from an iron(II) amide complex. Chem Lett, 2005, 34: 172-173

[85] Coucouvanis D, Salifoglou A, Kanatzidis MG, Dunham WR, Simopoulos A, Kostikas A. Synthesis, structural characterization, and electronic-properties of the [Fe6S6X6(M(CO)3)2]n- anions (M = Mo, W; n = 3, 4; X = Cl, Br, I). Heteronuclear clusters of possible structural relevance to the Fe/Mo/S center in nitrogenase. Inorg Chem, 1988, 27: 4066-4077

[86] Eldredge PA, Bryan RF, Sinn E, Averill BA. The [MoFe6S6(CO)16]2- ion—a new model for the FeMo-cofactor of nitrogenase. J Am Chem Soc, 1988, 110: 5573-5575

[87] Eldredge PA, Bose KS, Barber DE, Bryan RF, Sinn E, Rheingold A, Averill BA. Synthesis and structures of the MoFe6S6(CO)162-, MoFe4S3(CO)13(pet3)2-, and Mo2Fe2S2(CO)122- ions—high-nuclearity Mo-Fe-S clusters as potential precursors to models for the FeMo-cofactor of nitrogenase. Inorg Chem, 1991, 30: 2365-2375

[88] Ohki Y, Imada M, Murata A, Sunada Y, Ohta S, Honda M, Sasamori T, Tokitoh N, Katada M, Tatsumi K. Synthesis, structures, and electronic properties of 8Fe-7S cluster complexes modeling the nitrogenase P-cluster. J Am Chem Soc, 2009, 131: 13168-13178

[89] Ohki Y, Sunada Y, Honda M, Katada M, Tatsumi K. Synthesis of the P-cluster inorganic core of nitrogenases. J Am Chem Soc, 2003, 125: 4052-4053

[90] Ohki Y, Tanifuji K, Yamada N, Cramer RE, Tatsumi K. Formation of a nitrogenase P-cluster Fe8S7 core via reductive fusion of two all-ferric Fe4S4 clusters. Chem-Asian J, 2012, 7: 2222-2224

[91] Li DM, Xu JQ, Li ZC, Xing YH, Wang RZ, Liu SQ, Sun HR, Wang TG. Preparation and characterization of a novel complex of molybdenum (V) with homocitrate, K5(NH4) Mo2O2S2(C7H6O7)2·4H2O. Synth React Inorg M, 2000, 30: 319-333

[92] Li DM, Xing YH, Li ZC, Xu JQ, Song WB, Wang TG, Yang GD, Hu NH, Jia HQ, Zhang HM. Synthesis and characterization of binuclear molybdenum-polycarboxylate complexes with sulfur bridges. J Inorg Biochem, 2005, 99: 1602-1610

[93] Zhou ZH, Hou SY, Cao ZX, Tsai KR, Chow YL. Syntheses, spectroscopies and structures of molybdenum (VI) complexes with homocitrate. Inorg Chem, 2006, 45: 8447-8451

[94] Zhou ZH, Wang HX, Yu P, Olmstead MM, Cramer SP. Structure and spectroscopy of a bidentate bis-homocitrate dioxo-molybdenum (VI) complex: insights relevant to the structure and properties of the FeMo-cofactor in nitrogenase. J Inorg Biochem, 2013, 118: 100-106

[95] Cruywagen JJ, Rohwer EA, Wessels GFS. Molybdenum (VI) complex formation—8. Equilibria and thermodynamic quantities for the reactions with citrate. Polyhedron, 1995, 14: 3481-3493

[96] Cuin A, Massabni AC. Synthesis and characterization of solid molybdenum (VI) complexes with glycolic, mandelic and tartaric acids. Photochemistry behaviour of the glycolate molybdenum complex. J Coord Chem, 2007, 60: 1933-1940

[97] Zhang RH, Zhou ZH, Wan HL. Solid and solution structural studies of dimeric and tetrameric molybdenum (VI) malate complexes. Chin J Struct Chem, 2008, 27: 919-926

[98] Zhou ZH, Wan HL, Tsai KR. Molybdenum (VI) complex with citric acid: synthesis and structural characterization of 1:1 ratio citrate molybdate K2Na4(MoO2)2O(cit)2·5H2O. Polyhedron, 1997, 16: 75-79

[99] Xing YH, Xu HQ, Sun HR, Li DM, Xing Y, Lin YH, Jia HQ. A new dinuclear molybdenum (V)-sulfur complex containing citrate ligand: synthesis and characterization of K2.5Na2NH4Mo2O2S2(cit)2·5H2O. Eur J Solid State Inorg Chem, 1998, 35: 745-756

[100] Zhou XH, Xing YH, Xu JQ, Li DM, Wang RZ, Liu SQ, Zeng QX, Huang XY. Mobybdenum (VI)-oxygen complex containing citrage ligand: synthesis and characterization of K6Mo2O5(cit)2·5H2O. Solid State Sci, 1999, 1: 189-198

[101] Zhou ZH, Wan HL, Tsai KR. Syntheses and spectroscopic and structural characterization of molybdenum (VI) citrato monomeric raceme and dimer, K4MoO3(cit)·2H2O and K4(MoO2)2O(Hcit)2·4H2O. Inorg Chem, 2000, 39: 59-64

[102] Hamada YZ, Bayakly N, George D, Greer T. Speciation of molybdenum (VI)-citric acid complexes in aqueous solutions. Synth React Inorg M, 2008, 38: 664-668

[103] Zhang RH, Zhou XW, Guo YC, Chen ML, Cao ZX, Chow YL, Zhou ZH. Crystalline and solution chemistry of tetrameric and dimeric molybdenum (VI) citrato complexes. Inorg Chim Acta, 2013, 406: 27-36

[104] Zhou ZH, Deng YF, Cao ZX, Zhang RH, Chow YL. Dimeric dioxomolybdenum (VI) and oxomolybdenum (V) complexes with citrate at very low pH and neutral conditions. Inorg Chem, 2005, 44: 6912-6914

[105] Zhou ZH, Chen CY, Cao ZX, Tsai KR, Chow YL. N-heterocycle chelated oxomolybdenum (VI and V) complexes with bidentate citrate. Dalton Trans, 2008: 2475-2479

[106] Wright DW, Chang RT, Mandal SK, Armstrong WH, Orme-Johnson WH. Novel vanadium (V) homocitrate complex: synthesis, structure, and biological relevance of K2(H2O)5(VO2)2(R,S-homocitrate)2·H2O. J Biol Inorg Chem, 1996, 1: 143-151

[107] Chen CY, Zhou ZH, Mao SY, Wan HL. Asymmetric dinuclear hydroxyl and ethoxyl citrato dioxovanadates (V). J Coord Chem, 2007, 60: 1419-1426

[108] Chen CY, Zhou ZH, Chen HB, Huang PQ, Tsai KR, Chow YL. Formations of mixed-valence oxovanadium (V, IV) citrates and homocitrate with N-heterocycle chelated ligand. Inorg Chem, 2008, 47: 8714-8720

[109] Biagioli M, Strinna-Erre L, Micera G, Panzanelli A, Zema M. Molecular structure, characterization and reactivity of dioxo complexes formed by vanadium (V) with alpha-hydroxycarboxylate ligands. Inorg Chim Acta, 2000, 310: 1-9

[110] Demartin F, Biagioli M, Strinna-Erre L, Panzanelli A, Micera G. Molecular structure of a mono-peroxo vanadium (V) complex formed by D, L-lactic acid. Inorg Chim Acta, 2000, 299: 123-127

[111] Sergienko VS. Structural chemistry of oxoperoxo complexes of vanadium (V): a review. Crystallogr Rep, 2004, 49: 401-426

[112] Zhou ZH, Hou SY, Cao ZX, Wan HL, Ng SW. Syntheses, crystal structures and biological relevance of glycolato and S-lactato molybdates. J Inorg Biochem, 2004, 98: 1037-1044

[113] Schwendt P, Tracey AS, Tatiersky J, Galikova J, Zak Z. Vanadium (V) tartrato complexes: speciation in the H3O+(OH-)/ H2VO4-/ (2R,3R)-tartrate system and X-ray crystal structures of Na4[V4O8(rac-tart)2]·12H2O and (NEt4)4[V4O8((R,R)-tart)2]·6H2O (tart = C4H2O64-). Inorg Chem, 2007, 46: 3971-3983

[114] Galikova J, Schwendt P, Tatiersky J, Tracey AS, Zak Z. Stereospecific formation of dinuclear vanadium (V) tartrato complexes. Inorg Chem, 2009, 48: 8423-8430

[115] Yun G, Hwang Y, Yun H, Do J, Jacobson AJ. A vanadium tellurate, (NH4)2(VO2)2[TeO4(OH)2], containing two edge-shared square- pyramidal VO5 groups. Inorg Chem, 2010, 49: 229-233

[116] Llopis E, Ramirez JA, Domenech A, Cervilla A. Tungsten (VI) complexes with citric acid (H4cit). Structural characterisation of Na6[{WO2-(cit)}2O]·10H2O. J Chem Soc Dalton Trans, 1993: 1121-1124

[117] Wang G, Zhou ZH, Zhang H, Ye JL, Wan HL. Synthesis, spectroscopic properties and structural characterization of sodium potassium citrato oxotungstate (VI) dimer. Chin J Struct Chem, 2000, 19: 181-186

[118] Zhang H, Zhao H, Jiang YQ, Hou SY, Zhou ZH, Wan HL. pH- and mol-ratio dependent tungsten (VI)-citrate speciation from aqueous solutions: syntheses, spectroscopic properties and crystal structures. Inorg Chim Acta, 2003, 351: 311-318

[119] Kim JS, Rees DC. Structural models for the metal centers in the nitrogenase molybdenum-iron protein. Science, 1992, 257: 1677-1682

[120] Chan MK, Kim JS, Rees DC. The nitrogenase FeMo-cofactor and P-cluster pair: 2.2 Å resolution structures. Science, 1993, 260: 792-794

[121] Schindelin H, Kisker C, Schlessman JL, Howard JB, Rees DC. Structure of ADP·AIF-4--stabilized nitrogenase complex and its implications for signal transduction. Nature, 1997, 387: 370-376

[122] Zhou ZH, Yan WB, Wan HL, Tsai KR. Synthesis and characterization of homochiral polymeric S-malato molybdate (VI): toward the potentially stereospecific formation and absolute configuration of iron-molybdenum cofactor in nitrogenase. J Inorg Biochem, 2002, 90: 137-143

[123] Zhou ZH, Wan HL, Tsai KR. Bidentate citrate with free terminal carboxyl groups, syntheses and characterization of citrato oxomolybdate (VI) and oxotungstate (VI), Δ/Λ-Na2MO2(H2cit)2·3H2O (M = Mo or W). J Chem Soc Dalton Trans, 1999: 4289-4290

[124] Zhao H, Jiang YQ, Zhang H, Zhao ZH. Synthesis and crystal structure of ammonium cis-dioxo dibenzilato tungstate (VI) dihydrate. Chin J Struct Chem, 2004, 23: 502-505

[125] 颜文斌, 周朝晖, 章慧. 苹果酸钼外消旋体的合成、光谱性质和结构表征. 高等学校化学学报, 2001, 22: 2091-2094

[126] 颜文斌, 侯书雅, 赵宏, 周朝晖. 光学活性苹果酸氧钼(VI)络合物的合成、表征和晶体结构. 化学通报, 2001, 64: W117

[127] Hou SY, Yan WB, Ma ZJ. Syntheses, characterization and stereochemistry of S- and R,S-hydrogenmalato dioxotungstaten (VI). J Coord Chem, 2003, 56: 133-139

[128] Zhou ZH, Wang GF, Hou SY, Wan HL, Tsai KR. Tungsten-malate interaction. Synthesis, spectroscopic and structural studies of homochiral S-malato tungstate (VI), Na3WO2H (S-mal)2. Inorg Chim Acta, 2001, 314: 184-188

[129] Dance I. A molecular pathway for the egress of ammonia produced by nitrogenase. Sci Rep, 2013, 3: 3237

[130] Hu Y, Ribbe MW. Biosynthesis of nitrogenase FeMoco. Coord Chem Rev, 2011, 255: 1218-1224

[131] Kowalewski B, Poppe J, Demmer U, Warkentin E, Dierks T, Ermler U, Schneider K. Nature’s polyoxometalate chemistry: X-ray structure of the Mo storage protein loaded with discrete polynuclear Mo-O clusters. J Am Chem Soc, 2012, 134: 9768-9774

[132] Chen QL, Chen HB, Cao ZX, Zhou ZH. Synthesis, spectral, and structural characterizations of imidazole oxalato molybdenum (IV/V/VI) complexes. Dalton Trans, 2013, 42: 1627-1636

[133] 陈洪斌. 高柠檬酸同系物的合成及固氮酶催化反应中的质子传递研究. 博士学位论文. 厦门: 厦门大学, 2006

[134] 郭青娟, 彭涛, 常天驹, 张刚, 姜伟, 李颖, 李季伦. 产酸克氏杆菌(Klebsiella oxytoca)钼铁蛋白a-423Ile位点的突变导致固氮酶催化活性降低. 科学通报, 2014, 59: 1215-1222

[135] 关锋, 赵德华, 潘淼, 姜伟, 李季伦. N2和H+在固氮酶活性中心金属原子簇中还原位点的分析. 科学通报, 2007, 52: 1141-1146

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