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Nitrogenase Structure and Function Relationships by Density Functional Theory

  • Travis V. HarrisEmail author
  • Robert K. Szilagyi
Protocol
Part of the Methods in Molecular Biology book series (MIMB, volume 766)

Abstract

Modern density functional theory has tremendous potential with matching popularity in metalloenzymology to reveal the unseen atomic and molecular details of structural data, spectroscopic measurements, and biochemical experiments by providing insights into unobservable structures and states, while also offering theoretical justifications for observed trends and differences. An often untapped potential of this theoretical approach is to bring together diverse experimental structural and reactivity information and allow for these to be critically evaluated at the same level. This is particularly applicable for the tantalizingly complex problem of the structure and molecular mechanism of biological nitrogen fixation. In this chapter we provide a review with extensive practical details of the compilation and evaluation of experimental data for an unbiased and systematic density functional theory analysis that can lead to remarkable new insights about the structure–function relationships of the iron–sulfur clusters of nitrogenase.

Key words

Density functional theory electronic structure exchange functional correlation functional basis set saturation spectroscopic calibration broken symmetry calculation ferromagnetic coupling antiferromagnetic coupling exchange interaction 

References

  1. 1.
    Hohenberg P, Kohn W (1964) Inhomogeneous electron gas. Phys Rev 136:B864–B871CrossRefGoogle Scholar
  2. 2.
    Kohn W, Sham LJ (1965) Self-consistent equations including exchange and correlation effects. Phys Rev 140:A1133–A1138CrossRefGoogle Scholar
  3. 3.
    Koch W, Holthausen MC (2000) A chemist’s guide to density functional theory, Wiley-VCH, WeinheimGoogle Scholar
  4. 4.
    Slater JC, Johnson KH (1972) Self-consistent-field Xα cluster method for polyatomic molecules and solids. Phys Rev B 5:844–853CrossRefGoogle Scholar
  5. 5.
    Slater JC (1951) A simplification of the Hartree-Fock method. Phys Rev 81:385–390CrossRefGoogle Scholar
  6. 6.
    Perdew JP, Schmidt K (2001) Jacob’s ladder of density functional approximations for the exchange-correlation energy. AIP Conf Proc 577:1–20CrossRefGoogle Scholar
  7. 7.
    Ruzsinszky A, Perdew JP, Csonka GI (2010) The RPA atomization energy puzzle. J Chem Theory Comput 6:127–134CrossRefGoogle Scholar
  8. 8.
    Becke AD (1993) A new mixing of Hartree-Fock and local density-functional theories. J Chem Phys 98:1372–1377CrossRefGoogle Scholar
  9. 9.
    Becke AD (1993) Density-functional thermochemistry. III. The role of exact exchange. J Chem Phys 98:5648–5652CrossRefGoogle Scholar
  10. 10.
    Perdew JP (1986) Density-functional approximation for the correlation energy of the inhomogeneous electron gas. Phys Rev B 33:8822–8824CrossRefGoogle Scholar
  11. 11.
    Becke AD (1988) Density-functional exchange-energy approximation with correct asymptotic behavior. Phys Rev A 38:3098–3100PubMedCrossRefGoogle Scholar
  12. 12.
    Szilagyi RK, Metz M, Solomon EI (2002) Spectroscopic calibration of modern density functional methods using [CuCl4]2–. J Phys Chem A 106:2994–3007CrossRefGoogle Scholar
  13. 13.
    Siegbahn PEM, Blomberg MRA (2000) Transition-metal systems in biochemistry studied by high-accuracy 0quantum chemical methods. Chem Rev 100:421–437PubMedCrossRefGoogle Scholar
  14. 14.
    Noodleman L, Lovell T, Han WG et al (2004) Quantum chemical studies of intermediates and reaction pathways in selected enzymes and catalytic synthetic systems. Chem Rev 104:459–508PubMedCrossRefGoogle Scholar
  15. 15.
    Grimme S (2006) Semiempirical GGA-type density functional constructed with a long-range dispersion correction. J Comput Chem 27:1787–1799PubMedCrossRefGoogle Scholar
  16. 16.
    Chai JD, Head-Gordon M (2008) Long-range corrected hybrid density functionals with damped atom-atom dispersion corrections. Phys Chem Chem Phys 10:6615–6620PubMedCrossRefGoogle Scholar
  17. 17.
    Zhao Y, Truhlar DG (2008) The M06 suite of density functionals for main group thermochemistry, thermochemical kinetics, noncovalent interactions, excited states, and transition elements: two new functionals and systematic testing of four M06-class functionals and 12 other functionals. Theor Chem Acc 120:215–241CrossRefGoogle Scholar
  18. 18.
    Noodleman L (1981) Valence bond description of anti-ferromagnetic coupling in transition-metal dimers. J Chem Phys 74:5737–5743CrossRefGoogle Scholar
  19. 19.
    Neese F (2009) Prediction of molecular properties and molecular spectroscopy with density functional theory: from fundamental theory to exchange-coupling. Coord Chem Rev 253:526–563CrossRefGoogle Scholar
  20. 20.
    Szabo A, Ostlund NS (1982) Modern theoretical chemistry, MacMillan, New York, NYGoogle Scholar
  21. 21.
    Neese F (2004) Definition of corresponding orbitals and the diradical character in broken symmetry DFT calculations on spin coupled systems. J Phys Chem Solids 65:781–785CrossRefGoogle Scholar
  22. 22.
    Clark AE, Davidson ER (2001) Local spin. J Chem Phys 115:7382–7392CrossRefGoogle Scholar
  23. 23.
    Kitagawa Y, Saito T, Ito M et al (2007) Approximately spin-projected geometry optimization method and its application to di-chromium systems. Chem Phys Lett 442:445–450CrossRefGoogle Scholar
  24. 24.
    Harris TV, Szilagyi RK (2011) Comparative assessment of the composition and charge state of nitrogenase FeMo-cofactor. Inorg Chem in press, http://pubs.acs.org/doi/abs/10.1021/ic102446n
  25. 25.
    Szilagyi RK, Winslow MA (2006) On the accuracy of density functional theory for iron-sulfur clusters. J Comput Chem 27:1385–1397PubMedCrossRefGoogle Scholar
  26. 26.
    Schaefer A, Horn H, Ahlrichs R (1992) Fully optimized contracted Gaussian basis sets for atoms Li to Kr. J Chem Phys 97:2571–2577CrossRefGoogle Scholar
  27. 27.
    Schaefer A, Huber C, Ahlrichs R (1994) Fully optimized contracted Gaussian basis sets of triple zeta valence quality for atoms Li to Kr. J Chem Phys 100:5829–5835CrossRefGoogle Scholar
  28. 28.
    Krishnan R, Binkley JS, Seeger R et al (1980) Self-consistent molecular orbital methods. XX. A basis set for correlated wave functions. J Chem Phys 72:650–654CrossRefGoogle Scholar
  29. 29.
    McLean AD, Chandler GS (1980) Contracted Gaussian basis sets for molecular calculations. I. Second row atoms, Z = 11-18. J Chem Phys 72:5639–5648CrossRefGoogle Scholar
  30. 30.
    Solomon EI, Hedman B, Hodgson KO et al (2005) Ligand K-edge X-ray absorption spectroscopy: covalency of ligand-metal bonds. Coord Chem Rev 249:97–129CrossRefGoogle Scholar
  31. 31.
    Boysen RB, Szilagyi RK (2008) Development of palladium L-edge X-ray absorption spectroscopy and its application for chloropalladium complexes. Inorg Chim Acta 361:1047–1058CrossRefGoogle Scholar
  32. 32.
    Dey A, Glaser T, Couture MMJ et al (2004) Ligand K-edge X-ray absorption spectroscopy of [Fe4S4]1+,2+,3+ clusters: changes in bonding and electronic relaxation upon redox. J Am Chem Soc 126:8320–8328PubMedCrossRefGoogle Scholar
  33. 33.
    Reed AE, Weinhold F (1983) Natural bond orbital analysis of near-Hartree-Fock water dimer. J Chem Phys 78:4066–4073CrossRefGoogle Scholar
  34. 34.
    Dolg M, Wedig U, Stoll H et al (1987) Energy-adjusted ab initio pseudopotentials for the first row transition elements. J Chem Phys 86:866–872CrossRefGoogle Scholar
  35. 35.
    Ehlers AW, Bohme M, Dapprich S et al (1993) A set of f-polarization functions for pseudo-potential basis sets of the transition metals Sc-Cu, Y-Ag and La-Au. Chem Phys Lett 208:111–114CrossRefGoogle Scholar
  36. 36.
    Hollwarth A, Bohme M, Dapprich S et al (1993) A set of d-polarization functions for pseudo-potential basis sets of the main group elements Al-Bi and f-type polarization functions for Zn, Cd, Hg. Chem Phys Lett 208:237–240CrossRefGoogle Scholar
  37. 37.
    Stephens PJ, Devlin FJ, Chabalowski CF et al (1994) Ab initio calculation of vibrational absorption and circular dichroism spectra using density functional force fields. J Phys Chem 98:11623–11627CrossRefGoogle Scholar
  38. 38.
    Yoo SJ, Angove HC, Papaefthymiou V et al (2000) Mössbauer study of the MoFe protein of nitrogenase from Azotobacter vinelandii using selective 57Fe enrichment of the M-centers. J Am Chem Soc 122:4926–4936CrossRefGoogle Scholar
  39. 39.
    True AE, Nelson MJ, Venters RA et al (1988) 57Fe hyperfine coupling tensors of the FeMo cluster in Azotobacter vinelandii MoFe protein: determination by polycrystalline ENDOR spectroscopy. J Am Chem Soc 110:1935–1943CrossRefGoogle Scholar
  40. 40.
    Lovell T, Li J, Liu TQ et al (2001) FeMo cofactor of nitrogenase: a density functional study of states MN, MOX, MR, and MI. J Am Chem Soc 123:12392–12410PubMedCrossRefGoogle Scholar
  41. 41.
    Calculations involving other oxidation state distributions or compositions revealed that trends in the relative energies of spin coupling schemes are independent of the cluster composition and charge stateGoogle Scholar
  42. 42.
    Lukoyanov D, Pelmenschikov V, Maeser N et al (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 46:11437–11449PubMedCrossRefGoogle Scholar
  43. 43.
    Schimpl J, Petrilli HM, Blöchl PE (2003) Nitrogen binding to the FeMo-cofactor of nitrogenase. J Am Chem Soc 125:15772–15778PubMedCrossRefGoogle Scholar
  44. 44.
    Einsle O, Tezcan FA, Andrade SLA et al (2002) Nitrogenase MoFe-protein at 1.16 Å resolution: a central ligand in the FeMo-cofactor. Science 297:1696–1700PubMedCrossRefGoogle Scholar
  45. 45.
    Kim J, Rees DC (1992) Structural models for the metal centers in the nitrogenase molybdenum-iron protein. Science 257:1677–1682PubMedCrossRefGoogle Scholar
  46. 46.
    Lovell T, Liu TQ, Case DA et al (2003) Structural, spectroscopic, and redox consequences of central ligand in the FeMoco of nitrogenase: a density functional theoretical study. J Am Chem Soc 125:8377–8383PubMedCrossRefGoogle Scholar
  47. 47.
    Li J, Nelson MR, Peng CY et al (1998) Incorporating protein environments in density functional theory: a self-consistent reaction field calculation of redox potentials of [2Fe2S] clusters in ferredoxin and phthalate dioxygenase reductase. J Phys Chem A 102:6311–6324CrossRefGoogle Scholar
  48. 48.
    Yang X, Niu SQ, Ichiye T et al (2004) Direct measurement of the hydrogen-bonding effect on the intrinsic redox potentials of [4Fe-4S] cubane complexes. J Am Chem Soc 126:15790–15794PubMedCrossRefGoogle Scholar
  49. 49.
    Kitagawa Y, Shoji M, Saito T et al (2008) Theoretical studies on effects of hydrogen bonds attaching to cysteine ligands on 4Fe-4S clusters. Int J Quantum Chem 108:2881–2887CrossRefGoogle Scholar
  50. 50.
    Pelmenschikov V, Case DA, Noodleman L (2008) Ligand-bound S = 1/2 FeMo-cofactor of nitrogenase: hyperfine interaction analysis and implication for the central ligand X identity. Inorg Chem 47:6162–6172PubMedCrossRefGoogle Scholar
  51. 51.
    Tomasi J, Persico M (1994) Molecular interactions in solution: an overview of methods based on continuous distributions of the solvent. Chem Rev 94:2027–2094CrossRefGoogle Scholar
  52. 52.
    Cossi M, Barone V, Cammi R et al (1996) Ab initio study of solvated molecules: a new implementation of the polarizable continuum model. Chem Phys Lett 255:327–335CrossRefGoogle Scholar
  53. 53.
    Barone V, Cossi M, Tomasi J (1998) Geometry optimization of molecular structures in solution by the polarizable continuum model. J Comput Chem 19:404–417CrossRefGoogle Scholar
  54. 54.
    Lovell T, Li J, Case DA et al (2002) FeMo cofactor of nitrogenase: energetics and local interactions in the protein environment. J Biol Inorg Chem 7:735–749PubMedCrossRefGoogle Scholar
  55. 55.
    Xie HJ, Wu RB, Zhou ZH et al (2008) Exploring the interstitial atom in the FeMo cofactor of nitrogenase: insights from QM and QM/MM calculations. J Phys Chem B 112:11435–11439PubMedCrossRefGoogle Scholar
  56. 56.
    Rokhsana D, Dooley DM, Szilagyi RK (2008) Systematic development of computational models for the catalytic site in galactose oxidase: impact of outer-sphere residues on the geometric and electronic structures. J Biol Inorg Chem 13:371–383PubMedCrossRefGoogle Scholar
  57. 57.
    Siegbahn PEM, Himo F (2009) Recent developments of the quantum chemical cluster approach for modeling enzyme reactions. J Biol Inorg Chem 14:643–651PubMedCrossRefGoogle Scholar
  58. 58.
    Igarashi RY, Seefeldt LC (2003) Nitrogen fixation: the mechanism of the Mo-dependent nitrogenase. Crit Rev Biochem Mol Biol 38:351–384PubMedCrossRefGoogle Scholar
  59. 59.
    Huang HQ, Kofford M, Simpson FB et al (1993) Purification, composition, charge, and molecular weight of the FeMo cofactor from Azotobacter vinelandii nitrogenase. J Inorg Biochem 52:59–75PubMedCrossRefGoogle Scholar
  60. 60.
    Pickett CJ, Vincent KA, Ibrahim SK et al (2003) Electron-transfer chemistry of the iron-molybdenum cofactor of nitrogenase: delocalized and localized reduced states of FeMoco which allow binding of carbon monoxide to iron and molybdenum. Chem Eur J 9:76–87PubMedCrossRefGoogle Scholar
  61. 61.
    Hedman B, Frank P, Gheller SF et al (1988) New structural insights into the iron-molybdenum cofactor from Azotobacter vinelandii nitrogenase through sulfur K and molybdenum L X-ray absorption edge studies. J Am Chem Soc 110:3798–3805CrossRefGoogle Scholar
  62. 62.
    Corbett MC, Tezcan FA, Einsle O et al (2005) Mo K- and L-edge X-ray absorption spectroscopic study of the ADP·AlF4 --stabilized nitrogenase complex: comparison with MoFe protein in solution and single crystal. J Synchrotron Radiat 12:28–34PubMedCrossRefGoogle Scholar
  63. 63.
    Venters RA, Nelson MJ, McLean PA et al (1986) ENDOR of the resting state of nitrogenase molybdenum iron proteins from Azotobacter vinelandii, Klebsiella pneumoniae, and Clostridium pasteurianum: 1H, 57Fe, 95Mo, and 33S studies. J Am Chem Soc 108:3487–3498CrossRefGoogle Scholar
  64. 64.
    Lee HI, Hales BJ, Hoffman BM (1997) Metal-ion valencies of the FeMo cofactor in CO-inhibited and resting state nitrogenase by 57Fe Q-band ENDOR. J Am Chem Soc 119:11395–11400CrossRefGoogle Scholar
  65. 65.
    Huynh BH, Munck E, Orme-Johnson WH (1979) Nitrogenase XI: Mössbauer studies on the cofactor centers of the MoFe protein from Azotobacter vinelandii OP. Biochim Biophys Acta 576:192–203PubMedGoogle Scholar
  66. 66.
    Huynh BH, Henzl MT, Christner JA et al (1980) Nitrogenase XII: Mössbauer studies of the MoFe protein from Clostridium pasteurianum W5. Biochim Biophys Acta 623:124–138PubMedGoogle Scholar
  67. 67.
    Johnson MK, Thomson AJ, Robinson AE et al (1981) Characterization of the paramagnetic centers of the molybdenum-iron protein of nitrogenase from Klebsiella pneumoniae using low temperature magnetic circular dichroism spectroscopy. Biochim Biophys Acta 671:61–70Google Scholar
  68. 68.
    Conradson SD, Burgess BK, Holm RH (1988) Fluorine-19 chemical shifts as probes of the structure and reactivity of the iron-molybdenum cofactor of nitrogenase. J Biol Chem 263:13743–13749PubMedGoogle Scholar
  69. 69.
    Lukoyanov D, Barney BM, Dean DR et al (2007) Connecting nitrogenase intermediates with the kinetic scheme for N2 reduction by a relaxation protocol and identification of the N2 binding state. Proc Natl Acad Sci USA 104:1451–1455PubMedCrossRefGoogle Scholar
  70. 70.
    Seefeldt LC, Hoffman BM, Dean DR (2009) Mechanism of Mo-dependent nitrogenase. Annu Rev Biochem 78:701–722PubMedCrossRefGoogle Scholar
  71. 71.
    Vrajmasu V, Munck E, Bominaar EL (2003) Density functional study of the electric hyperfine interactions and the redox-structural correlations in the cofactor of nitrogenase. Analysis of general trends in 57Fe isomer shifts. Inorg Chem 42:5974–5988PubMedCrossRefGoogle Scholar
  72. 72.
    Huniar U, Ahlrichs R, Coucouvanis D (2004) Density functional theory calculations and exploration of a possible mechanism of N2 reduction by nitrogenase. J Am Chem Soc 126:2588–2601PubMedCrossRefGoogle Scholar
  73. 73.
    Dance I (2003) The consequences of an interstitial N atom in the FeMo cofactor of nitrogenase. Chem Commun (3):324–325.Google Scholar
  74. 74.
    Dance I (2006) The correlation of redox potential, HOMO energy, and oxidation state in metal sulfide clusters and its application to determine the redox level of the FeMo-co active-site cluster of nitrogenase. Inorg Chem 45:5084–5091PubMedCrossRefGoogle Scholar
  75. 75.
    Hinnemann B, Nørskov JK (2003) Modeling a central ligand in the nitrogenase FeMo cofactor. J Am Chem Soc 125:1466–1467PubMedCrossRefGoogle Scholar
  76. 76.
    Mayer SM, Niehaus WG, Dean DR (2002) Reduction of short chain alkynes by a nitrogenase α-70Ala-substituted MoFe protein. Dalton Trans 802–807Google Scholar
  77. 77.
    Benton PMC, Mayer SM, Shao JL et al (2001) Interaction of acetylene and cyanide with the resting state of nitrogenase alpha-96-substituted MoFe proteins. Biochemistry 40:13816–13825PubMedCrossRefGoogle Scholar
  78. 78.
    Fisher K, Dilworth MJ, Newton WE (2000) Differential effects on N2 binding and reduction, HD formation, and azide reduction with α-195His- and α191Gln-substituted MoFe proteins of Azotobacter vinelandii nitrogenase. Biochemistry 39:15570–15577PubMedCrossRefGoogle Scholar
  79. 79.
    Barney BM, Yurth MG, Dos Santos PC et al (2009) A substrate channel in the nitrogenase MoFe protein. J Biol Inorg Chem 14:1015–1022PubMedCrossRefGoogle Scholar
  80. 80.
    Barney BM, Lee HI, Dos Santos PC et al (2006) Breaking the N2 triple bond: insights into the nitrogenase mechanism. Dalton Trans 2277–2284Google Scholar
  81. 81.
    Barney BM, McClead J, Lukoyanov D et al (2007) Diazene (HN=NH) is a substrate for nitrogenase: insights into the pathway of N2 reduction. Biochemistry 46:6784–6794PubMedCrossRefGoogle Scholar
  82. 82.
    Hoffman BM, Dean DR, Seefeldt LC (2009) Climbing nitrogenase: toward a mechanism of enzymatic nitrogen fixation. Acc Chem Res 42:609–619PubMedCrossRefGoogle Scholar
  83. 83.
    Barney BM, Lukoyanov D, Igarashi RY et al (2009) Trapping an intermediate of dinitrogen (N2) reduction on nitrogenase. Biochemistry 48:9094–9102PubMedCrossRefGoogle Scholar
  84. 84.
    Yandulov DV, Schrock RR (2003) Catalytic reduction of dinitrogen to ammonia at a single molybdenum center. Science 301:76–78PubMedCrossRefGoogle Scholar
  85. 85.
    Schrock RR (2008) Catalytic reduction of dinitrogen to ammonia by molybdenum: theory versus experiment. Angew Chem Int Edn 47:5512–5522CrossRefGoogle Scholar
  86. 86.
    McLean PA, Dixon RA (1981) Requirement of nifV gene for production of wild-type nitrogenase enzyme in Klebsiella pneumoniae. Nature 292:655–656PubMedCrossRefGoogle Scholar
  87. 87.
    Smith BE, Durrant MC, Fairhurst SA et al (1999) Exploring the reactivity of the isolated iron-molybdenum cofactor of nitrogenase. Coord Chem Rev 185:669–687CrossRefGoogle Scholar
  88. 88.
    Hughes DL, Ibrahim SK, Pickett CJ et al (1994) On carboxylate as a leaving group at the active-site of Mo nitrogenase – electrochemical reactions of some Mo and W carboxylates, formation of mono-hydrides, di-hydrides and tri-hydrides and the detection of an MoH2(N2) intermediate. Polyhedron 13:3341–3348CrossRefGoogle Scholar
  89. 89.
    Durrant MC, Francis A, Lowe DJ et al (2006) Evidence for a dynamic role for homocitrate during nitrogen fixation: the effect of substitution at the α-Lys426 position in MoFe-protein of Azotobacter vinelandii. Biochem J 397:261–270PubMedCrossRefGoogle Scholar
  90. 90.
    Coucouvanis D, Demadis KD, Malinak SM et al (1996) Catalytic and stoichiometric multielectron reduction of hydrazine to ammonia and acetylene to ethylene with clusters that contain the MFe3S4 cores (M = Mo, V). Relevance to the function of nitrogenase. J Mol Catal A: Chem 107:123–135CrossRefGoogle Scholar
  91. 91.
    Demadis KD, Malinak SM, Coucouvanis D (1996) Catalytic reduction of hydrazine to ammonia with MoFe3S4-polycarboxylate clusters. Possible relevance regarding the function of the molybdenum-coordinated homocitrate in nitrogenase. Inorg Chem 35:4038–4046PubMedCrossRefGoogle Scholar
  92. 92.
    Lukoyanov D, Yang ZY, Dean DR et al (2010) Is Mo involved in hydride binding by the four-electron reduced (E4) intermediate of the nitrogenase MoFe protein? J Am Chem Soc 132:2526–2527PubMedCrossRefGoogle Scholar
  93. 93.
    Peters JW, Szilagyi RK (2006) Exploring new frontiers of nitrogenase structure and mechanism. Curr Opin Chem Biol 10:101–108PubMedCrossRefGoogle Scholar
  94. 94.
    Malinak SM, Simeonov AM, Mosier PE et al (1997) Catalytic reduction of cis-dimethyldiazene by the [MoFe3S4]3+ clusters. The four-electron reduction of a N=N bond by a nitrogenase-relevant cluster and implications for the function of nitrogenase. J Am Chem Soc 119:1662–1667CrossRefGoogle Scholar
  95. 95.
    Dance I (2006) Mechanistic significance of the preparatory migration of hydrogen atoms around the FeMo-co active site of nitrogenase. Biochemistry 45:6328–6340PubMedCrossRefGoogle Scholar
  96. 96.
    Dance I (2007) The mechanistically significant coordination chemistry of dinitrogen at FeMo-co, the catalytic site of nitrogenase. J Am Chem Soc 129:1076–1088PubMedCrossRefGoogle Scholar
  97. 97.
    Dance I (2008) 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 (43):5992–5998Google Scholar
  98. 98.
    Hinnemann B, Norskov JK (2006) Catalysis by enzymes: the biological ammonia synthesis. Top Catal 37:55–70CrossRefGoogle Scholar
  99. 99.
    Kästner J, Blöchl PE (2007) Ammonia production at the FeMo cofactor of nitrogenase: results from density functional theory. J Am Chem Soc 129:2998–3006PubMedCrossRefGoogle Scholar
  100. 100.
    McKee ML (2007) Modeling the nitrogenase FeMo cofactor with high-spin Fe8S9X+ (X=N, C) clusters. Is the first step for N2 reduction to NH3 a concerted dihydrogen transfer? J Comput Chem 28:1342–1356PubMedCrossRefGoogle Scholar
  101. 101.
    Frisch MJ, Trucks GW, Schlegel HB et al (2006) Gaussian 03 Rev E.01, Gaussian Inc., Wallingford, CTGoogle Scholar

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© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Department of Chemistry and BiochemistryAstrobiology Biogeochemistry Research Center, Montana State UniversityBozemanUSA

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