Structural, Spectroscopic, and Redox Consequences of a Central Ligand in the FeMoco of Nitrogenase:  A Density Functional Theoretical Study

Abstract

Broken symmetry density functional and electrostatics calculations have been used to shed light on which of three proposed atoms, C, N, or O, is most likely to be present in the center of the FeMoco, the active site of nitrogenase. At the Mo(4+)4Fe(2+)3Fe(3+) oxidation level, a central N(3-) anion results in (1) calculated Fe-N bond distances that are in very good agreement with the recent high-resolution X-ray data of Einsle et al.; (2) a calculated redox potential of 0.19 eV versus the standard hydrogen electrode (SHE) for FeMoco(oxidized) + e(-) --> FeMoco(resting), in good agreement with the measured value of -0.042 V in Azotobacter vinelandii; and (3) average Mössbauer isomer shift values (IS(av) = 0.48 mm s(-1)) compatible with experiment (IS(av) = 0.40 mm s(-1)). At the more reduced Mo(4+)6Fe(2+)1Fe(3+) level, the calculated geometry around a central N(3-) anion still correlates well with the X-ray data, but the average Mössbauer isomer shift value (IS(av) = 0.54 mm s(-1)) and the redox potential of -2.21 eV show a much poorer agreement with experiment. These calculated structural, spectroscopic, and redox data indicate the most likely iron oxidation state for the resting FeMoco of nitrogenase to be 4Fe(2+)3Fe(3+). At this favored oxidation state, oxygen or carbon coordination leads to (1) Fe-O distances in poor agreement and Fe-C distances in good agreement with experiment and (2) calculated redox potentials of +0.97 eV for O(2-) and -1.31 eV for C(4-). The calculated structural parameters and/or redox data suggest either O(2-) or C(4-) is unlikely as a central anion.

How many metals does it take to fix N 2 ? A mechanistic overview of biological nitrogen fixation

“…Subsequently, density functional and other studies have been reported (34,(46)(47)(48) incorporating the three alternative light elements, to model the electronic, magnetic, and chemical redox properties of the FeMo cofactor. These studies have found a preference order N Ͼ C Ͼ O; although not proving the element, it is suggestive of nitrogen as the core atom.…”

“…For clusters that are electronically complex, multielemental, and redundant of atom type, one component may be masked by unrecognized properties of the system or measurement process, as we found for the core atom in the first place. For example, in the density functional analysis of Lovell et al (47), the core atom is found to have little spin density (Ϫ0.02 of an electron), which would make these spectroscopic features difficult to observe. We would be less restrained and more convinced by the ENDOR͞ESEEM results if a positive control were available showing that model compounds, containing an interstitial nitrogen atom spin-coupled as for the cofactor, had signature 14 N ESEEM͞ENDOR resonances that are missing in the cofactor spectrum.…”

QM/MM Study of the Nitrogenase MoFe Protein Resting State: Broken-Symmetry States, Protonation States, and QM Region Convergence in the FeMoco Active Site

“…Noodleman and coworkers mainly used small models in their pioneering studies 8,9,10,11 but discussed the effect of the protein environment in a later study 12 . Studies by Norskov 13,14,15,16 , Blöchl 17,18 , Kästner 19 , Szilagyi 20 , Dance 21,22 and McKee 23 have used minimal cofactor models.…”

Density Functional Theory in Transition-Metal Chemistry: Relative Energies of Low-Lying States of Iron Compounds and the Effect of Spatial Symmetry Breaking

“…23 A large literature has developed on this and related broken-symmetry approaches. [24][25][26][27][28][29][30][31][32][33] Broken-symmetry solutions have also been studied in other contexts, and it has often been found that it is important to allow the orbitals to break symmetry in order to get a qualitatively correct description of the system. [33][34][35][36][37][38][39][40][41][42] The energies of the broken-symmetry states are often used without correcting for their spin character.…”