A model for dinitrogen binding in the E₄ state of nitrogenase

Area of Science:

• Biochemistry and enzymology
• Bioinorganic chemistry
• Computational chemistry

Background:

• Molybdenum nitrogenase is crucial for biological nitrogen fixation.
• The iron-molybdenum-sulfur cofactor (FeMoco) is central to its function.
• The exact structure and mechanism of the N2-binding E4 state remain unknown.

Purpose of the Study:

• To investigate the molecular and electronic structure of the E4 state of molybdenum nitrogenase.
• To propose and evaluate new structural models for the N2-binding E4 state.
• To elucidate the mechanism of N2 binding and activation by the FeMoco cofactor.

Main Methods:

• Theoretical Quantum Mechanics/Molecular Mechanics (QM/MM) calculations.
• Development and comparison of new structural models for the E4 state.
• Analysis of electronic structure, binding energies, and reaction pathways.

Main Results:

• Two novel structural models for the E4 state are proposed, featuring bridging hydrides and specific iron coordination.
• These models are energetically favorable and consistent with experimental data (ENDOR).
• Dinitrogen (N2) binds exothermically to Fe2 or Fe6 in the proposed models, facilitated by a low-spin Fe site and unique ligand field.

Conclusions:

• The proposed models provide a plausible structural basis for the E4 state of molybdenum nitrogenase.
• Reductive elimination and subsequent protonation steps are suggested as key for N2 activation.
• The Fe6-bound model appears more favorable for N2 stabilization and activation, potentially involving the apical heterometal ion.