FeMo cofactor of nitrogenase: a density functional study of states M(N), M(OX), M(R), and M(I).

The M(N) S = (3)/(2) resting state of the FeMo cofactor of nitrogenase has been proposed to have metal-ion valencies of either Mo(4+)6Fe(2+)Fe(3+) (derived from metal hyperfine interactions) or Mo(4+)4Fe(2+)3Fe(3+) (from Mössbauer isomer shifts). Spin-polarized broken-symmetry (BS) density functional theory (DFT) calculations have been undertaken to determine which oxidation level best represents the M(N) state and to provide a framework for understanding its energetics and spectroscopy. For the Mo(4+)6Fe(2+)Fe(3+) oxidation state, the spin coupling pattern for several spin state alignments compatible with S = (3)/(2) were generated and assessed by energy and geometric criteria. The most likely BS spin state is composed of a Mo3Fe cluster with spin S(a) = 2 antiferromagnetically coupled to a 4Fe' cluster with spin S(b) = (7)/(2). This state has a low DFT energy for the isolated FeMoco cluster and the lowest energy when the interaction with the protein and solvent environment is included. This spin state also displays calculated metal hyperfine and Mössbauer isomer shifts compatible with experiment, and optimized geometries that are in excellent agreement with the protein X-ray data. Our best model for the actual spin-coupled state within FeMoco alters this BS state by a slight canting of spins and is analogous in several respects to that found in the 8Fe P-cluster in the same protein. The spin-up and spin-down components of the LUMO contain atomic contributions from Mo(4+) and the homocitrate and from the central prismane Fe sites and muS(2) atoms, respectively. This qualitative picture of the accepting orbitals for M(N) is consistent with observations from Mössbauer spectra of the one-electron reduced states. Similar calculations for the Mo(4+)4Fe(2+)3Fe(3+) oxidation state yield results that are in poorer agreement with experiment. Using the Mo(4+)6Fe(2+)Fe(3+) oxidation level as the most plausible resting state, the geometric, electronic and energetic properties of the one-electron redox transition to the oxidized state, M(OX), catalytically observed M(R) and radiolytically reduced M(I) states have also been explored.