Survey of the Geometric and Electronic Structures of the Key Hydrogenated Forms of FeMo-co, the Active Site of the Enzyme Nitrogenase: Principles of the Mechanistically Significant Coordination Chemistry

Abstract

The enzyme nitrogenase naturally hydrogenates N2 to NH3, achieved through the accumulation of H atoms on FeMo-co, the Fe7MoS9C(homocitrate) cluster that is the catalytically active site. Four intermediates, E1H1, E2H2, E3H3, and E4H4, carry these hydrogen atoms. I report density functional calculations of the numerous possibilities for the geometric and electronic structures of these poly-hydrogenated forms of FeMo-co. This survey involves more than 100 structures, including those with bound H2, and assesses their relative energies and most likely electronic states. Twelve locations for bound H atoms in the active domain of FeMo-co, including Fe–H–Fe and Fe–H–S bridges, are studied. A significant result is that transverse Fe–H–Fe bridges (transverse to the pseudo-threefold axis of FeMo-co and shared with triply-bridging S) are not possible geometrically unless the S is hydrogenated to become doubly-bridging. The favourable Fe–H–Fe bridges are shared with doubly-bridging S. ENDOR data for an E4H4 intermediate trapped at low temperature, and interpretations in terms of the geometrical and electronic structure of E4H4, are assessed in conjunction with the calculated possibilities. The results reported here yield a set of 24 principles for the mechanistically significant coordination chemistry of H and H2 on FeMo-co, in the stages prior to N2 binding.

N2H2 binding to the nitrogenase FeMo cluster studied by QM/MM methods

“…It can be seen that the relative energies change quite extensively (by up to 70 kJ/mol, both increasing or decreasing the relative stability), but the correlation between the two data sets is quite good, R = 0.89. In particular, Fe2(trans) remains the most stable complex and it is stabilised compared to the other low-energy complex, 23,29,86,63,85,34 and 91 kJ/ mol more stable than Fe6(HNNH 2 ), Fe6(trans), Fe2(cis), Fe4(trans), Fe3/7Fe4/5, Fe6(cis) and Fe6 complexes. Thus, the Fe6(cis) complex becomes the fourth best structure.…”

“…Some groups suggest that N 2 binds instead to the central carbide ion [17,18]. There is not even any agreement regarding the structure of E 4 or where protons are added beyond the E 1 state [16,20,23,25,34].…”

“…As discussed before [23,34], this is a formidable task: There are more than 50 possible positions where protons can bind to the FeMo cluster. This gives more than 6 million structures of the E 4 state (50 4 ) and for each there are at least 35 possible broken-symmetry states.…”

Computational Investigations of the Chemical Mechanism of the Enzyme Nitrogenase

“…The DMol procedure is more straightforward, because the signs and starting magnitudes of atomic spin densities can be input (via the Start_Spin_Populations keyword) prior to scf convergence, and the spins of all metal atoms are allowed to adjust without constraint. This also allows electronic states to change during an energy minimisation calculation …”

“…I surveyed more than 100 structures that contain one, two, three or four H atoms bonded to FeMo‐co . It was not necessary to test all possible electronic and total spin states for each structure, because it became evident during the optimisations that a small number of electronic states (BS7‐1, BS7‐2, BS7‐3, BS10‐3, BS10‐6, BS6‐2, BS2) are generally more stable.…”