The E state of FeMoco: Hydride Formation versus Fe Reduction and a Mechanism for H Evolution.

The iron-molybdenum cofactor (FeMoco) is responsible for dinitrogen reduction in Mo nitrogenase. Unlike the resting state, E , reduced states of FeMoco are much less well characterized. The E state has been proposed to contain a hydride but direct spectroscopic evidence is still lacking. The E state can, however, relax back the E state via a H side-reaction, implying a hydride intermediate prior to H formation. This E →E pathway is one of the primary mechanisms for H formation under low-electron flux conditions. In this study we present an exploration of the energy surface of the E state. Utilizing both cluster-continuum and QM/MM calculations, we explore various classes of E models: including terminal hydrides, bridging hydrides with a closed or open sulfide-bridge, as well as models without. Importantly, we find the hemilability of a protonated belt-sulfide to strongly influence the stability of hydrides. Surprisingly, non-hydride models are found to be almost equally favorable as hydride models. While the cluster-continuum calculations suggest multiple possibilities, QM/MM suggests only two models as contenders for the E state. These models feature either i) a bridging hydride between Fe and Fe and an open sulfide-bridge with terminal SH on Fe (E -hyd) or ii) a double belt-sulfide protonated, reduced cofactor without a hydride (E -nonhyd). We suggest both models as contenders for the E redox state and further calculate a mechanism for H evolution. The changes in electronic structure of FeMoco during the proposed redox-state cycle, E →E →E →E , are discussed.