The E 2 state of FeMoco: Hydride Formation versus Fe Reduction and a Mechanism for H 2 Evolution.

The iron-molybdenum cofactor (FeMoco) is responsible for dinitrogen reduction in Mo nitrogenase. Unlike the resting state, E ₀ , reduced states of FeMoco are much less well characterized. The E ₂ state has been proposed to contain a hydride but direct spectroscopic evidence is still lacking. The E ₂ state can, however, relax back the E ₀ state via a H ₂ side-reaction, implying a hydride intermediate prior to H ₂ formation. This E ₂ →E ₀ pathway is one of the primary mechanisms for H ₂ formation under low-electron flux conditions. In this study we present an exploration of the energy surface of the E ₂ state. Utilizing both cluster-continuum and QM/MM calculations, we explore various classes of E ₂ 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 ₂ state. These models feature either i) a bridging hydride between Fe ₂ and Fe ₆ and an open sulfide-bridge with terminal SH on Fe ₆ (E ₂ -hyd) or ii) a double belt-sulfide protonated, reduced cofactor without a hydride (E ₂ -nonhyd). We suggest both models as contenders for the E ₂ redox state and further calculate a mechanism for H ₂ evolution. The changes in electronic structure of FeMoco during the proposed redox-state cycle, E ₀ →E ₁ →E ₂ →E ₀ , are discussed.
(© 2021 The Authors. Chemistry - A European Journal published by Wiley-VCH GmbH.)