Mechanism of Nitrogen Reduction to Ammonia in a Diiron Model of Nitrogenase

Nitrogenase is a
fascinating enzyme in biology that reduces dinitrogen
from air to ammonia through stepwise reduction and protonation. Despite
it being studied in detail by experimental and computational groups,
there are still many unknown factors in the catalytic cycle of nitrogenase,
especially related to the addition of protons and electrons and their
order. A recent biomimetic study characterized a potential dinitrogen-bridged
diiron cluster as a synthetic model of nitrogenase. Using strong acid
and reductants, the dinitrogen was converted into ammonia molecules,
but details of the mechanism remains unknown. In particular, it was
unclear from the experimental studies whether the proton and electron
transfer steps are sequential or alternating. Moreover, the work failed
to establish what the function of the diiron core is and whether it
split into mononuclear iron fragments during the reaction. To understand
the structure and reactivity of the biomimetic dinitrogen-bridged
diiron complex [(P2P′PhFeH)2(μ-N2)] with triphenylphosphine ligands, we performed
a density functional theory study. Our computational methods were
validated against experimental crystal structure coordinates, Mössbauer
parameters, and vibrational frequencies and show excellent agreement.
Subsequently, we investigated the alternating and consecutive addition
of electrons and protons to the system. The calculations identify
a number of possible reaction channels, namely, same-site protonation,
alternating protonation, and complex dissociation into mononuclear
iron centers. The calculations show that the overall mechanism is
not a pure sequential set of electron and proton transfers but a mixture
of alternating and consecutive steps. In particular, the first reaction
steps will start with double proton transfer followed by an electron
transfer, while thereafter, there is another proton transfer and a
second electron transfer to give a complex whereby ammonia can split
off with a low energetic barrier. The second channel starts with alternating
protonation of the two nitrogen atoms, whereafter the initial double
proton transfer, electrons and protons are added sequentially to form
a hydrazine-bound complex. The latter split off ammonia spontaneously
after further protonation. The various reaction channels are analyzed
with valence bond and orbital diagrams. We anticipate the nitrogenase
enzyme to operate with mixed alternating and consecutive protonation
and electron transfer steps.