Hey ho, where'd the proton go? Final deprotonation of O6 within the S3 state of photosystem II.

The deprotonation of O6 within the S3 state marks the final deprotonation event before the formation of oxygen­oxygen bond interactions and eventual production and release of dioxygen. Gaining a thorough understanding of this event, from the proton acceptors involved, to the exfiltration pathways available, is key in determining the nature of the resulting oxygen species, influencing the mechanism through which the first oxygen­oxygen bond forms. Computational analysis, using BS-DFT methodologies, showed that proton abstraction by the local Glu189 residue provides consistent evidence against this being a viable mechanistic pathway due to the lack of a stable product structure. In contrast, abstraction via W3 shows an increasingly stable oxo-oxo product state between r[O5O6] = 2.1 Å & 1.9 Å. The resulting oxo-oxo state is stabilised through donation of ß electron character from O6 to Mn1 and α electron character from O6 to O5. This donation from the O6 lone pair is shown to be a key factor in stabilising the oxo-oxo state, in addition to showing the initiation of first O5-O6 bond.

A Reappraisal of the S2 State of Nature's Water Oxidizing Complex in Its Low and High Spin Forms.

Density functional theory calculated 14N hyperfine couplings are obtained for the Mn1 ligated π-N of residue His332 of the photosystem 2 water oxidizing complex. An open cubane, O4H, model closely matches the experimental coupling obtained for the high spin S = 5/2 form of the S2 state, supporting an open cubane structure for this state. We also investigate the unusual geometric features for the S2 state obtained by X-ray free electron laser structure determinations and rationalize it as an equilibrium occurring at room temperature between W1/O4 deprotonated and protonated forms of the open cubane structure.

Insights into PSII's S3YZ• State: An Electronic and Magnetic Analysis.

Using BS-DFT (broken-symmetry density functional theory), the electronic and magnetic properties of the S3YZ• state of photosystem II were investigated and compared to those of the S3 state. While the O5 oxo-O6 hydroxo species presents little difference between the two states, a previously identified [O5O6]3- exhibits reduced stabilization of the O5-O6 shared spin. This species is shown to have some coupling with the YZ• center through Mn1 and O6. Similarly, a peroxo species is found to exhibit significant exchange couplings between the YZ• center and the Mn cluster through Mn1. Mechanistic changes in O-O bond formation in S3YZ• are highlighted by analysis of IBOs (intrinsic bonding orbitals) showing deviation for Mn1 and O6 centered IBOs. This change in coupling interactions throughout the complex as a result of S3YZ• formation presents implications for the determination of the mechanism spanning the end of the S3 and the start of the S4 states, affecting both electron movement and oxygen bond formation.

Computational Study on the Influence of Mo/V Centers on the Electronic Structure and Hydrazine Reduction Capability of [MFe3S4]3+/2+ Complexes.

[MFe3S4] cubanes have for some time been of interest for their ability to mimic the electronic and geometric structure of the active site of nitrogenase, the enzyme responsible for fixing N2 to NH3. Nitrogenase naturally occurs in three forms, with the major difference being that the metal ion present in the cofactor active site is either molybdenum (FeMoco), vanadium (FeVco), or iron. The molybdenum and vanadium versions of these cofactors are more closely studied, owing to their larger abundance and rate of catalysis. In this study, we compare free energy profiles and electronic properties of the Mo/V cubanes at various stages during the reduction of N2H4 to NH3. Our findings highlight the differences in how the complexes facilitate the reaction, in particular, vanadium's comparatively weaker ability to interact with the Fe/S network and stabilize reducing electrons prior to N-N bond cleavage, which may have implications when considering the lower efficiency of the vanadium-dependent nitrogenase.

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.