Effect of H₂ Binding on the Nonadiabatic Transition Probability between Singlet and Triplet States of the [NiFe]-Hydrogenase Active Site

Abstract

We investigate the effect of H2 binding on the spin-forbidden nonadiabatic transition probability between the lowest energy singlet and triplet electronic states of [NiFe]-hydrogenase active site model, using a velocity averaged Landau-Zener theory. Density functional and multireference perturbation theories were used to provide parameters for the Landau-Zener calculations. It was found that variation of the torsion angle between the terminal thiolate ligands around the Ni center induces an intersystem crossing between the lowest energy singlet and triplet electronic states in the bare active site and in the active site with bound H2. Potential energy curves between the singlet and triplet minima along the torsion angle and H2 binding energies to the two spin states were calculated. Upon H2 binding to the active site, there is a decrease in the torsion angle at the minimum energy crossing point between the singlet and triplet states. The probability of nonadiabatic transitions at temperatures between 270 and 370 K ranges from 35% to 32% for the active site with bound H2 and from 42% to 38% for the bare active site, thus indicating the importance of spin-forbidden nonadiabatic pathways for H2 binding on the [NiFe]-hydrogenase active site.

Hydrogenase Enzymes and Their Synthetic Models: The Role of Metal Hydrides

“…Yet the consensus is that while both metals may participate, Ni does the bulk of the work, not only because it is optimally positioned near the end of a hydrophobic H 2 transport channel, 324 but also because its unusual geometry is particularly reactive, as indicated by DFT calculations. 310,325 Recent work has suggested that the orientation of Cys ligands has a strong influence on spin densities at Ni and S. 326,327 Furthermore, several computational studies on truncated active sites indicate that rotation of terminal Cys modulates the relative stability of low- and high-spin Ni, 310,328,329 although the protein environment may also have nontrivial effects on Ni electronic structure. 325,330 In the case of a Ni(II)Fe(II) core such as that in Ni-SI a , one would expect square-planar and tetrahedral Ni to give rise to S = 0 and 1 states, respectively.…”

Nonadiabatic transition state theory: Application to intersystem crossings in the active sites of metal‐sulfur proteins

“…The mechanisms of these reactions are not completely understood . Our previous studies show that both the lowest energy singlet and triplet states could be important for the reactivity of the [NiFe]‐hydrogenase active site, and therefore, for understanding the catalytic behavior of this system . A model of the active form, Ni‐SI a , of the [NiFe]‐hydrogenase active site was constructed by replacing the cysteine ligands with SCH 3 groups (Fig.…”

“…Not surprisingly, the differences between the singlet and triplet states geometries are mostly due to the different values of the torsion angle α between planes p 1 (S1‐Ni‐S2) and p 2 (S3‐Ni‐S4). Thus, this angle can be used as a reasonable approximation to the reaction coordinate connecting the equilibrium geometries of the singlet and triplet states . The singlet and triplet state energies for the geometries interpolated between the equilibrium structures of the two spin states are shown in Figure b.…”

“…The magnetic properties of transition metal complexes and materials can be controlled by light, temperature, and pressure by initiating spin‐crossover transitions between the low‐spin and high‐spin states . Among many examples of processes where intersystem crossings play a central role are combustion, reactions in the atmosphere and in interstellar space, transition metal‐based catalysis, and binding of small molecules to the active sites of metalloproteins . Intersystem crossing has applications in photodynamic therapy, free‐radical polymerization reactions, organic‐light emitting diodes, and metal–organic frameworks .…”

Theoretical investigations of spin‐orbit coupling and intersystem crossing in reaction carbon dioxide activated by [Re(CO)2]+

“…The weighted average with statistical concepts based on the Landau‐Zener (LZ) model was introduced to evaluate the ISC probabilities at the MECP, which is defined as Equation . The LZ probability for the mass‐weighted component of the nuclear velocity perpendicular to the crossing seam and the Maxwell‐Boltzman velocity distribution, as is shown in Equations and . For kinetics of nonadiabatic spin‐forbidden reaction, we roughly estimated the rate constant based on the transition state theory Equation .…”