Critical Roles of Exchange and Superexchange Interactions in Dictating Electron Transfer and Reactivity in Metalloenzymes

Abstract

Electron transfer (ET) is a fundamental process in transition-metaldependent metalloenzymes. In these enzymes, the spin−spin interactions within the same metal center and/or between different metal sites can play a pivotal role in the catalytic cycle and reactivity. This Perspective highlights that the exchange and/or superexchange interactions can intrinsically modulate the inner-sphere and long-range electron transfer, thus controlling the mechanism and activity of metalloenzymes. For mixed-valence diiron oxygenases, the spin-regulated inner-sphere ET can be dictated by exchange interactions, leading to efficient O−O bond activations. Likewise, the spin-regulated inner-sphere ET can be enhanced by both exchange and superexchange interactions in [Fe4S4]-dependent SAM enzymes, which enable the efficient cleavage of the SC(γ) or SC5′ bond of SAM. In addition to inner-sphere ET, superexchange interactions may modulate the long-range ET between metalloenzymes. We anticipate that the exchange and superexchange enhanced reactivity could be applicable in other important metalloenzymes, such as Photosystem II and nitrogenases.

QM/MM Simulations for the Broken-Symmetry Catalytic Reaction Mechanism of Human Arginase I

“…The two electrons localized at the Mn 2+ ions are coupled by superexchange antiferromagnetically. A previous report 38 showed that exchange and superexchange interactions can dictate the catalytic mechanism and activity of metalloenzymes by influencing the electron transfer in the catalytic site. In metalloenzymes, exchange and superexchange interactions are important for the stabilization of the catalytic site.…”

Spin-Gated Selectivity of the Water Oxidation Reaction Mediated by Free Pentameric CaxMn5–xO5+ Clusters

“…The demonstrated ability to synthesize and control a series of complex clusters with variable stoichiometries and to probe their reactivitiesin particular water oxidation and O–O couplingunder reaction conditions that allow detailed comparisons with systematic first-principles simulations of the reaction pathways provides the impetus for further experimental and theoretical explorations using the hierarchical synthetic modeling strategy developed in this series of investigations. The uncovering of the subtle interplay between reactive pathways evolving on neighboring spin-isomeric potential-energy landscapes, belonging to ferromagnetically ordered majority spin manifolds, and of spin-gated selective processes steered by spin-conserving selection rules is expected to guide future probing of the OEC, as well as further development of catalysts for oxygen evolution reactions with an added emphasis on the role of spin, doping by magnetic atoms, magnetic ordering, synergetic spin and charge-transfer processes, and magnetic-field effects on such reactions. − ,, …”

“…The uncovering of the subtle interplay between reactive pathways evolving on neighboring spin-isomeric potential-energy landscapes, belonging to ferromagnetically ordered majority spin manifolds, and of spin-gated selective processes steered by spin-conserving selection rules 11 is expected to guide future probing of the OEC, as well as further development of catalysts for oxygen evolution reactions with an added emphasis on the role of spin, doping by magnetic atoms, magnetic ordering, synergetic spin and charge-transfer processes, and magnetic-field effects on such reactions. [5][6][7][8][9][10]13,36 ■ ASSOCIATED CONTENT…”

“…In particular, the coexistence of a high spin isomer in the S 2 stage of the cycle appears to be mandatory for subsequent O–O bond formation . Even though spin alignment has been suggested to play an important role in the O–O bond formation process, − current information and comprehensive understanding of mechanistic aspects and kinetic consequences of such spin changes are rather tenuous and incomplete. , …”

“…4 Even though spin alignment has been suggested to play an important role in the O−O bond formation process, 5−8 current information and comprehensive understanding of mechanistic aspects and kinetic consequences of such spin changes are rather tenuous and incomplete. 5,6 The importance of spin selectivity is currently gaining growing research interest, particularly in the context of explorations targeting electrochemical water oxidation reactions, 6−9 as well as in studies of spin selection in catalyzed CO oxidation. 10 Based on such studies, a ligated CaMn 4 O 5 cofactor cluster model of the S 4 state has been recently employed in theoretical modeling, which shows that O−O formation is possible with accessible energy barriers when the cluster is in an optimal ferromagnetic state, which is conserved 11,12 throughout the reaction, 13 thus suggesting an alternative to the mechanism based on a ferrimagnetic S3 state offered in ref 14.…”