Deciphering the origin of million-fold reactivity observed for the open core diiron [HO–Fe III –O– Fe IV ]O] 2+ species towards C–H bond activation: role of spin-states, spin-coupling, and spin- cooperation† Mursaleem Ansari, a Dhurairajan Senthilnathan * b and Gopalan Rajaraman * a High-valent metal–oxo species have been characterised as key intermediates in both heme and non-heme enzymes that are found to perform efficient aliphatic hydroxylation, epoxidation, halogenation, and dehydrogenation reactions. Several biomimetic model complexes have been synthesised over the years to mimic both the structure and function of metalloenzymes. The diamond-core [Fe 2 (m-O) 2 ] is one of the celebrated models in this context as this has been proposed as the catalytically active species in soluble methane monooxygenase enzymes (sMMO), which perform the challenging chemical conversion of methane to methanol at ease. In this context, a report of open core [HO(L)Fe III –O–Fe IV (O)(L)] 2+ (1) gains attention as this activates C–H bonds a million-fold faster compared to the diamond-core structure and has the dual catalytic ability to perform hydroxylation as well as desaturation with organic substrates. In this study, we have employed density functional methods to probe the origin of the very high reactivity observed for this complex and also to shed light on how this complex performs efficient hydroxylation and desaturation of alkanes. By modelling fifteen possible spin-states for 1 that could potentially participate in the reaction mechanism, our calculations reveal a doublet ground state for 1 arising from antiferromagnetic coupling between the quartet Fe IV centre and the sextet Fe III centre, which regulates the reactivity of this species. The unusual stabilisation of the high-spin ground state for Fe IV ]O is due to the strong overlap of Fe IV s * z 2 with the Fe III p * xz orbital, reducing the antibonding interactions via spin-cooperation. The electronic structure features computed for 1 are consistent with experiments offering confidence in the methodology chosen. Further, we have probed various mechanistic pathways for the C–H bond activation as well as –OH rebound/desaturation of alkanes. An extremely small barrier height computed for the first hydrogen atom abstraction by the terminal Fe IV ]O unit was found to be responsible for the million-fold activation observed in the experiments. The barrier height computed for –OH rebound by the Fe III –OH unit is also smaller suggesting a facile hydroxylation of organic substrates by 1. A strong spin-cooperation between the two iron centres also reduces the barrier for second hydrogen atom abstraction, thus making the desaturation pathway competitive. Both the spin-state as well as spin-coupling between the two metal centres play a crucial role in dictating the reactivity for species 1. By exploring various mechanistic pathways, our study unveils the fact that the bridged m-oxo group is a poor electrophile for both C–H activation as well for –OH rebound. As more and more evidence is gathered in recent years for the open core geometry of sMMO enzymes, the idea of enhancing the reactivity via an open-core motif has far-reaching consequences. Introduction High-valent metal–oxo complexes are of great interest due to their potent catalytic abilities. 1–25 Dinuclear metal–oxo complexes have different types of metal centres, but iron is the most common metal centre to oxidise C–H bonds through the dioxygen activation mechanism, in which high-valent oxo–iron species are oen postulated and demonstrated to act as the actual oxidising species. 26–33 Membrane-bound methane a Department of Chemistry, Indian Institute of Technology Bombay, Mumbai 400076, India. E-mail: rajaraman@chem.iitb.ac.in b Center for Computational Chemistry, CRD, PRIST University, Vallam, Thanjavur, Tamilnadu 613403, India † Electronic supplementary information (ESI) available. See DOI: 10.1039/d0sc02624g Cite this: DOI: 10.1039/d0sc02624g All publication charges for this article have been paid for by the Royal Society of Chemistry Received 8th May 2020 Accepted 16th June 2020 DOI: 10.1039/d0sc02624g rsc.li/chemical-science This journal is © The Royal Society of Chemistry 2020 Chem. Sci. Chemical Science EDGE ARTICLE Open Access Article. Published on 18 June 2020. Downloaded on 9/17/2020 10:19:12 AM. This article is licensed under a Creative Commons Attribution-NonCommercial 3.0 Unported Licence. View Article Online View Journal