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Isolation of a Ru(iv) side-on peroxo intermediate in the water oxidation reaction

Abstract

The electrons that nature uses to reduce CO2 during photosynthesis come from water oxidation at the oxygen-evolving complex of photosystem II. Molecular catalysts have served as models to understand its mechanism, in particular the O–O bond-forming reaction, which is still not fully understood. Here we report a Ru(iv) side-on peroxo complex that serves as a ‘missing link’ for the species that form after the rate-determining O–O bond-forming step. The Ru(iv) side-on peroxo complex (η2-1iv–OO) is generated from the isolated Ru(iv) oxo complex (1iv=O) in the presence of an excess of oxidant. The oxidation (iv) and spin state (singlet) of η2-1iv–OO were determined by a combination of experimental and theoretical studies. 18O- and 2H-labelling studies evidence the direct evolution of O2 through the nucleophilic attack of a H2O molecule on the highly electrophilic metal–oxo species via the formation of η2-1iv–OO. These studies demonstrate water nucleophilic attack as a viable mechanism for O–O bond formation, as previously proposed based on indirect evidence.

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Fig. 1: O–O bond-forming mechanisms.
Fig. 2: Summary of the synthesis and spectroscopic characterization of a closed-shell Ru(iv) side-on peroxo intermediate (η2-1iv–OO).
Fig. 3: CSI-HRMS isotopic labelling experiments evidencing the WNA mechanism.
Fig. 4: Summary of the reactivity of the Ru intermediates in relation to the WO catalytic cycle.

Data availability

The crystallographic data for η2-[Ruiv(OO)(Py2Metacn)](PF6)1.5(IO3)0.5, η2-[Ruiv(OO)(Py2Metacn)](PF6)2 and 1iv=O have been deposited with the Cambridge Crystallographic Data Centre under accession numbers 1944703, 1944703 and 1944705, respectively. The data supporting the findings of the current study are available within the paper and its Supplementary Information.

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Acknowledgements

We thank the ICIQ Foundation, MEC for PhD grants FPU14/02550 (C.C.) and FPU16/04234 (S.F.), and for the AP2Chem project (Ref: PID2019-110050RB-I00), the European Research Foundation for project FP7-PEOPLE-2010-ERG-268445 (J.L.-F.) and the CELLEX Foundation through the CELLEX-ICIQ high-throughput experimentation platform, the Netherlands Ministry of Education, Culture and Science (Gravity Program 024.001.035, W.R.B.) for financial support. We acknowledge Catexel for the generous gift of 1,4,7-tritosyl-1,4,7-triazacyclononane (Ts3tacn). We acknowledge the LUCIA Beamline staff at SOLEIL synchrotron where the XAS data was collected (V.M.-D.).

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Authors

Contributions

J.L.-F. and C.C. directed and conceived this project. C.C. synthesized all the intermediates, performed most of the experimental work, the DFT studies, the kinetic model and wrote the draft of the manuscript. V.M.-D., C.C., F.F. and B.L.-K. performed the synchrotron measurements and V.M.-D. analysed the data. W.R.B. and C.C. performed the Raman measurements and the analyses. V.M.-D. and C.C. performed the electron spin resonance experiments. S.F. performed the studies to calculate the activation parameters. C.C. and F.F. performed the electrochemical studies. N.C. optimized the experimental parameters of CSI-HRMS and, together with C.C., performed the CSI-HRMS studies and analysed the data. J.B.-B. performed the crystallographic analyses of the isolated intermediates. All the authors discussed the results and contributed to the manuscript.

Corresponding author

Correspondence to Julio Lloret-Fillol.

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The authors declare no competing interests.

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Peer review information Nature Chemistry thanks the anonymous reviewers for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–89, Schemes 1–3, Tables 1–15, discussion and references.

Supplementary Data 1

DFT cartesian coordinates for all calculated geometries, DFT optimized structures 1−46.

Supplementary Data 2

Crystallographic data for η2-[Ruiv(OO)(Py2Metacn)](PF6)1.5(IO3)0.5 CCDC reference 1944703.

Supplementary Data 3

Crystallographic data for η2-1iv–OO CCDC reference 1944704.

Supplementary Data 4

Crystallographic data for 1iv=O CCDC reference 1944705.

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Casadevall, C., Martin-Diaconescu, V., Browne, W.R. et al. Isolation of a Ru(iv) side-on peroxo intermediate in the water oxidation reaction. Nat. Chem. 13, 800–804 (2021). https://doi.org/10.1038/s41557-021-00702-5

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