Skip to main content

Thank you for visiting You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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


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.

This is a preview of subscription content

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

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.


  1. 1.

    Cox, N., Pantazis, D. A., Neese, F. & Lubitz, W. Biological water oxidation. Acc. Chem. Res. 46, 1588–1596 (2013).

    CAS  Article  Google Scholar 

  2. 2.

    Lubitz, W., Chrysina, M. & Cox, N. Water oxidation in photosystem II. Photosynth. Res. 142, 105–125 (2019).

    CAS  Article  Google Scholar 

  3. 3.

    Field, C. B., Behrenfeld, M. J., Randerson, J. T. & Falkowski, P. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237–240 (1998).

    CAS  Article  Google Scholar 

  4. 4.

    Lewis, N. S. Research opportunities to advance solar energy utilization. Science 351, aad1920 (2016).

    Article  Google Scholar 

  5. 5.

    Gersten, S. W., Samuels, G. J. & Meyer, T. J. Catalytic oxidation of water by an oxo-bridged ruthenium dimer. J. Am. Chem. Soc. 104, 4029–4030 (1982).

    CAS  Article  Google Scholar 

  6. 6.

    Zhang, B. & Sun, L. Artificial photosynthesis: opportunities and challenges of molecular catalysts. Chem. Soc. Rev. 48, 2216–2264 (2019).

    CAS  Article  Google Scholar 

  7. 7.

    Karkas, M. D., Verho, O., Johnston, E. V. & Akermark, B. Artificial photosynthesis: molecular systems for catalytic water oxidation. Chem. Rev. 114, 11863–12001 (2014).

    Article  Google Scholar 

  8. 8.

    Sartorel, A. et al. Polyoxometalate embedding of a tetraruthenium(iv)-oxo-core by template-directed metalation of [γ-SiW10O36]8−: a totally inorganic oxygen-evolving catalyst. J. Am. Chem. Soc. 130, 5006–5007 (2008).

    CAS  Article  Google Scholar 

  9. 9.

    Pantazis, D. A. Missing pieces in the puzzle of biological water oxidation. ACS Catal. 8, 9477–9507 (2018).

    CAS  Article  Google Scholar 

  10. 10.

    Blakemore, J. D., Crabtree, R. H. & Brudvig, G. W. Molecular catalysts for water oxidation. Chem. Rev. 115, 12974–13005 (2015).

    CAS  Article  Google Scholar 

  11. 11.

    Lloret-Fillol, J. & Costas, M. in Advances in Organometallic Chemistry Vol. 71 (ed. Pérez, P. J.) 1–52 (Academic, 2019).

  12. 12.

    Fukuzumi, S., Lee, Y.-M. & Nam, W. Kinetics and mechanisms of catalytic water oxidation. Dalton Trans. 48, 779–798 (2019).

    CAS  Article  Google Scholar 

  13. 13.

    Shaffer, D. W., Xie, Y. & Concepcion, J. J. O–O bond formation in ruthenium-catalyzed water oxidation: single-site nucleophilic attack vs. O–O radical coupling. Chem. Soc. Rev. 46, 6170–6193 (2017).

    CAS  Article  Google Scholar 

  14. 14.

    Gamba, I., Codolà, Z., Lloret-Fillol, J. & Costas, M. Making and breaking of the OO bond at iron complexes. Coord. Chem. Rev. 334, 2–24 (2017).

    CAS  Article  Google Scholar 

  15. 15.

    Wasylenko, D. J. et al. Electronic modification of the [Ruii(tpy)(bpy)(OH2)]2+ scaffold: effects on catalytic water oxidation. J. Am. Chem. Soc. 132, 16094–16106 (2010).

    CAS  Article  Google Scholar 

  16. 16.

    Concepcion, J. J., Tsai, M. K., Muckerman, J. T. & Meyer, T. J. Mechanism of water oxidation by single-site ruthenium complex catalysts. J. Am. Chem. Soc. 132, 1545–1557 (2010).

    CAS  Article  Google Scholar 

  17. 17.

    Kang, R., Yao, J., Chen, H. & Are, D. F. T. Methods accurate in mononuclear ruthenium-catalyzed water oxidation? An ab initio assessment. J. Chem. Theory Comput. 9, 1872–1879 (2013).

    CAS  Article  Google Scholar 

  18. 18.

    Duffy, E. M., Marsh, B. M., Voss, J. M. & Garand, E. Characterization of the oxygen binding motif in a ruthenium water oxidation catalyst by vibrational spectroscopy. Angew. Chem. Int. Ed. 55, 4079–4082 (2016).

    CAS  Article  Google Scholar 

  19. 19.

    Cramer, C. J., Tolman, W. B., Theopold, K. H. & Rheingold, A. L. Variable character of O–O and M–O bonding in side-on (η2) 1:1 metal complexes of O2. Proc. Natl. Acad. Sci. USA 100, 3635–3640 (2003).

    CAS  Article  Google Scholar 

  20. 20.

    Holland, P. L. Metal–dioxygen and metal–dinitrogen complexes: where are the electrons? Dalton Trans. 39, 5415–5425 (2010).

    CAS  Article  Google Scholar 

  21. 21.

    Company, A., Lloret-Fillol, J. & Costas, M. in Comprehensive Inorganic Chemistry II 2nd edn (eds Reedijk, J. & Poeppelmeier, K) 487–564 (Elsevier, 2013).

  22. 22.

    Cho, J. et al. Structure and reactivity of a mononuclear non-haem iron(iii)–peroxo complex. Nature 478, 502–505 (2011).

    CAS  Article  Google Scholar 

  23. 23.

    Bang, S. et al. Redox-inactive metal ions modulate the reactivity and oxygen release of mononuclear non-haem iron(iii)–peroxo complexes. Nat. Chem. 6, 934–940 (2014).

    CAS  Article  Google Scholar 

  24. 24.

    Fukuzumi, S. et al. Catalytic four-electron reduction of O2 via rate-determining proton-coupled electron transfer to a dinuclear cobalt-μ-1,2-peroxo complex. J. Am. Chem. Soc. 134, 9906–9909 (2012).

    CAS  Article  Google Scholar 

  25. 25.

    Polyansky, D. E. et al. Water oxidation by a mononuclear ruthenium catalyst: characterization of the intermediates. J. Am. Chem. Soc. 133, 14649–14665 (2011).

    CAS  Article  Google Scholar 

  26. 26.

    Wang, L., Wu, Q. & Voorhis, T. V. Acid−base mechanism for ruthenium water oxidation catalysts. Inorg. Chem. 49, 4543–4553 (2010).

    CAS  Article  Google Scholar 

  27. 27.

    Casadevall, C., Codolà, Z., Costas, M. & Lloret-Fillol, J. Spectroscopic, electrochemical and computational characterisation of Ru species involved in catalytic water oxidation: evidence for a [Ruv(O)(Py2Metacn)] intermediate. Chem. Eur. J. 22, 10111–10126 (2016).

    CAS  Article  Google Scholar 

  28. 28.

    Shen, J., Stevens, E. D. & Nolan, S. P. Synthesis and reactivity of the ruthenium(ii) dihydride Ru(Ph2PNMeNMePPh2)2H2. Organometallics 17, 3875–3882 (1998).

    CAS  Article  Google Scholar 

  29. 29.

    Cho, J., Sarangi, R. & Nam, W. Mononuclear metal–O2 complexes bearing macrocyclic N-tetramethylated cyclam ligands. Acc. Chem. Res. 45, 1321–1330 (2012).

    CAS  Article  Google Scholar 

  30. 30.

    Savini, A. et al. Mechanistic aspects of water oxidation catalyzed by organometallic iridium complexes. Eur. J. Inorg. Chem. 2014, 690–697 (2014).

    CAS  Article  Google Scholar 

Download references


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.).

Author information




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.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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).

Download citation


Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing