Skip to main content

Thank you for visiting nature.com. 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.

Redox-inactive metals modulate the reduction potential in heterometallic manganese–oxido clusters

Abstract

Redox-inactive metals are found in biological and heterogeneous water oxidation catalysts, but, at present, their roles in catalysis are not well understood. Here, we report a series of high-oxidation-state tetranuclear-dioxido clusters comprising three manganese centres and a redox-inactive metal (M). Crystallographic studies show an unprecedented Mn3M(µ4-O)(µ2-O) core that remains intact on changing M or the manganese oxidation state. Electrochemical studies reveal that the reduction potentials span a window of 700 mV and are dependent on the Lewis acidity of the second metal. With the pKa of the redox-inactive metal–aqua complex as a measure of Lewis acidity, these compounds demonstrate a linear dependence between reduction potential and acidity with a slope of 100 mV per pKa unit. The Sr2+ and Ca2+ compounds show similar potentials, an observation that correlates with the behaviour of the oxygen-evolving complex of photosystem II, which is active only if one of these two metals is present.

Your institute does not have access to this article

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Proposed structures of water oxidation catalysts containing redox-inactive metals (M) in the OEC (left, middle) and in heterogeneous cobalt oxide water oxidation catalysts (right)12,43.
Figure 2: Synthesis of tetrametallic trimanganese dioxido complexes.
Figure 3: Solid-state structures of reported complexes (thermal ellipsoids shown at 50% level).
Figure 4: The shift in the rising edge energy in the Mn XANES spectra.
Figure 5: The redox potentials of the [MMn3O2] complexes are correlated with the Lewis acidity of the redox-inactive metal.

References

  1. Fukuzumi, S. & Ohkubo, K. Metal ion-coupled and decoupled electron transfer. Coord. Chem. Rev. 254, 372–385 (2010).

    CAS  Article  Google Scholar 

  2. Fukuzumi, S. in Progress in Inorganic Chemistry Vol. 56 (ed. Karlin, K. A.) 49–154 (Wiley, 2009).

    Book  Google Scholar 

  3. Yachandra, V. K. & Yano, J. Calcium in the oxygen-evolving complex: structural and mechanistic role determined by X-ray spectroscopy. J. Photochem. Photobiol. B 104, 51–59 (2011).

    CAS  Article  Google Scholar 

  4. Yocum, C. F. The calcium and chloride requirements of the O2 evolving complex. Coord. Chem. Rev. 252, 296–305 (2008).

    CAS  Article  Google Scholar 

  5. McEvoy, J. P. & Brudvig, G. W. Water-splitting chemistry of photosystem II. Chem. Rev. 106, 4455–4483 (2006).

    CAS  Article  Google Scholar 

  6. Park, J. et al. Scandium ion-enhanced oxidative dimerization and N-demethylation of N,N-dimethylanilines by a non-heme iron(IV)–oxo complex. Inorg. Chem. 50, 11612–11622 (2011).

    CAS  Article  Google Scholar 

  7. Fukuzumi, S. et al. Crystal structure of a metal ion-bound oxoiron(IV) complex and implications for biological electron transfer. Nature Chem. 2, 756–759 (2010).

    CAS  Article  Google Scholar 

  8. Morimoto, Y. et al. Metal ion-coupled electron transfer of a nonheme oxoiron(IV) complex: remarkable enhancement of electron-transfer rates by Sc3+. J. Am. Chem. Soc. 133, 403–405 (2011).

    CAS  Article  Google Scholar 

  9. Park, Y. J., Ziller, J. W. & Borovik, A. S. The effects of redox-inactive metal ions on the activation of dioxygen: isolation and characterization of a heterobimetallic complex containing a MnIII-(μ-OH)-CaII core. J. Am. Chem. Soc. 133, 9258–9261 (2011).

    CAS  Article  Google Scholar 

  10. Park, Y. J. et al. Heterobimetallic complexes with MIII-(μ-OH)-MII cores (MIII=Fe, Mn, Ga; MII=Ca, Sr, and Ba): structural, kinetic, and redox properties. Chem. Sci. 4, 717–726 (2013).

    CAS  Article  Google Scholar 

  11. Miller, C. G. et al. A method for driving O-atom transfer: secondary ion binding to a tetraamide macrocyclic ligand. J. Am. Chem. Soc. 120, 11540–11541 (1998).

    CAS  Article  Google Scholar 

  12. Risch, M. et al. Water oxidation by electrodeposited cobalt oxides—role of anions and redox-inert cations in structure and function of the amorphous catalyst. ChemSusChem 5, 542–549 (2012).

    CAS  Article  Google Scholar 

  13. Kanan, M. W. et al. Structure and valency of a cobalt-phosphate water oxidation catalyst determined by in situ X-ray spectroscopy. J. Am. Chem. Soc. 132, 13692–13701 (2010).

    CAS  Article  Google Scholar 

  14. Kanan, M. W. & Nocera, D. G. In situ formation of an oxygen-evolving catalyst in neutral water containing phosphate and Co2+. Science 321, 1072–1075 (2008).

    CAS  Article  Google Scholar 

  15. Wiechen, M., Zaharieva, I., Dau, H. & Kurz, P. Layered manganese oxides for water oxidation: alkaline earth cations influence catalytic activity in a photosystem II-like fashion. Chem. Sci. 3, 2330–2339 (2012).

    CAS  Article  Google Scholar 

  16. Najafpour, M. M., Ehrenberg, T., Wiechen, M. & Kurz, P. Calcium manganese(III) oxides (CaMn2O4·xH2O) as biomimetic oxygen-evolving catalysts. Angew. Chem. Int. Ed. 49, 2233–2237 (2010).

    CAS  Article  Google Scholar 

  17. Najafpour, M. M., Pashaei, B. & Nayeri, S. Calcium manganese(IV) oxides: biomimetic and efficient catalysts for water oxidation. Dalton Trans. 41, 4799–4805 (2012).

    CAS  Article  Google Scholar 

  18. Umena, Y., Kawakami, K., Shen, J. R. & Kamiya, N. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473, 55–U65 (2011).

    CAS  Article  Google Scholar 

  19. Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J. & Iwata, S. Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831–1838 (2004).

    CAS  Google Scholar 

  20. Yamada, Y., Yano, K., Hong, D. & Fukuzumi, S. LaCoO3 acting as an efficient and robust catalyst for photocatalytic water oxidation with persulfate. Phys. Chem. Chem. Phys. 14, 5753–5760 (2012).

    CAS  Article  Google Scholar 

  21. Kanady, J. S., Tsui, E. Y., Day, M. W. & Agapie, T. A synthetic model of the Mn3Ca subsite of the oxygen-evolving complex in photosystem II. Science 333, 733–736 (2011).

    CAS  Article  Google Scholar 

  22. Tsui, E. Y., Day, M. W. & Agapie, T. Trinucleating copper: synthesis and magnetostructural characterization of complexes supported by a hexapyridyl 1,3,5-triarylbenzene ligand. Angew. Chem. Int. Ed. 50, 1668–1672 (2011).

    CAS  Article  Google Scholar 

  23. Tsui, E. Y., Kanady, J. S., Day, M. W. & Agapie, T. Trinuclear first row transition metal complexes of a hexapyridyl, trialkoxy 1,3,5-triarylbenzene ligand. Chem. Commun. 47, 4189–4191 (2011).

    CAS  Article  Google Scholar 

  24. Kanady, J. S., Mendoza-Cortes, J. L., Tsui, E. Y., Nielsen, R. J., Goddard, W. A., and Agapie, T. Oxygen atom transfer and oxidative water incorporation in cuboidal Mn3MOn complexes based on synthetic, isotopic labeling, and computational studies. J. Am. Chem. Soc. 135, 1073–1082 (2013).

    CAS  Article  Google Scholar 

  25. Lacy, D. C., Park, Y. J., Ziller, J. W., Yano, J. & Borovik, A. S. Assembly and properties of heterobimetallic CoII/III/CaII complexes with aquo and hydroxo ligands. J. Am. Chem. Soc. 134, 17526–17535 (2012).

    CAS  Article  Google Scholar 

  26. Mukherjee, S. et al. Synthetic model of the asymmetric [Mn3CaO4] cubane core of the oxygen-evolving complex of photosystem II. Proc. Natl Acad. Sci. USA 109, 2257–2262 (2012).

    CAS  Article  Google Scholar 

  27. Mishra, A. et al. Heteronuclear Mn–Ca/Sr complexes, and Ca/Sr EXAFS spectral comparisons with the oxygen-evolving complex of photosystem II. Chem. Commun. 1538–1540 (2007).

  28. Mishra, A., Wernsdorfer, W., Abboud, K. A. & Christou, G. The first high oxidation state manganese-calcium cluster: relevance to the water oxidizing complex of photosynthesis. Chem. Commun. 54–56 (2005).

  29. Kotzabasaki, V., Siczek, M., Lis, T. & Milios, C. J. The first heterometallic Mn–Ca cluster containing exclusively Mn(III) centers. Inorg. Chem. Commun. 14, 213–216 (2011).

    CAS  Article  Google Scholar 

  30. Hewitt, I. J. et al. A series of new structural models for the OEC in photosystem II. Chem. Commun. 2650–2652 (2006).

  31. Nayak, S., Nayek, H. P., Dehnen, S., Powell, A. K. & Reedijk, J. Trigonal propeller-shaped [MnIII3MIINa] complexes (M=Mn, Ca): structural and functional models for the dioxygen evolving centre of PSII. Dalton Trans. 40, 2699–2702 (2011).

    CAS  Article  Google Scholar 

  32. Visser, H. et al. Mn K-edge XANES and Kβ XES studies of two Mn–Oxo binuclear complexes: investigation of three different oxidation states relevant to the oxygen-evolving complex of photosystem II. J. Am. Chem. Soc. 123, 7031–7039 (2001).

    CAS  Article  Google Scholar 

  33. Pushkar, Y., Yano, J., Sauer, K., Boussac, A., & Yachandra, V. K. Structural changes in the Mn4Ca cluster and the mechanism of photosynthetic water splitting. Proc. Natl Acad. Sci. USA 105, 1879–1884 (2008).

    CAS  Article  Google Scholar 

  34. Leeladee, P. et al. Valence tautomerism in a high-valent manganese–oxo porphyrinoid complex induced by a Lewis acid. J. Am. Chem. Soc. 134, 10397–10400 (2012).

    CAS  Article  Google Scholar 

  35. Horwitz, C. P. & Ciringh, Y. Synthesis and electrochemical properties of oxo-bridged manganese dimers incorporating alkali and alkaline earth cations. Inorg. Chim. Acta 225, 191–200 (1994).

    CAS  Article  Google Scholar 

  36. Horwitz, C. P., Ciringh, Y. & Weintraub, S. T. Formation pathway of a Mn(IV),Mn(IV) bis(μ-oxo) dimer that incorporates alkali and alkaline earth cations and electron transfer properties of the dimer. Inorg. Chim. Acta 294, 133–139 (1999).

    CAS  Article  Google Scholar 

  37. Fukuzumi, S. & Ohkubo, K. Quantitative evaluation of Lewis acidity of metal ions derived from the g values of ESR spectra of superoxide: metal ion complexes in relation to the promoting effects in electron transfer reactions. Chem. Eur. J. 6, 4532–4535 (2000).

    CAS  Article  Google Scholar 

  38. Perrin, D. D. Ionisation Constants of Inorganic Acids and Bases in Aqueous Solution (Pergamon, 1982).

    Google Scholar 

  39. Cox, N. et al. Effect of Ca2+/Sr2+ substitution on the electronic structure of the oxygen-evolving complex of photosystem II: a combined multifrequency EPR, 55Mn-ENDOR, and DFT study of the S2 state. J. Am. Chem. Soc. 133, 3635–3648 (2011).

    CAS  Article  Google Scholar 

  40. Pecoraro, V. L., Baldwin, M. J., Caudle, M. T., Hsieh, W. Y. & Law, N. A. A proposal for water oxidation in photosystem II. Pure Appl. Chem. 70, 925–929 (1998).

    CAS  Article  Google Scholar 

  41. Saltzman, H. & Sharefkin, J. G. Iodosobenzene. Org. Synth. Coll. 5, 658–659 (1973).

    Google Scholar 

  42. Sheldrick, G. A short history of SHELX. Acta Crysallogr. A 64, 112–122 (2008).

    CAS  Article  Google Scholar 

  43. Symes, M. D., Surendranath, Y., Lutterman, D. A. & Nocera, D. G. Bidirectional and unidirectional PCET in a molecular model of a cobalt-based oxygen-evolving catalyst. J. Am. Chem. Soc. 133, 5174–5177 (2011).

    CAS  Article  Google Scholar 

  44. Yano, J. et al. Where water is oxidized to dioxygen: structure of the photosynthetic Mn4Ca cluster. Science 314, 821–825 (2006).

    CAS  Article  Google Scholar 

  45. Peloquin, J. M. et al. 55Mn ENDOR of the S2-state multiline EPR signal of photosystem II: implications on the structure of the tetranuclear Mn cluster. J. Am. Chem. Soc. 122, 10926–10942 (2000).

    CAS  Article  Google Scholar 

  46. Ames, W. et al. Theoretical evaluation of structural models of the S2 state in the oxygen evolving complex of photosystem II: protonation states and magnetic interactions. J. Am. Chem. Soc. 133, 19743–19757 (2011).

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the California Institute of Technology, the Searle Scholars Program, an NSF CAREER award (CHE-1151918 to T.A.) and the NSF Graduate Research Fellowship Program (to E.Y.T.). The authors thank L.M. Henling and D.E. Herbert for assistance with crystallography, and P-H. Lin for assistance with magnetic susceptibility studies. The Bruker KAPPA APEXII X-ray diffractometer was purchased with an NSF Chemistry Research Instrumentation award to Caltech (CHE-0639094). The X-ray spectroscopy work was supported by the NIH (grant no. F32GM100595 to R.T.) and by the Director of the Office of Basic Energy Science (OBES), Division of Chemical Sciences, Geosciences, and Biosciences, DOE (contract no. DE-AC02-05CH11231 to J.Y.). Synchrotron facilities were provided by the Stanford Synchrotron Radiation Lightsource (SSRL), operated by the DOE, OBER.

Author information

Authors and Affiliations

Authors

Contributions

E.Y.T. and T.A. designed the research. E.Y.T. and R.T. performed the experiments. R.T. and J.Y. provided XANES characterization. E.Y.T., R.T., J.Y. and T.A. analysed data. E.Y.T. and T.A. wrote the paper.

Corresponding author

Correspondence to Theodor Agapie.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary information

Supplementary information (PDF 3845 kb)

Supplementary information

Crystallographic data for compound [1-Ca(DME)(OTf)](OTf)2 (CIF 42 kb)

Supplementary information

Crystallographic data for compound [1-Ca(H¬2O)3](OTf)3 (CIF 57 kb)

Supplementary information

Crystallographic data for compound [2-Ca(DME)(OTf)](OTf) (CIF 44 kb)

Supplementary information

Crystallographic data for compound [1-Sr(DME)(OTf)](OTf)2 (CIF 42 kb)

Supplementary information

Crystallographic data for compound [2-Sr(DME)(OTf)](OTf) (CIF 44 kb)

Supplementary information

Crystallographic data for compound [1-Zn(CH3CN)](OTf)3 (CIF 40 kb)

Supplementary information

Crystallographic data for compound [1-Na]2(OTf)4 (CIF 36 kb)

Supplementary information

Crystallographic data for compound [2-Y(DME)(OTf)](OTf)2 (CIF 63 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Tsui, E., Tran, R., Yano, J. et al. Redox-inactive metals modulate the reduction potential in heterometallic manganese–oxido clusters. Nature Chem 5, 293–299 (2013). https://doi.org/10.1038/nchem.1578

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nchem.1578

Further reading

Search

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