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.

  • Article
  • Published:

Crystal structure of a metal ion-bound oxoiron(IV) complex and implications for biological electron transfer

Nature Chemistry volume 2, pages 756–759 (2010)Cite this article

Subjects

Abstract

Critical biological electron-transfer processes involving high-valent oxometal chemistry occur widely, for example in haem proteins [oxoiron(IV); FeIV(O)] and in photosystem II. Photosystem II involves Ca2+ as well as high-valent oxomanganese cluster species. However, there is no example of an interaction between metal ions and oxoiron(IV) complexes. Here, we report new findings concerning the binding of the redox-inactive metal ions Ca2+ and Sc3+ to a non-haem oxoiron(IV) complex, [(TMC)FeIV(O)]2+ (TMC = 1,4,8,11-tetramethyl-1,4,8,11-tetraazacyclotetradecane). As determined by X-ray diffraction analysis, an oxo-Sc3+ interaction leads to a structural distortion of the oxoiron(IV) moiety. More importantly, this interaction facilitates a two-electron reduction by ferrocene, whereas only a one-electron reduction process occurs without the metal ions. This control of redox behaviour provides valuable mechanistic insights into oxometal redox chemistry, and suggests a possible key role that an auxiliary Lewis acid metal ion could play in nature, as in photosystem II.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Sc3+ effect on the ET reaction of [(TMC)FeIV(O)]2+.
Figure 2: Kinetic measurements of ET from Fc to [(TMC)FeIV(O)]2+.
Figure 3: Temperature dependence on the ET rate constants.
Figure 4: Sc3+-bound (TMC)FeIV(O) complex.
Figure 5: Comparison of the (TMC)FeIV(O) complex and the Sc3+-bound (TMC)FeIV(O) complex.

Similar content being viewed by others

References

  1. Kaim, W. & Schwederski, B. Bioinorganic Chemistry: Inorganic Elements in the Chemistry of Life (Wiley, 1994).

    Google Scholar 

  2. Kovacs, J. A. How iron activates O2 . Science 299, 1024–1025 (2009).

    Article  Google Scholar 

  3. Ferguson-Miller, S. & Babcock, G. T. Heme/copper terminal oxidases. Chem. Rev. 96, 2889–2908 (1996).

    Article  CAS  Google Scholar 

  4. Diner, B. A. & Babcock, G. T. Oxygenic Photosynthesis: The Light Reactions (Kluwer Academic Publishers, 1996).

    Google Scholar 

  5. Yagi, M. & Kaneko, M. Molecular catalysts for water oxidation. Chem. Rev. 101, 21–36 (2001).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  7. Ferreira, K. N. et al. Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831–1838 (2004).

    Article  CAS  Google Scholar 

  8. Loll, B. et al. Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438, 1040–1044 (2005).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  10. Sporoviero, E. M. et al. Quantum mechanics/molecular mechanics study of the catalytic cycle of water splitting in photosystem II. J. Am. Chem. Soc. 130, 3428–3442 (2008).

    Article  Google Scholar 

  11. Barber, J. Photosynthetic energy conversion: natural and artificial. Chem. Soc. Rev. 38, 185–196 (2009).

    Article  CAS  Google Scholar 

  12. Que, L. Jr The road to non-heme oxoferryls and beyond. Acc. Chem. Res. 40, 493–500 (2007).

    Article  CAS  Google Scholar 

  13. Nam, W. High-valent iron(IV)–oxo complexes of heme and non-heme ligands in oxygenation reactions. Acc. Chem. Res. 40, 522–531 (2007).

    Article  CAS  Google Scholar 

  14. Sono, M., Roach, M. P., Coulter, E. D. & Dawson, J. H. Heme-containing oxygenases. Chem. Rev. 96, 2841–2887 (1996).

    Article  CAS  Google Scholar 

  15. Meunier, B. (ed.) Metal-Oxo and Metal-Peroxo Species in Catalytic Oxidations (Springer-Verlag, 2000).

    Book  Google Scholar 

  16. Ortiz de Montellano, P. R. (ed.) Cytochrome P450: Structure, Mechanism, and Biochemistry (Kluwer Acaemic/Plenum Publishers, 2005).

    Book  Google Scholar 

  17. Fukuzumi, S. Roles of metal ions in controlling bioinspired electron-transfer systems. Metal ion-coupled electron transfer. Prog. Inorg. Chem. 56, 49–153 (2009).

    Article  CAS  Google Scholar 

  18. Fukuzumi, S. Catalysis on electron transfer and the mechanistic insight into redox reactions. Bull. Chem. Soc. Jpn 70, 1–28 (1997).

    Article  CAS  Google Scholar 

  19. Fukuzumi, S. New perspective of electron transfer chemistry. Org. Biomol. Chem. 1, 609–620 (2003).

    Article  CAS  Google Scholar 

  20. Rohde, J.-U. et al. Crystallographic and spectroscopic characterization of a nonheme Fe(IV)=O complex. Science 299, 1037–1039 (2003).

    Article  CAS  Google Scholar 

  21. Lee, Y.-M. et al. Fundamental electron-transfer properties of non-heme oxoiron(IV) complexes. J. Am. Chem. Soc. 130, 434–435 (2008).

    Article  CAS  Google Scholar 

  22. 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 with the promoting effects in electron transfer reactions. Chem. Eur. J. 6, 4532–4535 (2000).

    Article  CAS  Google Scholar 

  23. Fukuzumi, S. & Ohkubo, K. Fluorescence maxima of 10-methylacridone–metal ion salt complexes: a convenient and quantitative measure of Lewis acidity of metal ion salts. J. Am. Chem. Soc. 124, 10270–10271 (2002).

    Article  CAS  Google Scholar 

  24. Bukowski, M. R. et al. A thiolate-ligated nonheme oxoiron(IV) complex relevant to cytochrome P450. Science 310, 1000–1002 (2005).

    Article  CAS  Google Scholar 

  25. Thibon, A. et al. Proton- and reductant-assisted dioxygen activation by a nonheme iron(II) complex to form an oxoiron(IV) intermediate. Angew. Chem. Int. Ed. 47, 7064–7067 (2008).

    Article  CAS  Google Scholar 

  26. Ray, K. et al. An inverted and more oxidizing isomer of [FeIV(O)(tmc)(NCCH3)]2+. Angew. Chem. Int. Ed. 47, 8068–8071 (2008).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by a Grant-in-Aid (no. 20108010 to S.F.) and a Global COE program, ‘the Global Education and Research Center for Bio-Environmental Chemistry’ from the Ministry of Education, Culture, Sports, Science and Technology, Japan (to S.F.), and NRF/MEST through a WCU project (R31-2008-000-10010-0) (to S.F. and W.N.) and the Creative Research Initiatives Program (to W.N.). Crystallographic data for [(TMC)FeIV(O)–Sc(OTf)4(OH)] have been deposited with the Cambridge Crystallographic Data Center under reference numbers CCDC-742067 (X-ray).

Author information

Authors and Affiliations

  1. Department of Material and Life Science, Division of Advanced Science and Biotechnology, Graduate School of Engineering, Osaka University, SORST, Japan Science and Technology Agency (JST), Suita, 565-0871, Osaka, Japan

    Shunichi Fukuzumi, Yuma Morimoto, Hiroaki Kotani & Panče Naumov

  2. Department of Bioinspired Science, Ewha Womans University, Seoul, 120-750, Korea

    Shunichi Fukuzumi, Yong-Min Lee & Wonwoo Nam

  3. Department of Chemistry and Nano Science, Center for Biomimetic Systems, Ewha Womans University, Seoul, 120-750, Korea

    Yong-Min Lee & Wonwoo Nam

Authors
  1. Shunichi Fukuzumi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yuma Morimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hiroaki Kotani
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Panče Naumov
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yong-Min Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Wonwoo Nam
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

S.F., Y.M., H.K. and W.N. conceived and designed the experiments. Y.M. and P.N. performed the experiments. Y.M., H.K. and P.N. analysed the data. P.N. and Y.M.L. contributed materials and analysis tools. S.F. and W.N. co-wrote the paper.

Corresponding authors

Correspondence to Shunichi Fukuzumi or Wonwoo Nam.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary information

Supplementary information (PDF 1206 kb)

Supplementary information

Crystallographic data for the non-heme oxoiron(IV) complex (CIF 24 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Fukuzumi, S., Morimoto, Y., Kotani, H. et al. Crystal structure of a metal ion-bound oxoiron(IV) complex and implications for biological electron transfer. Nature Chem 2, 756–759 (2010). https://doi.org/10.1038/nchem.731

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nchem.731

This article is cited by

Search

Advanced 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