Why copper is preferred over iron for oxygen activation and reduction in haem-copper oxidases

Ambika Bhagi-Damodaran, Matthew A. Michael, Qianhong Zhu, Julian Reed, Braddock A. Sandoval, Evan N. Mirts, Saumen Chakraborty, Pierre Moenne-Loccoz, Yong Zhang, Yi Lu

Research output: Contribution to journalArticle

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Abstract

Haem-copper oxidase (HCO) catalyses the natural reduction of oxygen to water using a haem-copper centre. Despite decades of research on HCOs, the role of non-haem metal and the reason for nature's choice of copper over other metals such as iron remains unclear. Here, we use a biosynthetic model of HCO in myoglobin that selectively binds different non-haem metals to demonstrate 30-fold and 11-fold enhancements in the oxidase activity of Cu- and Fe-bound HCO mimics, respectively, as compared with Zn-bound mimics. Detailed electrochemical, kinetic and vibrational spectroscopic studies, in tandem with theoretical density functional theory calculations, demonstrate that the non-haem metal not only donates electrons to oxygen but also activates it for efficient O-O bond cleavage. Furthermore, the higher redox potential of copper and the enhanced weakening of the O-O bond from the higher electron density in the d orbital of copper are central to its higher oxidase activity over iron. This work resolves a long-standing question in bioenergetics, and renders a chemical-biological basis for the design of future oxygen-reduction catalysts.

Original languageEnglish (US)
Pages (from-to)257-263
Number of pages7
JournalNature Chemistry
Volume9
Issue number3
DOIs
StatePublished - Mar 1 2017

Fingerprint

Heme
Copper
Iron
Metals
Chemical activation
Oxygen
Oxidoreductases
Myoglobin
Density functional theory
Carrier concentration
Catalysts
Kinetics
copper oxidase
Electrons
Water

ASJC Scopus subject areas

  • Chemistry(all)
  • Chemical Engineering(all)

Cite this

Bhagi-Damodaran, A., Michael, M. A., Zhu, Q., Reed, J., Sandoval, B. A., Mirts, E. N., ... Lu, Y. (2017). Why copper is preferred over iron for oxygen activation and reduction in haem-copper oxidases. Nature Chemistry, 9(3), 257-263. https://doi.org/10.1038/nchem.2643

Why copper is preferred over iron for oxygen activation and reduction in haem-copper oxidases. / Bhagi-Damodaran, Ambika; Michael, Matthew A.; Zhu, Qianhong; Reed, Julian; Sandoval, Braddock A.; Mirts, Evan N.; Chakraborty, Saumen; Moenne-Loccoz, Pierre; Zhang, Yong; Lu, Yi.

In: Nature Chemistry, Vol. 9, No. 3, 01.03.2017, p. 257-263.

Research output: Contribution to journalArticle

Bhagi-Damodaran, A, Michael, MA, Zhu, Q, Reed, J, Sandoval, BA, Mirts, EN, Chakraborty, S, Moenne-Loccoz, P, Zhang, Y & Lu, Y 2017, 'Why copper is preferred over iron for oxygen activation and reduction in haem-copper oxidases', Nature Chemistry, vol. 9, no. 3, pp. 257-263. https://doi.org/10.1038/nchem.2643
Bhagi-Damodaran A, Michael MA, Zhu Q, Reed J, Sandoval BA, Mirts EN et al. Why copper is preferred over iron for oxygen activation and reduction in haem-copper oxidases. Nature Chemistry. 2017 Mar 1;9(3):257-263. https://doi.org/10.1038/nchem.2643
Bhagi-Damodaran, Ambika ; Michael, Matthew A. ; Zhu, Qianhong ; Reed, Julian ; Sandoval, Braddock A. ; Mirts, Evan N. ; Chakraborty, Saumen ; Moenne-Loccoz, Pierre ; Zhang, Yong ; Lu, Yi. / Why copper is preferred over iron for oxygen activation and reduction in haem-copper oxidases. In: Nature Chemistry. 2017 ; Vol. 9, No. 3. pp. 257-263.
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