Switching the redox mechanism: Models for proton-coupled electron transfer from tyrosine and tryptophan

Martin Sjödin, Stenbjörn Styring, Henriette Wolpher, Yunhua Xu, Licheng Sun, Leif Hammarström

Research output: Contribution to journalArticle

189 Citations (Scopus)

Abstract

The coupling of electron and proton transfer is an important controlling factor in radical proteins, such as photosystem II, ribinucleotide reductase, cytochrome oxidases, and DNA photolyase. This was investigated in model complexes in which a tyrosine or tryptophan residue was oxidized by a laser-flash generated trisbipyridine-RuIII moiety in an intramolecular, proton-coupled electron transfer (PCET) reaction. The PCET was found to proceed in a competition between a stepwise reaction, in which electron transfer is followed by deprotonation of the amino acid radical (ETPT), and a concerted reaction, in which both the electron and proton are transferred in a single reaction step (CEP). Moreover, we found that we could analyze the kinetic data for PCET by Marcus' theory for electron transfer. By altering the solution pH, the strength of the RuIII oxidant, or the identity of the amino acid, we could induce a switch between the two mechanisms and obtain quantitative data for the parameters that control which one will dominate. The characteristic pH-dependence of the CEP rate (M. Sjödin et al. J. Am. Chem. Soc. 2000, 122, 3932) reflects the pH-dependence of the driving force caused by proton release to the bulk. For the pH-independent ETPT on the other hand, the driving force of the rate-determining ET step is pH-independent and smaller. On the other hand, temperature-dependent data showed that the reorganization energy was higher for CEP, while the pre-exponential factors showed no significant difference between the mechanisms. Thus, the opposing effect of the differences in driving force and reorganization energy determines which of the mechanisms will dominate. Our results show that a concerted mechanism is in general quite likely and provides a low-barrier reaction pathway for weakly exoergonic reactions. In addition, the kinetic isotope effect was much higher for CEP (kH/kD > 10) than for ETPT (kH/kD = 2), consistent with significant changes along the proton reaction coordinate in the rate-determining step of CEP.

Original languageEnglish
Pages (from-to)3855-3863
Number of pages9
JournalJournal of the American Chemical Society
Volume127
Issue number11
DOIs
Publication statusPublished - 2005 Mar 23
Externally publishedYes

Fingerprint

Tryptophan
Oxidation-Reduction
Tyrosine
Protons
Electrons
Amino acids
Deoxyribodipyrimidine Photo-Lyase
Amino Acids
Deprotonation
Kinetics
Proton transfer
Photosystem II Protein Complex
Electron Transport Complex IV
Oxidants
Isotopes
Oxidoreductases
Lasers
DNA
Switches
Proteins

ASJC Scopus subject areas

  • Catalysis
  • Chemistry(all)
  • Biochemistry
  • Colloid and Surface Chemistry

Cite this

Switching the redox mechanism : Models for proton-coupled electron transfer from tyrosine and tryptophan. / Sjödin, Martin; Styring, Stenbjörn; Wolpher, Henriette; Xu, Yunhua; Sun, Licheng; Hammarström, Leif.

In: Journal of the American Chemical Society, Vol. 127, No. 11, 23.03.2005, p. 3855-3863.

Research output: Contribution to journalArticle

Sjödin, Martin ; Styring, Stenbjörn ; Wolpher, Henriette ; Xu, Yunhua ; Sun, Licheng ; Hammarström, Leif. / Switching the redox mechanism : Models for proton-coupled electron transfer from tyrosine and tryptophan. In: Journal of the American Chemical Society. 2005 ; Vol. 127, No. 11. pp. 3855-3863.
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AU - Sjödin, Martin

AU - Styring, Stenbjörn

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AU - Xu, Yunhua

AU - Sun, Licheng

AU - Hammarström, Leif

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