Pourbaix Diagram, Proton-Coupled Electron Transfer, and Decay Kinetics of a Protein Tryptophan Radical: Comparing the Redox Properties of W32 and Y32 Generated Inside the Structurally Characterized α3W and α3Y Proteins

Starla D. Glover, Robin Tyburski, Li Liang, Cecilia Tommos, Leif Hammarström

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4 Citations (Scopus)

Abstract

Protein-based "hole" hopping typically involves spatially arranged redox-active tryptophan or tyrosine residues. Thermodynamic information is scarce for this type of process. The well-structured α3W model protein was studied by protein film square wave voltammetry and transient absorption spectroscopy to obtain a comprehensive thermodynamic and kinetic description of a buried tryptophan residue. A Pourbaix diagram, correlating thermodynamic potentials (E°′) with pH, is reported for W32 in α3W and compared to equivalent data recently presented for Y32 in α3Y (Ravichandran, K. R.; Zong, A. B.; Taguchi, A. T.; Nocera, D. G.; Stubbe, J.; Tommos, C. J. Am. Chem. Soc. 2017, 139, 2994-3004). The α3W Pourbaix diagram displays a pKOX of 3.4, a E°′(W32(N•+/NH)) of 1293 mV, and a E°′(W32(N/NH); pH 7.0) of 1095 ± 4 mV versus the normal hydrogen electrode. W32(N/NH) is 109 ± 4 mV more oxidizing than Y32(O/OH) at pH 5.4-10. In the voltammetry measurements, W32 oxidation-reduction occurs on a time scale of about 4 ms and is coupled to the release and subsequent uptake of one full proton to and from bulk. Kinetic analysis further shows that W32 oxidation likely involves pre-equilibrium electron transfer followed by proton transfer to a water or small water cluster as the primary acceptor. A well-resolved absorption spectrum of W32 is presented, and analysis of decay kinetics show that W32 persists ∼104 times longer than aqueous W due to significant stabilization by the protein. The redox characteristics of W32 and Y32 are discussed relative to global and local protein properties.

Original languageEnglish
Pages (from-to)185-192
Number of pages8
JournalJournal of the American Chemical Society
Volume140
Issue number1
DOIs
Publication statusPublished - Jan 10 2018

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Tryptophan
Oxidation-Reduction
Protons
Electrons
Proteins
Kinetics
Thermodynamics
Voltammetry
Proton transfer
Water
Absorption spectroscopy
Tyrosine
Absorption spectra
Hydrogen
Spectrum Analysis
Electrodes
Stabilization
Oxidation

ASJC Scopus subject areas

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

Cite this

@article{19a4a542e96147b9884f5d407d2e378c,
title = "Pourbaix Diagram, Proton-Coupled Electron Transfer, and Decay Kinetics of a Protein Tryptophan Radical: Comparing the Redox Properties of W32 • and Y32 • Generated Inside the Structurally Characterized α3W and α3Y Proteins",
abstract = "Protein-based {"}hole{"} hopping typically involves spatially arranged redox-active tryptophan or tyrosine residues. Thermodynamic information is scarce for this type of process. The well-structured α3W model protein was studied by protein film square wave voltammetry and transient absorption spectroscopy to obtain a comprehensive thermodynamic and kinetic description of a buried tryptophan residue. A Pourbaix diagram, correlating thermodynamic potentials (E°′) with pH, is reported for W32 in α3W and compared to equivalent data recently presented for Y32 in α3Y (Ravichandran, K. R.; Zong, A. B.; Taguchi, A. T.; Nocera, D. G.; Stubbe, J.; Tommos, C. J. Am. Chem. Soc. 2017, 139, 2994-3004). The α3W Pourbaix diagram displays a pKOX of 3.4, a E°′(W32(N•+/NH)) of 1293 mV, and a E°′(W32(N•/NH); pH 7.0) of 1095 ± 4 mV versus the normal hydrogen electrode. W32(N•/NH) is 109 ± 4 mV more oxidizing than Y32(O•/OH) at pH 5.4-10. In the voltammetry measurements, W32 oxidation-reduction occurs on a time scale of about 4 ms and is coupled to the release and subsequent uptake of one full proton to and from bulk. Kinetic analysis further shows that W32 oxidation likely involves pre-equilibrium electron transfer followed by proton transfer to a water or small water cluster as the primary acceptor. A well-resolved absorption spectrum of W32 • is presented, and analysis of decay kinetics show that W32 • persists ∼104 times longer than aqueous W• due to significant stabilization by the protein. The redox characteristics of W32 and Y32 are discussed relative to global and local protein properties.",
author = "Glover, {Starla D.} and Robin Tyburski and Li Liang and Cecilia Tommos and Leif Hammarstr{\"o}m",
year = "2018",
month = "1",
day = "10",
doi = "10.1021/jacs.7b08032",
language = "English",
volume = "140",
pages = "185--192",
journal = "Journal of the American Chemical Society",
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TY - JOUR

T1 - Pourbaix Diagram, Proton-Coupled Electron Transfer, and Decay Kinetics of a Protein Tryptophan Radical

T2 - Comparing the Redox Properties of W32 • and Y32 • Generated Inside the Structurally Characterized α3W and α3Y Proteins

AU - Glover, Starla D.

AU - Tyburski, Robin

AU - Liang, Li

AU - Tommos, Cecilia

AU - Hammarström, Leif

PY - 2018/1/10

Y1 - 2018/1/10

N2 - Protein-based "hole" hopping typically involves spatially arranged redox-active tryptophan or tyrosine residues. Thermodynamic information is scarce for this type of process. The well-structured α3W model protein was studied by protein film square wave voltammetry and transient absorption spectroscopy to obtain a comprehensive thermodynamic and kinetic description of a buried tryptophan residue. A Pourbaix diagram, correlating thermodynamic potentials (E°′) with pH, is reported for W32 in α3W and compared to equivalent data recently presented for Y32 in α3Y (Ravichandran, K. R.; Zong, A. B.; Taguchi, A. T.; Nocera, D. G.; Stubbe, J.; Tommos, C. J. Am. Chem. Soc. 2017, 139, 2994-3004). The α3W Pourbaix diagram displays a pKOX of 3.4, a E°′(W32(N•+/NH)) of 1293 mV, and a E°′(W32(N•/NH); pH 7.0) of 1095 ± 4 mV versus the normal hydrogen electrode. W32(N•/NH) is 109 ± 4 mV more oxidizing than Y32(O•/OH) at pH 5.4-10. In the voltammetry measurements, W32 oxidation-reduction occurs on a time scale of about 4 ms and is coupled to the release and subsequent uptake of one full proton to and from bulk. Kinetic analysis further shows that W32 oxidation likely involves pre-equilibrium electron transfer followed by proton transfer to a water or small water cluster as the primary acceptor. A well-resolved absorption spectrum of W32 • is presented, and analysis of decay kinetics show that W32 • persists ∼104 times longer than aqueous W• due to significant stabilization by the protein. The redox characteristics of W32 and Y32 are discussed relative to global and local protein properties.

AB - Protein-based "hole" hopping typically involves spatially arranged redox-active tryptophan or tyrosine residues. Thermodynamic information is scarce for this type of process. The well-structured α3W model protein was studied by protein film square wave voltammetry and transient absorption spectroscopy to obtain a comprehensive thermodynamic and kinetic description of a buried tryptophan residue. A Pourbaix diagram, correlating thermodynamic potentials (E°′) with pH, is reported for W32 in α3W and compared to equivalent data recently presented for Y32 in α3Y (Ravichandran, K. R.; Zong, A. B.; Taguchi, A. T.; Nocera, D. G.; Stubbe, J.; Tommos, C. J. Am. Chem. Soc. 2017, 139, 2994-3004). The α3W Pourbaix diagram displays a pKOX of 3.4, a E°′(W32(N•+/NH)) of 1293 mV, and a E°′(W32(N•/NH); pH 7.0) of 1095 ± 4 mV versus the normal hydrogen electrode. W32(N•/NH) is 109 ± 4 mV more oxidizing than Y32(O•/OH) at pH 5.4-10. In the voltammetry measurements, W32 oxidation-reduction occurs on a time scale of about 4 ms and is coupled to the release and subsequent uptake of one full proton to and from bulk. Kinetic analysis further shows that W32 oxidation likely involves pre-equilibrium electron transfer followed by proton transfer to a water or small water cluster as the primary acceptor. A well-resolved absorption spectrum of W32 • is presented, and analysis of decay kinetics show that W32 • persists ∼104 times longer than aqueous W• due to significant stabilization by the protein. The redox characteristics of W32 and Y32 are discussed relative to global and local protein properties.

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