Construction of artificial photosynthetic reaction centers on a protein surface: Vectorial, multistep, and proton-coupled electron transfer for long- lived charge separation

Yi Zhen Hu, Shinya Tsukiji, Seiji Shinkai, Shigero Oishi, Itaru Hamachi

Research output: Contribution to journalArticle

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Abstract

Artificial photosynthetic reaction centers have been constructed on a protein surface by cofactor reconstitution, which mimic the function of photosynthetic organisms to convert light energy to chemical potential in the form of long-lived charge-separated states. They feature a ruthenium tris(2,2'-bipyridine) moiety as the sensitizer, which is mechanically linked (i.e., in catenane-type) with a cyclobis(paraquat-p-phenylene) unit (BXV4+, acceptor) and covalently linked with a protoheme or Zn-protoporphyrin (donor) located in the myoglobin pocket. Their cofactors 1 and 2, which are tris(heteroleptic) Ru-bipyridine complexes, were synthesized by sequential coordination of the two different functionalized bipyridine ligands with a readily obtainable precursor [Ru(4,4'-dimethyl-2,2'-bipyridine)Cl3](n) followed by metal insertion; this represents a new efficient synthetic method for tris(heteroleptic) Ru(II) complexes of bidentate polypyridine ligands. Reconstitution of apo-myoglobin (Mb) with 1 and 2 affords the two Mb-based artificial triads, Mb(Fe(III)OH2)-Ru2+-BXV4+ and Mb(Zn)-Ru2+-BXV4+. Laser flash photolysis of the Ru(bpy)3 moiety of Mb(Fe(III)OH2)-Ru2+- BXV4+ in an aqueous solution yields an initial charge-separated state, Mb(Fe(III)OH2)-Ru3+-BXV3+(·), via noncovalent electron transfer, followed by dark electron transfer to generate an intermediate consisting of porphyrin cation radical, Mb(Fe(III·)OH2)-Ru2+-BXV3+(·). Mb(Fe(III ·)OH2)-Ru2+-BXV3+ (·) thus generated is subsequently converted, via a proton-coupled process and with a quantum yield of 0.005, into the final charge-separated state, Mb(Fe(IV)=O)-Ru2+-BXV3+ (·), which bears an energy more than 1 eV above the ground state and a lifetime (τ > 2 ms) comparable to that of natural photosynthetic reaction center. Photoexcitation of Mb(Zn)-Ru2+ -BXV4+ also gives rise to a vectorial two-step electron- transfer relay with the intermediate CS state, Mb(Zn)-Ru3+-BXV3+ (·), for the main pathway leading to the final CS state, Mb(Zn+)-Ru2+-BXV3+ (·), in a yield of 0.08. Although the driving forces for the recombination of Mb(Fe(IV)=O)-Ru2+-BXV3+ (·) and Mb(Zn+)-Ru2+-BXV3+ (·) are similar (ΔG ≃ 1.30 eV), the recombination rate of the former is at least 102-103-fold slower than that of the latter. By analogy with a related system reported previously, it was considered that back ET from BXV3+ (·) to Mb(Fe(IV)=O) might be coupled to the protonation of Mb(Fe(IV)=O) and governed by the slow interconversion between the metal-oxo form and the proton-activated species, rendering the CS state Mb(Fe(IV)=O)-Ru2+-BXV3+ (·) specially long-lived. Control experiments clearly demonstrated that partial incorporation of the triads into the protein matrix plays a crucial role in regulating the electron-transfer pathway and stabilizing the charge separation state.

Original languageEnglish
Pages (from-to)241-253
Number of pages13
JournalJournal of the American Chemical Society
Volume122
Issue number2
DOIs
Publication statusPublished - Jan 19 2000

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Photosynthetic Reaction Center Complex Proteins
Myoglobin
Protons
Membrane Proteins
Electrons
Proteins
Ligands
Photoexcitation
Chemical potential
Protonation
Photolysis
Porphyrins
Quantum yield
Metals
Ruthenium
Ground state
Positive ions
Lasers
Genetic Recombination
Experiments

All Science Journal Classification (ASJC) codes

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

Cite this

Construction of artificial photosynthetic reaction centers on a protein surface : Vectorial, multistep, and proton-coupled electron transfer for long- lived charge separation. / Hu, Yi Zhen; Tsukiji, Shinya; Shinkai, Seiji; Oishi, Shigero; Hamachi, Itaru.

In: Journal of the American Chemical Society, Vol. 122, No. 2, 19.01.2000, p. 241-253.

Research output: Contribution to journalArticle

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T1 - Construction of artificial photosynthetic reaction centers on a protein surface

T2 - Vectorial, multistep, and proton-coupled electron transfer for long- lived charge separation

AU - Hu, Yi Zhen

AU - Tsukiji, Shinya

AU - Shinkai, Seiji

AU - Oishi, Shigero

AU - Hamachi, Itaru

PY - 2000/1/19

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N2 - Artificial photosynthetic reaction centers have been constructed on a protein surface by cofactor reconstitution, which mimic the function of photosynthetic organisms to convert light energy to chemical potential in the form of long-lived charge-separated states. They feature a ruthenium tris(2,2'-bipyridine) moiety as the sensitizer, which is mechanically linked (i.e., in catenane-type) with a cyclobis(paraquat-p-phenylene) unit (BXV4+, acceptor) and covalently linked with a protoheme or Zn-protoporphyrin (donor) located in the myoglobin pocket. Their cofactors 1 and 2, which are tris(heteroleptic) Ru-bipyridine complexes, were synthesized by sequential coordination of the two different functionalized bipyridine ligands with a readily obtainable precursor [Ru(4,4'-dimethyl-2,2'-bipyridine)Cl3](n) followed by metal insertion; this represents a new efficient synthetic method for tris(heteroleptic) Ru(II) complexes of bidentate polypyridine ligands. Reconstitution of apo-myoglobin (Mb) with 1 and 2 affords the two Mb-based artificial triads, Mb(Fe(III)OH2)-Ru2+-BXV4+ and Mb(Zn)-Ru2+-BXV4+. Laser flash photolysis of the Ru(bpy)3 moiety of Mb(Fe(III)OH2)-Ru2+- BXV4+ in an aqueous solution yields an initial charge-separated state, Mb(Fe(III)OH2)-Ru3+-BXV3+(·), via noncovalent electron transfer, followed by dark electron transfer to generate an intermediate consisting of porphyrin cation radical, Mb(Fe(III·)OH2)-Ru2+-BXV3+(·). Mb(Fe(III ·)OH2)-Ru2+-BXV3+ (·) thus generated is subsequently converted, via a proton-coupled process and with a quantum yield of 0.005, into the final charge-separated state, Mb(Fe(IV)=O)-Ru2+-BXV3+ (·), which bears an energy more than 1 eV above the ground state and a lifetime (τ > 2 ms) comparable to that of natural photosynthetic reaction center. Photoexcitation of Mb(Zn)-Ru2+ -BXV4+ also gives rise to a vectorial two-step electron- transfer relay with the intermediate CS state, Mb(Zn)-Ru3+-BXV3+ (·), for the main pathway leading to the final CS state, Mb(Zn+)-Ru2+-BXV3+ (·), in a yield of 0.08. Although the driving forces for the recombination of Mb(Fe(IV)=O)-Ru2+-BXV3+ (·) and Mb(Zn+)-Ru2+-BXV3+ (·) are similar (ΔG ≃ 1.30 eV), the recombination rate of the former is at least 102-103-fold slower than that of the latter. By analogy with a related system reported previously, it was considered that back ET from BXV3+ (·) to Mb(Fe(IV)=O) might be coupled to the protonation of Mb(Fe(IV)=O) and governed by the slow interconversion between the metal-oxo form and the proton-activated species, rendering the CS state Mb(Fe(IV)=O)-Ru2+-BXV3+ (·) specially long-lived. Control experiments clearly demonstrated that partial incorporation of the triads into the protein matrix plays a crucial role in regulating the electron-transfer pathway and stabilizing the charge separation state.

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