Hydrogen-bond promoted intramolecular electron transfer to photogenerated Ru(III)

A functional mimic of tyrosine(z) and histidine 190 in photosystem II

Licheng Sun, Mark Burkitt, Markus Tamm, Mary Katherine Raymond, Malin Abrahamsson, Denis LeGourriérec, Yves Frapart, Ann Magnuson, Ping Huang Kenéz, Peter Brandt, Anh Tran, Leif Hammarström, Stenbjörn Styring, Björn Åkermark

Research output: Contribution to journalArticle

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Abstract

As a model for redox components on the donor side of photosystem II (PS II) in green plants, a supramolecular complex 4 has been prepared. In this, a ruthenium(II) tris-bipyridyl complex which mimics the function of P680 in PS II, has been covalently linked to a tyrosine unit which bears two hydrogen-bonding substituents, dipicolylamine (dpa) ligands. Our aim is to mimic the interaction between tyrosine(z) and a basic histidine residue, namely His190 in PSII, and also to use the dpa ligands for coordination of manganese. Two different routes for the synthesis of the compound 4 are presented. Its structure was fully characterized by 1H NMR, COSY, NOESY, 13C NMR, IR, and mass spectrometry. 1H NMR and NOESY gave evidence for the existence of intramolecular hydrogen bonding in 4. The interaction between the ruthenium and the substituted tyrosine unit was probed by steady-state and time-resolved emission measurements as well as by chemical oxidation. Flash photolysis and EPR measurements on 4 in the presence of an electron acceptor (methylviologen, MV2+, or cobalt pentaminechloride, Co3+) showed that an intermolecular electron transfer from the excited state of Ru(II) in 4 to the electron acceptor took place, forming Ru(III) and the methylviologen radical MV+· or Co2+. This was followed by intramolecular electron transfer from the substituted tyrosine moiety to the photogenerated Ru(m), regenerating Ru(II) and forming a tyrosyl radical. In water, the radical has a g value of 2.0044, indicative of a deprotonated tyrosyl radical. In acetonitrile, a radical with a g value of 2.0029 was formed, which can be assigned to the tyrosine radical cation. In both solvents the electron transfer is intramolecular with a rate constant κ(ET) > 1 x 107 s-1. This is 2 orders of magnitude greater than the one for a similar compound 3, in which no dpa arm is attached to the tyrosine unit. Therefore the hydrogen bonding between the substituted tyrosine and the dpa arms in 4 is proposed to be responsible for the fast electron transfer. This interaction mimics the proposed His190 and tyrosine(z) interaction in the donor side of PS II.

Original languageEnglish
Pages (from-to)6834-6842
Number of pages9
JournalJournal of the American Chemical Society
Volume121
Issue number29
DOIs
Publication statusPublished - Jul 28 1999

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Photosystem II Protein Complex
Histidine
Tyrosine
Hydrogen
Hydrogen bonds
Electrons
Hydrogen Bonding
Nuclear magnetic resonance
Ruthenium
Ligands
Viridiplantae
Photolysis
2,2'-Dipyridyl
Acetonitrile
Excited states
Manganese
Mass spectrometry
Paramagnetic resonance
Cobalt
Rate constants

ASJC Scopus subject areas

  • Chemistry(all)

Cite this

Hydrogen-bond promoted intramolecular electron transfer to photogenerated Ru(III) : A functional mimic of tyrosine(z) and histidine 190 in photosystem II. / Sun, Licheng; Burkitt, Mark; Tamm, Markus; Raymond, Mary Katherine; Abrahamsson, Malin; LeGourriérec, Denis; Frapart, Yves; Magnuson, Ann; Kenéz, Ping Huang; Brandt, Peter; Tran, Anh; Hammarström, Leif; Styring, Stenbjörn; Åkermark, Björn.

In: Journal of the American Chemical Society, Vol. 121, No. 29, 28.07.1999, p. 6834-6842.

Research output: Contribution to journalArticle

Sun, L, Burkitt, M, Tamm, M, Raymond, MK, Abrahamsson, M, LeGourriérec, D, Frapart, Y, Magnuson, A, Kenéz, PH, Brandt, P, Tran, A, Hammarström, L, Styring, S & Åkermark, B 1999, 'Hydrogen-bond promoted intramolecular electron transfer to photogenerated Ru(III): A functional mimic of tyrosine(z) and histidine 190 in photosystem II', Journal of the American Chemical Society, vol. 121, no. 29, pp. 6834-6842. https://doi.org/10.1021/ja984048c
Sun, Licheng ; Burkitt, Mark ; Tamm, Markus ; Raymond, Mary Katherine ; Abrahamsson, Malin ; LeGourriérec, Denis ; Frapart, Yves ; Magnuson, Ann ; Kenéz, Ping Huang ; Brandt, Peter ; Tran, Anh ; Hammarström, Leif ; Styring, Stenbjörn ; Åkermark, Björn. / Hydrogen-bond promoted intramolecular electron transfer to photogenerated Ru(III) : A functional mimic of tyrosine(z) and histidine 190 in photosystem II. In: Journal of the American Chemical Society. 1999 ; Vol. 121, No. 29. pp. 6834-6842.
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abstract = "As a model for redox components on the donor side of photosystem II (PS II) in green plants, a supramolecular complex 4 has been prepared. In this, a ruthenium(II) tris-bipyridyl complex which mimics the function of P680 in PS II, has been covalently linked to a tyrosine unit which bears two hydrogen-bonding substituents, dipicolylamine (dpa) ligands. Our aim is to mimic the interaction between tyrosine(z) and a basic histidine residue, namely His190 in PSII, and also to use the dpa ligands for coordination of manganese. Two different routes for the synthesis of the compound 4 are presented. Its structure was fully characterized by 1H NMR, COSY, NOESY, 13C NMR, IR, and mass spectrometry. 1H NMR and NOESY gave evidence for the existence of intramolecular hydrogen bonding in 4. The interaction between the ruthenium and the substituted tyrosine unit was probed by steady-state and time-resolved emission measurements as well as by chemical oxidation. Flash photolysis and EPR measurements on 4 in the presence of an electron acceptor (methylviologen, MV2+, or cobalt pentaminechloride, Co3+) showed that an intermolecular electron transfer from the excited state of Ru(II) in 4 to the electron acceptor took place, forming Ru(III) and the methylviologen radical MV+· or Co2+. This was followed by intramolecular electron transfer from the substituted tyrosine moiety to the photogenerated Ru(m), regenerating Ru(II) and forming a tyrosyl radical. In water, the radical has a g value of 2.0044, indicative of a deprotonated tyrosyl radical. In acetonitrile, a radical with a g value of 2.0029 was formed, which can be assigned to the tyrosine radical cation. In both solvents the electron transfer is intramolecular with a rate constant κ(ET) > 1 x 107 s-1. This is 2 orders of magnitude greater than the one for a similar compound 3, in which no dpa arm is attached to the tyrosine unit. Therefore the hydrogen bonding between the substituted tyrosine and the dpa arms in 4 is proposed to be responsible for the fast electron transfer. This interaction mimics the proposed His190 and tyrosine(z) interaction in the donor side of PS II.",
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T1 - Hydrogen-bond promoted intramolecular electron transfer to photogenerated Ru(III)

T2 - A functional mimic of tyrosine(z) and histidine 190 in photosystem II

AU - Sun, Licheng

AU - Burkitt, Mark

AU - Tamm, Markus

AU - Raymond, Mary Katherine

AU - Abrahamsson, Malin

AU - LeGourriérec, Denis

AU - Frapart, Yves

AU - Magnuson, Ann

AU - Kenéz, Ping Huang

AU - Brandt, Peter

AU - Tran, Anh

AU - Hammarström, Leif

AU - Styring, Stenbjörn

AU - Åkermark, Björn

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N2 - As a model for redox components on the donor side of photosystem II (PS II) in green plants, a supramolecular complex 4 has been prepared. In this, a ruthenium(II) tris-bipyridyl complex which mimics the function of P680 in PS II, has been covalently linked to a tyrosine unit which bears two hydrogen-bonding substituents, dipicolylamine (dpa) ligands. Our aim is to mimic the interaction between tyrosine(z) and a basic histidine residue, namely His190 in PSII, and also to use the dpa ligands for coordination of manganese. Two different routes for the synthesis of the compound 4 are presented. Its structure was fully characterized by 1H NMR, COSY, NOESY, 13C NMR, IR, and mass spectrometry. 1H NMR and NOESY gave evidence for the existence of intramolecular hydrogen bonding in 4. The interaction between the ruthenium and the substituted tyrosine unit was probed by steady-state and time-resolved emission measurements as well as by chemical oxidation. Flash photolysis and EPR measurements on 4 in the presence of an electron acceptor (methylviologen, MV2+, or cobalt pentaminechloride, Co3+) showed that an intermolecular electron transfer from the excited state of Ru(II) in 4 to the electron acceptor took place, forming Ru(III) and the methylviologen radical MV+· or Co2+. This was followed by intramolecular electron transfer from the substituted tyrosine moiety to the photogenerated Ru(m), regenerating Ru(II) and forming a tyrosyl radical. In water, the radical has a g value of 2.0044, indicative of a deprotonated tyrosyl radical. In acetonitrile, a radical with a g value of 2.0029 was formed, which can be assigned to the tyrosine radical cation. In both solvents the electron transfer is intramolecular with a rate constant κ(ET) > 1 x 107 s-1. This is 2 orders of magnitude greater than the one for a similar compound 3, in which no dpa arm is attached to the tyrosine unit. Therefore the hydrogen bonding between the substituted tyrosine and the dpa arms in 4 is proposed to be responsible for the fast electron transfer. This interaction mimics the proposed His190 and tyrosine(z) interaction in the donor side of PS II.

AB - As a model for redox components on the donor side of photosystem II (PS II) in green plants, a supramolecular complex 4 has been prepared. In this, a ruthenium(II) tris-bipyridyl complex which mimics the function of P680 in PS II, has been covalently linked to a tyrosine unit which bears two hydrogen-bonding substituents, dipicolylamine (dpa) ligands. Our aim is to mimic the interaction between tyrosine(z) and a basic histidine residue, namely His190 in PSII, and also to use the dpa ligands for coordination of manganese. Two different routes for the synthesis of the compound 4 are presented. Its structure was fully characterized by 1H NMR, COSY, NOESY, 13C NMR, IR, and mass spectrometry. 1H NMR and NOESY gave evidence for the existence of intramolecular hydrogen bonding in 4. The interaction between the ruthenium and the substituted tyrosine unit was probed by steady-state and time-resolved emission measurements as well as by chemical oxidation. Flash photolysis and EPR measurements on 4 in the presence of an electron acceptor (methylviologen, MV2+, or cobalt pentaminechloride, Co3+) showed that an intermolecular electron transfer from the excited state of Ru(II) in 4 to the electron acceptor took place, forming Ru(III) and the methylviologen radical MV+· or Co2+. This was followed by intramolecular electron transfer from the substituted tyrosine moiety to the photogenerated Ru(m), regenerating Ru(II) and forming a tyrosyl radical. In water, the radical has a g value of 2.0044, indicative of a deprotonated tyrosyl radical. In acetonitrile, a radical with a g value of 2.0029 was formed, which can be assigned to the tyrosine radical cation. In both solvents the electron transfer is intramolecular with a rate constant κ(ET) > 1 x 107 s-1. This is 2 orders of magnitude greater than the one for a similar compound 3, in which no dpa arm is attached to the tyrosine unit. Therefore the hydrogen bonding between the substituted tyrosine and the dpa arms in 4 is proposed to be responsible for the fast electron transfer. This interaction mimics the proposed His190 and tyrosine(z) interaction in the donor side of PS II.

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