Mimicking the electron transfer chain in photosystem II with a molecular triad thermodynamically capable of water oxidation

Jackson D. Megiatto, Antaeres Antoniuk-Pablant, Benjamin D. Sherman, Gerdenis Kodis, Miguel Gervaldo, Thomas Moore, Ana Moore, Devens Gust

Research output: Contribution to journalArticle

78 Citations (Scopus)

Abstract

In the photosynthetic photosystem II, electrons are transferred from the manganese-containing oxygen evolving complex (OEC) to the oxidized primary electron-donor chlorophyll P680•+ by a proton-coupled electron transfer process involving a tyrosine-histidine pair. Proton transfer from the tyrosine phenolic group to a histidine nitrogen positions the redox potential of the tyrosine between those of P680•+ and the OEC. We report the synthesis and time-resolved spectroscopic study of a molecular triad that models this electron transfer. The triad consists of a high-potential porphyrin bearing two pentafluorophenyl groups (PF10), a tetracyanoporphyrin electron acceptor (TCNP), and a benzimidazole-phenol secondary electron-donor (Bi-PhOH). Excitation of PF10 in benzonitrile is followed by singlet energy transfer to TCNP (τ = 41 ps), whose excited state decays by photoinduced electron transfer (τ = 830 ps) to yield Bi-PhOH-PF 10 •+-TCNP•-. A second electron transfer reaction follows (τ < 12 ps), giving a final state postulated as BiH+-PhO-PF10-TCNP•-, in which the phenolic proton now resides on benzimidazole. This final state decays with a time constant of 3.8 μs. The triad thus functionally mimics the electron transfers involving the tyrosine-histidine pair in PSII. The final charge-separated state is thermodynamically capable of water oxidation, and its long lifetime suggests the possibility of coupling systems such as this system to water oxidation catalysts for use in artificial photosynthetic fuel production.

Original languageEnglish (US)
Pages (from-to)15578-15583
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume109
Issue number39
DOIs
StatePublished - Sep 25 2012

Fingerprint

Photosystem II Protein Complex
triciribine phosphate
Electrons
Water
Tyrosine
Histidine
Protons
Oxygen
Molecular Models
Energy Transfer
Porphyrins
Chlorophyll
Manganese
Phenol
Oxidation-Reduction
Nitrogen

Keywords

  • Biomimicry
  • Photochemistry

ASJC Scopus subject areas

  • General

Cite this

Mimicking the electron transfer chain in photosystem II with a molecular triad thermodynamically capable of water oxidation. / Megiatto, Jackson D.; Antoniuk-Pablant, Antaeres; Sherman, Benjamin D.; Kodis, Gerdenis; Gervaldo, Miguel; Moore, Thomas; Moore, Ana; Gust, Devens.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 109, No. 39, 25.09.2012, p. 15578-15583.

Research output: Contribution to journalArticle

@article{0d97a078b769494b905e1b333032a62c,
title = "Mimicking the electron transfer chain in photosystem II with a molecular triad thermodynamically capable of water oxidation",
abstract = "In the photosynthetic photosystem II, electrons are transferred from the manganese-containing oxygen evolving complex (OEC) to the oxidized primary electron-donor chlorophyll P680•+ by a proton-coupled electron transfer process involving a tyrosine-histidine pair. Proton transfer from the tyrosine phenolic group to a histidine nitrogen positions the redox potential of the tyrosine between those of P680•+ and the OEC. We report the synthesis and time-resolved spectroscopic study of a molecular triad that models this electron transfer. The triad consists of a high-potential porphyrin bearing two pentafluorophenyl groups (PF10), a tetracyanoporphyrin electron acceptor (TCNP), and a benzimidazole-phenol secondary electron-donor (Bi-PhOH). Excitation of PF10 in benzonitrile is followed by singlet energy transfer to TCNP (τ = 41 ps), whose excited state decays by photoinduced electron transfer (τ = 830 ps) to yield Bi-PhOH-PF 10 •+-TCNP•-. A second electron transfer reaction follows (τ < 12 ps), giving a final state postulated as BiH+-PhO•-PF10-TCNP•-, in which the phenolic proton now resides on benzimidazole. This final state decays with a time constant of 3.8 μs. The triad thus functionally mimics the electron transfers involving the tyrosine-histidine pair in PSII. The final charge-separated state is thermodynamically capable of water oxidation, and its long lifetime suggests the possibility of coupling systems such as this system to water oxidation catalysts for use in artificial photosynthetic fuel production.",
keywords = "Biomimicry, Photochemistry",
author = "Megiatto, {Jackson D.} and Antaeres Antoniuk-Pablant and Sherman, {Benjamin D.} and Gerdenis Kodis and Miguel Gervaldo and Thomas Moore and Ana Moore and Devens Gust",
year = "2012",
month = "9",
day = "25",
doi = "10.1073/pnas.1118348109",
language = "English (US)",
volume = "109",
pages = "15578--15583",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
issn = "0027-8424",
number = "39",

}

TY - JOUR

T1 - Mimicking the electron transfer chain in photosystem II with a molecular triad thermodynamically capable of water oxidation

AU - Megiatto, Jackson D.

AU - Antoniuk-Pablant, Antaeres

AU - Sherman, Benjamin D.

AU - Kodis, Gerdenis

AU - Gervaldo, Miguel

AU - Moore, Thomas

AU - Moore, Ana

AU - Gust, Devens

PY - 2012/9/25

Y1 - 2012/9/25

N2 - In the photosynthetic photosystem II, electrons are transferred from the manganese-containing oxygen evolving complex (OEC) to the oxidized primary electron-donor chlorophyll P680•+ by a proton-coupled electron transfer process involving a tyrosine-histidine pair. Proton transfer from the tyrosine phenolic group to a histidine nitrogen positions the redox potential of the tyrosine between those of P680•+ and the OEC. We report the synthesis and time-resolved spectroscopic study of a molecular triad that models this electron transfer. The triad consists of a high-potential porphyrin bearing two pentafluorophenyl groups (PF10), a tetracyanoporphyrin electron acceptor (TCNP), and a benzimidazole-phenol secondary electron-donor (Bi-PhOH). Excitation of PF10 in benzonitrile is followed by singlet energy transfer to TCNP (τ = 41 ps), whose excited state decays by photoinduced electron transfer (τ = 830 ps) to yield Bi-PhOH-PF 10 •+-TCNP•-. A second electron transfer reaction follows (τ < 12 ps), giving a final state postulated as BiH+-PhO•-PF10-TCNP•-, in which the phenolic proton now resides on benzimidazole. This final state decays with a time constant of 3.8 μs. The triad thus functionally mimics the electron transfers involving the tyrosine-histidine pair in PSII. The final charge-separated state is thermodynamically capable of water oxidation, and its long lifetime suggests the possibility of coupling systems such as this system to water oxidation catalysts for use in artificial photosynthetic fuel production.

AB - In the photosynthetic photosystem II, electrons are transferred from the manganese-containing oxygen evolving complex (OEC) to the oxidized primary electron-donor chlorophyll P680•+ by a proton-coupled electron transfer process involving a tyrosine-histidine pair. Proton transfer from the tyrosine phenolic group to a histidine nitrogen positions the redox potential of the tyrosine between those of P680•+ and the OEC. We report the synthesis and time-resolved spectroscopic study of a molecular triad that models this electron transfer. The triad consists of a high-potential porphyrin bearing two pentafluorophenyl groups (PF10), a tetracyanoporphyrin electron acceptor (TCNP), and a benzimidazole-phenol secondary electron-donor (Bi-PhOH). Excitation of PF10 in benzonitrile is followed by singlet energy transfer to TCNP (τ = 41 ps), whose excited state decays by photoinduced electron transfer (τ = 830 ps) to yield Bi-PhOH-PF 10 •+-TCNP•-. A second electron transfer reaction follows (τ < 12 ps), giving a final state postulated as BiH+-PhO•-PF10-TCNP•-, in which the phenolic proton now resides on benzimidazole. This final state decays with a time constant of 3.8 μs. The triad thus functionally mimics the electron transfers involving the tyrosine-histidine pair in PSII. The final charge-separated state is thermodynamically capable of water oxidation, and its long lifetime suggests the possibility of coupling systems such as this system to water oxidation catalysts for use in artificial photosynthetic fuel production.

KW - Biomimicry

KW - Photochemistry

UR - http://www.scopus.com/inward/record.url?scp=84866853538&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84866853538&partnerID=8YFLogxK

U2 - 10.1073/pnas.1118348109

DO - 10.1073/pnas.1118348109

M3 - Article

VL - 109

SP - 15578

EP - 15583

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 39

ER -