Distribution of the cationic state over the chlorophyll pair of the photosystem II reaction center

Keisuke Saito, Toyokazu Ishida, Miwa Sugiura, Keisuke Kawakami, Yasufumi Umena, Nobuo Kamiya, Jian-Ren Shen, Hiroshi Ishikita

Research output: Contribution to journalArticle

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Abstract

The reaction center chlorophylls a (Chla) of photosystem II (PSII) are composed of six Chla molecules including the special pair Chla P D1/P D2 harbored by the D1/D2 heterodimer. They serve as the ultimate electron abstractors for water oxidation in the oxygen-evolving Mn 4CaO 5 cluster. Using the PSII crystal structure analyzed at 1.9 Å resolution, the redox potentials of P D1/P D2 for one-electron oxidation (E m) were calculated by considering all PSII subunits and the protonation pattern of all titratable residues. The E m(Chla) values were calculated to be 1015-1132 mV for P D1 and 1141-1201 mV for P D2, depending on the protonation state of the Mn 4CaO 5 cluster. The results showed that E m(P D1) was lower than E m(P D2), favoring localization of the charge of the cationic state more on P D1. The P D1 •+/P D2 •+ charge ratio determined by the large-scale QM/MM calculations with the explicit PSII protein environment yielded a P D1 •+/P D2 •+ ratio of ∼80/∼20, which was found to be due to the asymmetry in electrostatic characters of several conserved D1/D2 residue pairs that cause the E m(P D1)/E m(P D2) difference, e.g., D1-Asn181/D2-Arg180, D1-Asn298/D2-Arg294, D1-Asp61/D2-His61, D1-Glu189/D2-Phe188, and D1-Asp170/D2-Phe169. The larger P D1 •+ population than P D2 •+ appears to be an inevitable fate of the intact PSII that possesses water oxidation activity.

Original languageEnglish
Pages (from-to)14379-14388
Number of pages10
JournalJournal of the American Chemical Society
Volume133
Issue number36
DOIs
Publication statusPublished - Sep 14 2011

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Photosystem II Protein Complex
Chlorophyll
Protonation
Oxidation
Electrons
Water
Electrostatics
Static Electricity
Crystal structure
Oxidation-Reduction
Proteins
Molecules
Oxygen
chlorophyll a
Population

ASJC Scopus subject areas

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

Cite this

Distribution of the cationic state over the chlorophyll pair of the photosystem II reaction center. / Saito, Keisuke; Ishida, Toyokazu; Sugiura, Miwa; Kawakami, Keisuke; Umena, Yasufumi; Kamiya, Nobuo; Shen, Jian-Ren; Ishikita, Hiroshi.

In: Journal of the American Chemical Society, Vol. 133, No. 36, 14.09.2011, p. 14379-14388.

Research output: Contribution to journalArticle

Saito, Keisuke ; Ishida, Toyokazu ; Sugiura, Miwa ; Kawakami, Keisuke ; Umena, Yasufumi ; Kamiya, Nobuo ; Shen, Jian-Ren ; Ishikita, Hiroshi. / Distribution of the cationic state over the chlorophyll pair of the photosystem II reaction center. In: Journal of the American Chemical Society. 2011 ; Vol. 133, No. 36. pp. 14379-14388.
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abstract = "The reaction center chlorophylls a (Chla) of photosystem II (PSII) are composed of six Chla molecules including the special pair Chla P D1/P D2 harbored by the D1/D2 heterodimer. They serve as the ultimate electron abstractors for water oxidation in the oxygen-evolving Mn 4CaO 5 cluster. Using the PSII crystal structure analyzed at 1.9 {\AA} resolution, the redox potentials of P D1/P D2 for one-electron oxidation (E m) were calculated by considering all PSII subunits and the protonation pattern of all titratable residues. The E m(Chla) values were calculated to be 1015-1132 mV for P D1 and 1141-1201 mV for P D2, depending on the protonation state of the Mn 4CaO 5 cluster. The results showed that E m(P D1) was lower than E m(P D2), favoring localization of the charge of the cationic state more on P D1. The P D1 •+/P D2 •+ charge ratio determined by the large-scale QM/MM calculations with the explicit PSII protein environment yielded a P D1 •+/P D2 •+ ratio of ∼80/∼20, which was found to be due to the asymmetry in electrostatic characters of several conserved D1/D2 residue pairs that cause the E m(P D1)/E m(P D2) difference, e.g., D1-Asn181/D2-Arg180, D1-Asn298/D2-Arg294, D1-Asp61/D2-His61, D1-Glu189/D2-Phe188, and D1-Asp170/D2-Phe169. The larger P D1 •+ population than P D2 •+ appears to be an inevitable fate of the intact PSII that possesses water oxidation activity.",
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T1 - Distribution of the cationic state over the chlorophyll pair of the photosystem II reaction center

AU - Saito, Keisuke

AU - Ishida, Toyokazu

AU - Sugiura, Miwa

AU - Kawakami, Keisuke

AU - Umena, Yasufumi

AU - Kamiya, Nobuo

AU - Shen, Jian-Ren

AU - Ishikita, Hiroshi

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N2 - The reaction center chlorophylls a (Chla) of photosystem II (PSII) are composed of six Chla molecules including the special pair Chla P D1/P D2 harbored by the D1/D2 heterodimer. They serve as the ultimate electron abstractors for water oxidation in the oxygen-evolving Mn 4CaO 5 cluster. Using the PSII crystal structure analyzed at 1.9 Å resolution, the redox potentials of P D1/P D2 for one-electron oxidation (E m) were calculated by considering all PSII subunits and the protonation pattern of all titratable residues. The E m(Chla) values were calculated to be 1015-1132 mV for P D1 and 1141-1201 mV for P D2, depending on the protonation state of the Mn 4CaO 5 cluster. The results showed that E m(P D1) was lower than E m(P D2), favoring localization of the charge of the cationic state more on P D1. The P D1 •+/P D2 •+ charge ratio determined by the large-scale QM/MM calculations with the explicit PSII protein environment yielded a P D1 •+/P D2 •+ ratio of ∼80/∼20, which was found to be due to the asymmetry in electrostatic characters of several conserved D1/D2 residue pairs that cause the E m(P D1)/E m(P D2) difference, e.g., D1-Asn181/D2-Arg180, D1-Asn298/D2-Arg294, D1-Asp61/D2-His61, D1-Glu189/D2-Phe188, and D1-Asp170/D2-Phe169. The larger P D1 •+ population than P D2 •+ appears to be an inevitable fate of the intact PSII that possesses water oxidation activity.

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