Similarity between oxygen evolution in photosystem II and oxygen reduction in cytochrome c oxidase via proton coupled electron transfers. A unified view of the oxygenic life from four electron oxidation–reduction reactions

Yamaguchi, Kizashi; Miyagawa, Koichi; Shoji, Mitsuo; Isobe, Hiroshi; Kawakami, Takashi

doi:https://doi.org/10.1007/s43630-024-00648-w

Similarity between oxygen evolution in photosystem II and oxygen reduction in cytochrome c oxidase via proton coupled electron transfers. A unified view of the oxygenic life from four electron oxidation–reduction reactions

Yamaguchi, Kizashi; Miyagawa, Koichi; Shoji, Mitsuo et al.

Photochemical and Photobiological Sciences, 2024, 23, 2133-2155

Number of Access:790（2025-08-14 15:05 Counts）

Identifier to cite or link to this item: https://hdl.handle.net/11094/100313

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Title	Similarity between oxygen evolution in photosystem II and oxygen reduction in cytochrome c oxidase via proton coupled electron transfers. A unified view of the oxygenic life from four electron oxidation–reduction reactions
Creator	NRID 1000080029537 1000080029537 Scopus Author ID 7405929506 7405929506 ORCID 0000-0002-4411-7425 0000-0002-4411-7425 CreatorName Yamaguchi, Kizashi
	CreatorName Miyagawa, Koichi
	NRID 1000000593550 1000000593550 CreatorName Shoji, Mitsuo
	NRID 1000000379281 1000000379281 CreatorName Isobe, Hiroshi
	NRID 1000030321748 1000030321748 researchmap permalink kawakamitakashi kawakamitakashi Scopus Author ID 7401566433 7401566433 CreatorName Kawakami, Takashi
Subject	Broken symmetry
	Cytochrome c oxidase
	Photosystem II
	Proton transfer coupled electron transfer
	Strongly correlated electron systems
Description	The version of record of this article, first published in Photochemical and Photobiological Sciences, is available online at Publisher’s website: https://doi.org/10.1007/s43630-024-00648-w.
Abstract	Basic concepts and theoretical foundations of broken symmetry (BS) and post BS methods for strongly correlated electron systems (SCES) such as electron-transfer (ET) diradical, multi-center polyradicals with spin frustration are described systematically to elucidate structures, bonding and reactivity of the high-valent transition metal oxo bonds in metalloenzymes: photosystem II (PSII) and cytochrome c oxidase (CcO). BS hybrid DFT (HDFT) and DLPNO coupled-cluster (CC) SD(T0) computations are performed to elucidate electronic and spin states of CaMn4Ox cluster in the key step for oxygen evolution, namely S4 [S3 with Mn(IV) = O + Tyr161-O radical] state of PSII and PM [Fe(IV) = O + HO-Cu(II) + Tyr161-O radical] step for oxygen reduction in CcO. The cycle of water oxidation catalyzed by the CaMn4Ox cluster in PSII and the cycle of oxygen reduction catalyzed by the CuA-Fea-Fea3-CuB cluster in CcO are examined on the theoretical grounds, elucidating similar concerted and/or stepwise proton transfer coupled electron transfer (PT-ET) processes for the four-electron oxidation in PSII and four-electron reduction in CcO. Interplay between theory and experiments have revealed that three electrons in the metal sites and one electron in tyrosine radical site are characteristic for PT-ET in these biological redox reaction systems, indicating no necessity of harmful Mn(V) = O and Fe(V) = O bonds with strong oxyl-radical character. Implications of the computational results are discussed in relation to design of artificial systems consisted of earth abundant transition metals for water oxidation.
Publisher	Springer Nature
Source Title	Photochemical and Photobiological Sciences
Volume (Issue)	23
Page	2133-2155
Date of Issued	2024-12-01
Language	English
Handle URL	https://hdl.handle.net/11094/100313
PISSN	1474905X
eISSN	14749092
Relation.isIdenticalTo	DOI (Publisher Version) https://doi.org/10.1007/s43630-024-00648-w
Access Rights	open access
CopyRight	This article is licensed under a Creative Commons Attribution 4.0 International License.
oaire:version	Version of Record
Category	学術雑誌論文 Journal Article

Resource Type	journal article
Local Type	Journal Article
DCTERMS.bibliographicCitation	Photochemical and Photobiological Sciences. 2024, 23, p. 2133-2155
DC.title	Similarity between oxygen evolution in photosystem II and oxygen reduction in cytochrome c oxidase via proton coupled electron transfers. A unified view of the oxygenic life from four electron oxidation–reduction reactions
DC.creator	Yamaguchi, Kizashi
	Miyagawa, Koichi
	Shoji, Mitsuo
	Isobe, Hiroshi
	Kawakami, Takashi
DC.publisher	Springer Nature
DC.language' scheme='DCTERMS.RFC1766	English
DCTERMS.issued' scheme='DCTERMS.W3CDTF	2024-12-01
DC.identifier	https://doi.org/10.1007/s43630-024-00648-w
DC.subject	Broken symmetry
	Cytochrome c oxidase
	Photosystem II
	Proton transfer coupled electron transfer
	Strongly correlated electron systems
DC.description	The version of record of this article, first published in Photochemical and Photobiological Sciences, is available online at Publisher’s website: https://doi.org/10.1007/s43630-024-00648-w.
DCTERMS.abstract	Basic concepts and theoretical foundations of broken symmetry (BS) and post BS methods for strongly correlated electron systems (SCES) such as electron-transfer (ET) diradical, multi-center polyradicals with spin frustration are described systematically to elucidate structures, bonding and reactivity of the high-valent transition metal oxo bonds in metalloenzymes: photosystem II (PSII) and cytochrome c oxidase (CcO). BS hybrid DFT (HDFT) and DLPNO coupled-cluster (CC) SD(T0) computations are performed to elucidate electronic and spin states of CaMn4Ox cluster in the key step for oxygen evolution, namely S4 [S3 with Mn(IV) = O + Tyr161-O radical] state of PSII and PM [Fe(IV) = O + HO-Cu(II) + Tyr161-O radical] step for oxygen reduction in CcO. The cycle of water oxidation catalyzed by the CaMn4Ox cluster in PSII and the cycle of oxygen reduction catalyzed by the CuA-Fea-Fea3-CuB cluster in CcO are examined on the theoretical grounds, elucidating similar concerted and/or stepwise proton transfer coupled electron transfer (PT-ET) processes for the four-electron oxidation in PSII and four-electron reduction in CcO. Interplay between theory and experiments have revealed that three electrons in the metal sites and one electron in tyrosine radical site are characteristic for PT-ET in these biological redox reaction systems, indicating no necessity of harmful Mn(V) = O and Fe(V) = O bonds with strong oxyl-radical character. Implications of the computational results are discussed in relation to design of artificial systems consisted of earth abundant transition metals for water oxidation.
DC.rights	This article is licensed under a Creative Commons Attribution 4.0 International License.
DC.format	100313
citation_title	Similarity between oxygen evolution in photosystem II and oxygen reduction in cytochrome c oxidase via proton coupled electron transfers. A unified view of the oxygenic life from four electron oxidation–reduction reactions
citation_author	Yamaguchi, Kizashi
	Miyagawa, Koichi
	Shoji, Mitsuo
	Isobe, Hiroshi
	Kawakami, Takashi
citation_publisher	Springer Nature
citation_language	English
citation_date	2024-12-01
citation_journal_title	Photochemical and Photobiological Sciences
citation_volume	23
citation_firstpage	2133
citation_lastpage	2155
citation_doi	https://doi.org/10.1007/s43630-024-00648-w
citation_public_url	https://hdl.handle.net/11094/100313

Similarity between oxygen evolution in photosystem II and oxygen reduction in cytochrome c oxidase via proton coupled electron transfers. A unified view of the oxygenic life from four electron oxidation–reduction reactions

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