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Orientations and water dynamics of photoinduced secondary charge-separated states for magnetoreception by cryptochrome

In the biological magnetic compass, blue-light photoreceptor protein of cryptochrome is thought to conduct the sensing of the Earth’s magnetic field by photoinduced sequential long-range charge-separation (CS) through a cascade of tryptophan residues, W(A)(H), W(B)(H) and W(C)(H). Mechanism of gener...

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Autores principales: Hamada, Misato, Iwata, Tatsuya, Fuki, Masaaki, Kandori, Hideki, Weber, Stefan, Kobori, Yasuhiro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9814139/
https://www.ncbi.nlm.nih.gov/pubmed/36697801
http://dx.doi.org/10.1038/s42004-021-00573-4
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author Hamada, Misato
Iwata, Tatsuya
Fuki, Masaaki
Kandori, Hideki
Weber, Stefan
Kobori, Yasuhiro
author_facet Hamada, Misato
Iwata, Tatsuya
Fuki, Masaaki
Kandori, Hideki
Weber, Stefan
Kobori, Yasuhiro
author_sort Hamada, Misato
collection PubMed
description In the biological magnetic compass, blue-light photoreceptor protein of cryptochrome is thought to conduct the sensing of the Earth’s magnetic field by photoinduced sequential long-range charge-separation (CS) through a cascade of tryptophan residues, W(A)(H), W(B)(H) and W(C)(H). Mechanism of generating the weak-field sensitive radical pair (RP) is poorly understood because geometries, electronic couplings and their modulations by molecular motion have not been investigated in the secondary CS states generated prior to the terminal RP states. In this study, water dynamics control of the electronic coupling is revealed to be a key concept for sensing the direction of weak magnetic field. Geometry and exchange coupling (singlet–triplet energy gap: 2J) of photoinduced secondary CS states composed of flavin adenine dinucleotide radical anion (FAD(−•)) and radical cation W(B)(H)(+•) in the cryptochrome DASH from Xenopus laevis were clarified by time-resolved electron paramagnetic resonance. We found a time-dependent energetic disorder in 2J and was interpreted by a trap CS state capturing one reorientated water molecule at 120 K. Enhanced electron-tunneling by water-libration was revealed for the terminal charge-separation event at elevated temperature. This highlights importance of optimizing the electronic coupling for regulation of the anisotropic RP yield on the possible magnetic compass senses.
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spelling pubmed-98141392023-01-10 Orientations and water dynamics of photoinduced secondary charge-separated states for magnetoreception by cryptochrome Hamada, Misato Iwata, Tatsuya Fuki, Masaaki Kandori, Hideki Weber, Stefan Kobori, Yasuhiro Commun Chem Article In the biological magnetic compass, blue-light photoreceptor protein of cryptochrome is thought to conduct the sensing of the Earth’s magnetic field by photoinduced sequential long-range charge-separation (CS) through a cascade of tryptophan residues, W(A)(H), W(B)(H) and W(C)(H). Mechanism of generating the weak-field sensitive radical pair (RP) is poorly understood because geometries, electronic couplings and their modulations by molecular motion have not been investigated in the secondary CS states generated prior to the terminal RP states. In this study, water dynamics control of the electronic coupling is revealed to be a key concept for sensing the direction of weak magnetic field. Geometry and exchange coupling (singlet–triplet energy gap: 2J) of photoinduced secondary CS states composed of flavin adenine dinucleotide radical anion (FAD(−•)) and radical cation W(B)(H)(+•) in the cryptochrome DASH from Xenopus laevis were clarified by time-resolved electron paramagnetic resonance. We found a time-dependent energetic disorder in 2J and was interpreted by a trap CS state capturing one reorientated water molecule at 120 K. Enhanced electron-tunneling by water-libration was revealed for the terminal charge-separation event at elevated temperature. This highlights importance of optimizing the electronic coupling for regulation of the anisotropic RP yield on the possible magnetic compass senses. Nature Publishing Group UK 2021-09-30 /pmc/articles/PMC9814139/ /pubmed/36697801 http://dx.doi.org/10.1038/s42004-021-00573-4 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Hamada, Misato
Iwata, Tatsuya
Fuki, Masaaki
Kandori, Hideki
Weber, Stefan
Kobori, Yasuhiro
Orientations and water dynamics of photoinduced secondary charge-separated states for magnetoreception by cryptochrome
title Orientations and water dynamics of photoinduced secondary charge-separated states for magnetoreception by cryptochrome
title_full Orientations and water dynamics of photoinduced secondary charge-separated states for magnetoreception by cryptochrome
title_fullStr Orientations and water dynamics of photoinduced secondary charge-separated states for magnetoreception by cryptochrome
title_full_unstemmed Orientations and water dynamics of photoinduced secondary charge-separated states for magnetoreception by cryptochrome
title_short Orientations and water dynamics of photoinduced secondary charge-separated states for magnetoreception by cryptochrome
title_sort orientations and water dynamics of photoinduced secondary charge-separated states for magnetoreception by cryptochrome
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9814139/
https://www.ncbi.nlm.nih.gov/pubmed/36697801
http://dx.doi.org/10.1038/s42004-021-00573-4
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