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Effects of Dynamical Degrees of Freedom on Magnetic Compass Sensitivity: A Comparison of Plant and Avian Cryptochromes

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    Effects of Dynamical Degrees of Freedom on Magnetic Compass Sensitivity: A Comparison of Plant and Avian Cryptochromes
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    Journal of the American Chemical Society

    Cite this: J. Am. Chem. Soc. 2022, 144, 50, 22902–22914
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    https://doi.org/10.1021/jacs.2c06233
    Published December 2, 2022
    Copyright © 2022 American Chemical Society
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    Abstract

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    The magnetic compass of migratory birds is thought to rely on a radical pair reaction inside the blue-light photoreceptor protein cryptochrome. The sensitivity of such a sensor to weak external magnetic fields is determined by a variety of magnetic interactions, including electron-nuclear hyperfine interactions. Here, we investigate the implications of thermal motion, focusing on fluctuations in the dihedral and librational angles of flavin adenine dinucleotide (FAD) and tryptophan (Trp) radicals in cryptochrome 4a from European robin (Erithacus rubecula, ErCry4a) and pigeon (Columba livia, ClCry4a) and cryptochrome 1 from the plant Arabidopsis thaliana (AtCry1). Molecular dynamics simulations and density functional theory-derived hyperfine interactions are used to calculate the quantum yield of radical pair recombination dependent on the direction of the geomagnetic field. This quantity and various dynamical parameters are compared for [FAD•– Trp•+] in ErCry4a, ClCry4a, and AtCry1, with TrpC or TrpD being the third and fourth components of the tryptophan triad/tetrad in the respective proteins. We find that (i) differences in the average dihedral angles in the radical pairs are small, (ii) the librational motions of TrpC•+ in the avian cryptochromes are appreciably smaller than in AtCry1, (iii) the rapid vibrational motions of the radicals leading to strong fluctuations in the hyperfine couplings affect the spin dynamics depending on the usage of instantaneous or time-averaged interactions. Future investigations of radical pair compass sensitivity should therefore not be based on single snapshots of the protein structure but should include the ensemble properties of the hyperfine interactions.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/jacs.2c06233.

    • Exemplary input files for the hyperfine and quantum yield calculations and supporting theoretical methods used in the present investigation; distributions of librational and dihedral angles; and results of (additional) hyperfine coupling and spin dynamics calculations (PDF)

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    This article is cited by 17 publications.

    1. Marta Majewska, Maja Hanić, Rabea Bartölke, Jessica Schmidt, Justyna Bożek, Luca Gerhards, Henrik Mouritsen, Karl-Wilhelm Koch, Ilia A. Solov’yov, Izabella Brand. European Robin Cryptochrome-4a Associates with Lipid Bilayers in an Ordered Manner, Fulfilling a Molecular-Level Condition for Magnetoreception. ACS Chemical Biology 2025, 20 (3) , 592-606. https://doi.org/10.1021/acschembio.4c00576
    2. Lewis M. Antill, Emil Vatai. RadicalPy: A Tool for Spin Dynamics Simulations. Journal of Chemical Theory and Computation 2024, 20 (21) , 9488-9499. https://doi.org/10.1021/acs.jctc.4c00887
    3. Gediminas Jurgis Pažėra, Thomas P. Fay, Ilia A. Solov’yov, P. J. Hore, Luca Gerhards. Spin Dynamics of Radical Pairs Using the Stochastic Schrödinger Equation in MolSpin. Journal of Chemical Theory and Computation 2024, 20 (19) , 8412-8421. https://doi.org/10.1021/acs.jctc.4c00361
    4. Andrey V. Solov’yov, Alexey V. Verkhovtsev, Nigel J. Mason, Richard A. Amos, Ilko Bald, Gérard Baldacchino, Brendan Dromey, Martin Falk, Juraj Fedor, Luca Gerhards, Michael Hausmann, Georg Hildenbrand, Miloš Hrabovský, Stanislav Kadlec, Jaroslav Kočišek, Franck Lépine, Siyi Ming, Andrew Nisbet, Kate Ricketts, Leo Sala, Thomas Schlathölter, Andrew E. H. Wheatley, Ilia A. Solov’yov. Condensed Matter Systems Exposed to Radiation: Multiscale Theory, Simulations, and Experiment. Chemical Reviews 2024, 124 (13) , 8014-8129. https://doi.org/10.1021/acs.chemrev.3c00902
    5. Fabian Schuhmann, Jessica L. Ramsay, Daniel R. Kattnig, Ilia A. Solov’yov. Structural Rearrangements of Pigeon Cryptochrome 4 Undergoing a Complete Redox Cycle. The Journal of Physical Chemistry B 2024, 128 (16) , 3844-3855. https://doi.org/10.1021/acs.jpcb.4c00424
    6. Jessica L. Ramsay, Fabian Schuhmann, Ilia A. Solov’yov, Daniel R. Kattnig. Cryptochrome magnetoreception: Time course of photoactivation from non-equilibrium coarse-grained molecular dynamics. Computational and Structural Biotechnology Journal 2024, 26 , 58-69. https://doi.org/10.1016/j.csbj.2024.11.001
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    8. Matt C. J. Denton, Luke D. Smith, Wenhao Xu, Jodeci Pugsley, Amelia Toghill, Daniel R. Kattnig. Magnetosensitivity of tightly bound radical pairs in cryptochrome is enabled by the quantum Zeno effect. Nature Communications 2024, 15 (1) https://doi.org/10.1038/s41467-024-55124-x
    9. Pedro H. Alvarez, Luca Gerhards, Ilia A. Solov’yov, Marcos C. de Oliveira. Quantum phenomena in biological systems. Frontiers in Quantum Science and Technology 2024, 3 https://doi.org/10.3389/frqst.2024.1466906
    10. Gesa Grüning, Luca Gerhards, Siu Y. Wong, Daniel R. Kattnig, Ilia A. Solov'yov. The Effect of Spin Relaxation on Magnetic Compass Sensitivity in ErCry4a. ChemPhysChem 2024, 25 (19) https://doi.org/10.1002/cphc.202400129
    11. Jiate Luo, Philip Benjamin, Luca Gerhards, Hannah J. Hogben, P. J. Hore. Orientation of birds in radiofrequency fields in the absence of the Earth’s magnetic field: a possible test for the radical pair mechanism of magnetoreception. Journal of The Royal Society Interface 2024, 21 (217) https://doi.org/10.1098/rsif.2024.0133
    12. Luke D Smith, Jonas Glatthard, Farhan T Chowdhury, Daniel R Kattnig. On the optimality of the radical-pair quantum compass. Quantum Science and Technology 2024, 9 (3) , 035041. https://doi.org/10.1088/2058-9565/ad48b4
    13. Ju-Zhao Liu, Lu Wang, Li-Jie Jiang, Hong-Chang Lyu, Qiang Yuan, Guang-Fu Wang, Yu-Jie Fu, Qi Cui. In sight the behavior of natural Bletilla striata polysaccharide hydrocolloids by molecular dynamics method. International Journal of Biological Macromolecules 2024, 266 , 131245. https://doi.org/10.1016/j.ijbiomac.2024.131245
    14. Thawatchai Thoradit, Kanjana Thongyoo, Khwanchai Kamoltheptawin, Lalin Tunprasert, Mohamed A. El-Esawi, Blanche Aguida, Nathalie Jourdan, Kittisak Buddhachat, Marootpong Pooam. Cryptochrome and quantum biology: unraveling the mysteries of plant magnetoreception. Frontiers in Plant Science 2023, 14 https://doi.org/10.3389/fpls.2023.1266357
    15. Luca Gerhards, Claus Nielsen, Daniel R. Kattnig, P. J. Hore, Ilia A. Solov'yov. Modeling spin relaxation in complex radical systems using MolSpin . Journal of Computational Chemistry 2023, 44 (19) , 1704-1714. https://doi.org/10.1002/jcc.27120
    16. Jessica L. Ramsay, Daniel R. Kattnig. Magnetoreception in cryptochrome enabled by one-dimensional radical motion. AVS Quantum Science 2023, 5 (2) https://doi.org/10.1116/5.0142227
    17. Jörg Matysik, Luca Gerhards, Tobias Theiss, Lisa Timmermann, Patrick Kurle-Tucholski, Guzel Musabirova, Ruonan Qin, Frank Ortmann, Ilia A. Solov’yov, Tanja Gulder. Spin Dynamics of Flavoproteins. International Journal of Molecular Sciences 2023, 24 (9) , 8218. https://doi.org/10.3390/ijms24098218
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    Journal of the American Chemical Society

    Cite this: J. Am. Chem. Soc. 2022, 144, 50, 22902–22914
    Click to copy citationCitation copied!
    https://doi.org/10.1021/jacs.2c06233
    Published December 2, 2022
    Copyright © 2022 American Chemical Society
    Request reuse permissions

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