Pair your accounts.

Export articles to Mendeley

Get article recommendations from ACS based on references in your Mendeley library.

Pair your accounts.

Export articles to Mendeley

Get article recommendations from ACS based on references in your Mendeley library.

You’ve supercharged your research process with ACS and Mendeley!

STEP 1:
Click to create an ACS ID

Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

MENDELEY PAIRING EXPIRED
Your Mendeley pairing has expired. Please reconnect
ACS Publications. Most Trusted. Most Cited. Most Read
Early Photocycle of Slr1694 Blue-Light Using Flavin Photoreceptor Unraveled through Adiabatic Excited-State Quantum Mechanical/Molecular Mechanical Dynamics

OR SEARCH CITATIONS

My Activity
Publications

Figure 1Loading Img
Download Hi-Res ImageDownload to MS-PowerPointCite This:J. Am. Chem. Soc. 2019, 141, 51, 20470-20479
    Article

    Early Photocycle of Slr1694 Blue-Light Using Flavin Photoreceptor Unraveled through Adiabatic Excited-State Quantum Mechanical/Molecular Mechanical Dynamics
    Click to copy article linkArticle link copied!

    Other Access OptionsSupporting Information (1)

    Journal of the American Chemical Society

    Cite this: J. Am. Chem. Soc. 2019, 141, 51, 20470–20479
    Click to copy citationCitation copied!
    https://doi.org/10.1021/jacs.9b11196
    Published November 19, 2019
    Copyright © 2019 American Chemical Society
    Request reuse permissions

    Abstract

    Click to copy section linkSection link copied!
    Abstract Image

    Blue-light using flavin (BLUF) photoreceptor proteins are essential to many biological processes and are attractive candidates for use in optogenetics. To understand the photocycle mechanism in the Slr1694 BLUF photoreceptor, adiabatic excited-state quantum mechanical/molecular mechanical (QM/MM) molecular dynamics simulations are performed using Tamm–Dancoff time-dependent density functional theory. These simulations elucidate the roles of protein dynamics, conformational changes, and electrostatics. After photoexcitation to a locally excited state of the flavin, protein reorganization drives electron transfer from Tyr8 to the flavin. The movement of certain charged residues and a decrease in the distance between Tyr8 and the flavin are found to play important roles in facilitating this charge transfer. The formation of this charge-transfer state drives sequential double proton transfer: Tyr8 transfers a proton to the intervening Gln50, which then relays a second proton to the flavin. Although the second proton transfer involves the formation of a singlet diradical ground state, which requires multireference methods, the photocycle dynamics can be continued in an approximate manner by switching to a spin-flip approach. The resulting trajectories trace out the mechanism of photoinduced proton-coupled electron transfer (PCET) in the Slr1694 BLUF photocycle. Propagating the trajectories beyond the PCET reaction identifies possible pathways involving different tautomers of Gln50 that will eventually lead to the light-adapted state. These simulations provide insights into the nonequilibrium dynamics of photoinduced PCET in the Slr1694 BLUF photocycle that have not been attainable with previous simulations.

    Copyright © 2019 American Chemical Society

    Subjects

    what are subjects

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. Add or change your institution or let them know you’d like them to include access.

    Supporting Information

    Click to copy section linkSection link copied!

    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/jacs.9b11196.

    • Benchmarking of DFT functionals; schematic of local QM heating and relaxation procedure; temperature distribution after local heating and QM/MM relaxation; figures depicting time evolution of electrostatic potential, electron donor–acceptor distances, residue contributions to electrostatic potential, and double proton transfer after charge transfer; and theoretical analysis of physical factors governing charge transfer, including Figures S1–S15 (PDF)

    Terms & Conditions

    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    Click to copy section linkSection link copied!

    This article is cited by 32 publications.

    1. Mohammad Pabel Kabir, Paulami Ghosh, Samer Gozem. Electronic Structure Methods for Simulating Flavin’s Spectroscopy and Photophysics: Comparison of Multi-reference, TD-DFT, and Single-Reference Wave Function Methods. The Journal of Physical Chemistry B 2024, 128 (31) , 7545-7557. https://doi.org/10.1021/acs.jpcb.4c03748
    2. Xiu-Wen Kang, Kailin Wang, Xiaofan Zhang, Dongping Zhong, Bei Ding. Elementary Reactions in the Functional Triads of the Blue-Light Photoreceptor BLUF Domain. The Journal of Physical Chemistry B 2024, 128 (9) , 2065-2075. https://doi.org/10.1021/acs.jpcb.3c07988
    3. Tomoyasu Noji, Hiroyuki Tamura, Hiroshi Ishikita, Keisuke Saito. Difference in the Charge-Separation Energetics between Distinct Conformers in the PixD Photoreceptor. The Journal of Physical Chemistry B 2023, 127 (48) , 10351-10359. https://doi.org/10.1021/acs.jpcb.3c06483
    4. Takumi Nakanishi, Yuta Hori, Yasuteru Shigeta, Hiroyasu Sato, Ryoji Kiyanagi, Koji Munakata, Takashi Ohhara, Atsushi Okazawa, Rintaro Shimada, Akira Sakamoto, Osamu Sato. Development of an Iron(II) Complex Exhibiting Thermal- and Photoinduced Double Proton-Transfer-Coupled Spin Transition in a Short Hydrogen Bond. Journal of the American Chemical Society 2023, 145 (35) , 19177-19181. https://doi.org/10.1021/jacs.3c06323
    5. Shaima Hashem, Giovanni Battista Alteri, Lorenzo Cupellini, Benedetta Mennucci. Integrated Computational Study of the Light-Activated Structure of the AppA BLUF Domain and Its Spectral Signatures. The Journal of Physical Chemistry A 2023, 127 (23) , 5065-5074. https://doi.org/10.1021/acs.jpca.3c02385
    6. Zijing Chen, Xiu-Wen Kang, Yalin Zhou, Zhongneng Zhou, Siwei Tang, Shuhua Zou, Kailin Wang, Jiulong Huang, Bei Ding, Dongping Zhong. Dissecting the Ultrafast Stepwise Bidirectional Proton Relay in a Blue-Light Photoreceptor. Journal of the American Chemical Society 2023, 145 (6) , 3394-3400. https://doi.org/10.1021/jacs.2c10206
    7. Patrizia Mazzeo, Shaima Hashem, Filippo Lipparini, Lorenzo Cupellini, Benedetta Mennucci. Fast Method for Excited-State Dynamics in Complex Systems and Its Application to the Photoactivation of a Blue Light Using Flavin Photoreceptor. The Journal of Physical Chemistry Letters 2023, 14 (5) , 1222-1229. https://doi.org/10.1021/acs.jpclett.2c03797
    8. Yusaku Hontani, Jennifer Mehlhorn, Tatiana Domratcheva, Sebastian Beck, Miroslav Kloz, Peter Hegemann, Tilo Mathes, John T. M. Kennis. Spectroscopic and Computational Observation of Glutamine Tautomerization in the Blue Light Sensing Using Flavin Domain Photoreaction. Journal of the American Chemical Society 2023, 145 (2) , 1040-1052. https://doi.org/10.1021/jacs.2c10621
    9. Shunrou Tokonami, Morihiko Onose, Yusuke Nakasone, Masahide Terazima. Slow Conformational Changes of Blue Light Sensor BLUF Proteins in Milliseconds. Journal of the American Chemical Society 2022, 144 (9) , 4080-4090. https://doi.org/10.1021/jacs.1c13121
    10. Tomotsumi Fujisawa, Shinji Masuda, Satoshi Takeuchi, Tahei Tahara. Femtosecond Time-Resolved Absorption Study of Signaling State of a BLUF Protein PixD from the Cyanobacterium Synechocystis: Hydrogen-Bond Rearrangement Completes during Forward Proton-Coupled Electron Transfer. The Journal of Physical Chemistry B 2021, 125 (44) , 12154-12165. https://doi.org/10.1021/acs.jpcb.1c05957
    11. Maria G. Khrenova, Anna M. Kulakova, Alexander V. Nemukhin. Light-Induced Change of Arginine Conformation Modulates the Rate of Adenosine Triphosphate to Cyclic Adenosine Monophosphate Conversion in the Optogenetic System Containing Photoactivated Adenylyl Cyclase. Journal of Chemical Information and Modeling 2021, 61 (3) , 1215-1225. https://doi.org/10.1021/acs.jcim.0c01308
    12. Felipe Curtolo, Guilherme M. Arantes. Mechanisms for Flavin-Mediated Oxidation: Hydride or Hydrogen-Atom Transfer?. Journal of Chemical Information and Modeling 2020, 60 (12) , 6282-6287. https://doi.org/10.1021/acs.jcim.0c00945
    13. Yalin Zhou, Siwei Tang, Zijing Chen, Zhongneng Zhou, Jiulong Huang, Xiu-Wen Kang, Shuhua Zou, Bingyao Wang, Tianyi Zhang, Bei Ding, Dongping Zhong. Origin of the multi-phasic quenching dynamics in the BLUF domains across the species. Nature Communications 2024, 15 (1) https://doi.org/10.1038/s41467-023-44565-5
    14. Yalin Zhou, Xiu-Wen Kang, Zhongneng Zhou, Zijing Chen, Shuhua Zou, Siwei Tang, Bingyao Wang, Kailin Wang, Dongping Zhong, Bei Ding. Unified Mechanism of Light-state BLUF Domain Photocycles by Capturing Proton Relay Intermediates. Ultrafast Science 2024, https://doi.org/10.34133/ultrafastscience.0072
    15. Jinnette Tolentino Collado, Emoke Bodis, Jonatan Pasitka, Mihaly Szucs, Zsuzsanna Fekete, Nikolett Kis-Bicskei, Elek Telek, Kinga Pozsonyi, Sofia M. Kapetanaki, Greg Greetham, Peter J. Tonge, Stephen R. Meech, Andras Lukacs. Single Amino Acid Mutation Decouples Photochemistry of the BLUF Domain from the Enzymatic Function of OaPAC and Drives the Enzyme to a Switched-on State. Journal of Molecular Biology 2024, 436 (5) , 168312. https://doi.org/10.1016/j.jmb.2023.168312
    16. Giacomo Salvadori, Patrizia Mazzeo, Davide Accomasso, Lorenzo Cupellini, Benedetta Mennucci. Deciphering Photoreceptors Through Atomistic Modeling from Light Absorption to Conformational Response. Journal of Molecular Biology 2024, 436 (5) , 168358. https://doi.org/10.1016/j.jmb.2023.168358
    17. Xiang­-Yang Liu, Wei-Hai Fang, Ganglong Cui. Photochemistry of Biological Systems: Excited-State Electronic Structure Calculations and Nonadiabatic Dynamics Simulations with QM/MM Methods. 2024, 345-384. https://doi.org/10.1016/B978-0-12-821978-2.00047-7
    18. Michele Nottoli, Mattia Bondanza, Patrizia Mazzeo, Lorenzo Cupellini, Carles Curutchet, Daniele Loco, Louis Lagardère, Jean‐Philip Piquemal, Benedetta Mennucci, Filippo Lipparini. QM / AMOEBA description of properties and dynamics of embedded molecules. WIREs Computational Molecular Science 2023, 13 (6) https://doi.org/10.1002/wcms.1674
    19. Yusuke Nakasone, Hiroto Murakami, Shunrou Tokonami, Takashi Oda, Masahide Terazima. Time-resolved study on signaling pathway of photoactivated adenylate cyclase and its nonlinear optical response. Journal of Biological Chemistry 2023, 299 (11) , 105285. https://doi.org/10.1016/j.jbc.2023.105285
    20. Carolina Ramírez Martínez, Leonardo S. Gómez-Pérez, Alberto Ordaz, Ana Laura Torres-Huerta, Aurora Antonio-Perez. Current Trends of Bacterial and Fungal Optoproteins for Novel Optical Applications. International Journal of Molecular Sciences 2023, 24 (19) , 14741. https://doi.org/10.3390/ijms241914741
    21. Katalin Raics, Katalin Pirisi, Bo Zhuang, Zsuzsanna Fekete, Nikolett Kis-Bicskei, Ildiko Pecsi, Kinga Pozsonyi Ujfalusi, Elek Telek, Yin Li, Jinnette Tolentino Collado, Peter J. Tonge, Stephen R. Meech, Marten H. Vos, Emoke Bodis, Andras Lukacs. Photocycle alteration and increased enzymatic activity in genetically modified photoactivated adenylate cyclase OaPAC. Journal of Biological Chemistry 2023, 299 (8) , 105056. https://doi.org/10.1016/j.jbc.2023.105056
    22. Sharon Hammes-Schiffer. Exploring proton-coupled electron transfer at multiple scales. Nature Computational Science 2023, 3 (4) , 291-300. https://doi.org/10.1038/s43588-023-00422-5
    23. Josene M. Toldo, Mariana T. do Casal, Elizete Ventura, Silmar A. do Monte, Mario Barbatti. Surface hopping modeling of charge and energy transfer in active environments. Physical Chemistry Chemical Physics 2023, 25 (12) , 8293-8316. https://doi.org/10.1039/D3CP00247K
    24. Zhongneng Zhou, Zijing Chen, Xiu-Wen Kang, Yalin Zhou, Bingyao Wang, Siwei Tang, Shuhua Zou, Yifei Zhang, Qiaoyu Hu, Fang Bai, Bei Ding, Dongping Zhong. The nature of proton-coupled electron transfer in a blue light using flavin domain. Proceedings of the National Academy of Sciences 2022, 119 (26) https://doi.org/10.1073/pnas.2203996119
    25. Rajiv K. Kar, Anne‐Frances Miller, Maria‐Andrea Mroginski. Understanding flavin electronic structure and spectra. WIREs Computational Molecular Science 2022, 12 (2) https://doi.org/10.1002/wcms.1541
    26. Ari Dwijayanti, Congqiang Zhang, Chueh Loo Poh, Thomas Lautier. Toward Multiplexed Optogenetic Circuits. Frontiers in Bioengineering and Biotechnology 2022, 9 https://doi.org/10.3389/fbioe.2021.804563
    27. Zhaoxi Sun, Payam Kalhor, Yang Xu, Jian Liu. Extensive numerical tests of leapfrog integrator in middle thermostat scheme in molecular simulations. Chinese Journal of Chemical Physics 2021, 34 (6) , 932-948. https://doi.org/10.1063/1674-0068/cjcp2111242
    28. Prokopis C. Andrikopoulos, Aditya S. Chaudhari, Yingliang Liu, Patrick E. Konold, John T. M. Kennis, Bohdan Schneider, Gustavo Fuertes. QM calculations predict the energetics and infrared spectra of transient glutamine isomers in LOV photoreceptors. Physical Chemistry Chemical Physics 2021, 23 (25) , 13934-13950. https://doi.org/10.1039/D1CP00447F
    29. Katalin Pirisi, Lipsa Nag, Zsuzsanna Fekete, James N. Iuliano, Jinnette Tolentino Collado, Ian P. Clark, Ildikó Pécsi, Pierre Sournia, Ursula Liebl, Gregory M. Greetham, Peter J. Tonge, Stephen R. Meech, Marten H. Vos, Andras Lukacs. Identification of the vibrational marker of tyrosine cation radical using ultrafast transient infrared spectroscopy of flavoprotein systems. Photochemical & Photobiological Sciences 2021, 20 (3) , 369-378. https://doi.org/10.1007/s43630-021-00024-y
    30. Maria‐Andrea Mroginski, Suliman Adam, Gil S. Amoyal, Avishai Barnoy, Ana‐Nicoleta Bondar, Veniamin A. Borin, Jonathan R. Church, Tatiana Domratcheva, Bernd Ensing, Francesca Fanelli, Nicolas Ferré, Ofer Filiba, Laura Pedraza‐González, Ronald González, Cristina E. González‐Espinoza, Rajiv K. Kar, Lukas Kemmler, Seung Soo Kim, Jacob Kongsted, Anna I. Krylov, Yigal Lahav, Michalis Lazaratos, Qays NasserEddin, Isabelle Navizet, Alexander Nemukhin, Massimo Olivucci, Jógvan Magnus Haugaard Olsen, Alberto Pérez de Alba Ortíz, Elisa Pieri, Aditya G. Rao, Young Min Rhee, Niccolò Ricardi, Saumik Sen, Ilia A. Solov'yov, Luca De Vico, Tomasz A. Wesolowski, Christian Wiebeler, Xuchun Yang, Igor Schapiro. Frontiers in Multiscale Modeling of Photoreceptor Proteins. Photochemistry and Photobiology 2021, 97 (2) , 243-269. https://doi.org/10.1111/php.13372
    31. Joshua J. Goings, Pengfei Li, Qiwen Zhu, Sharon Hammes-Schiffer. Formation of an unusual glutamine tautomer in a blue light using flavin photocycle characterizes the light-adapted state. Proceedings of the National Academy of Sciences 2020, 117 (43) , 26626-26632. https://doi.org/10.1073/pnas.2016719117
    32. Komsun Chaihan, Nawee Kungwan. Effect of number and different types of proton donors on excited-state intramolecular single and double proton transfer in bipyridine derivatives: theoretical insights. New Journal of Chemistry 2020, 44 (19) , 8018-8031. https://doi.org/10.1039/D0NJ01304H
    Download PDF
    Go to Journal of the American Chemical Society
    Get e-Alerts
    Get e-Alerts

    Journal of the American Chemical Society

    Cite this: J. Am. Chem. Soc. 2019, 141, 51, 20470–20479
    Click to copy citationCitation copied!
    https://doi.org/10.1021/jacs.9b11196
    Published November 19, 2019
    Copyright © 2019 American Chemical Society
    Request reuse permissions

    Article Views

    1293

    Altmetric

    -

    Citations

    32
    Learn about these metrics

    Article Views are the COUNTER-compliant sum of full text article downloads since November 2008 (both PDF and HTML) across all institutions and individuals. These metrics are regularly updated to reflect usage leading up to the last few days.

    Citations are the number of other articles citing this article, calculated by Crossref and updated daily. Find more information about Crossref citation counts.

    The Altmetric Attention Score is a quantitative measure of the attention that a research article has received online. Clicking on the donut icon will load a page at altmetric.com with additional details about the score and the social media presence for the given article. Find more information on the Altmetric Attention Score and how the score is calculated.