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Download Hi-Res ImageDownload to MS-PowerPointCite This:J. Phys. Chem. B 2018, 122, 18, 4784-4792
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Origin of the Reactive and Nonreactive Excited States in the Primary Reaction of Rhodopsins: pH Dependence of Femtosecond Absorption of Light-Driven Sodium Ion Pump Rhodopsin KR2

  • Shinya Tahara
    Shinya Tahara
    Molecular Spectroscopy Laboratory, RIKEN, 2-1 Hirosawa, Wako 351-0198, Japan
    More by Shinya Tahara
    Orcidhttp://orcid.org/0000-0003-3979-3135
  • , 
  • Satoshi Takeuchi
    Satoshi Takeuchi
    Molecular Spectroscopy Laboratory  and  Ultrafast Spectroscopy Research Team, RIKEN, 2-1 Hirosawa, Wako 351-0198, Japan
    More by Satoshi Takeuchi
  • , 
  • Rei Abe-Yoshizumi
    Rei Abe-Yoshizumi
    Department of Frontier Materials, Nagoya Institute of Technology, Showa-ku, Nagoya 466-8555, Japan
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  • , 
  • Keiichi Inoue
    Keiichi Inoue
    Department of Frontier Materials  and  OptoBioTechnology Research Center, Nagoya Institute of Technology, Showa-ku, Nagoya 466-8555, Japan
    PRESTO, Japan Science and Technology Agency, 4-1-8 Honcho Kawaguchi, Saitama 332-0012, Japan
    More by Keiichi Inoue
  • , 
  • Hiroyuki Ohtani
    Hiroyuki Ohtani
    Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Yokohama 226-8501, Japan
    More by Hiroyuki Ohtani
  • , 
  • Hideki Kandori
    Hideki Kandori
    Department of Frontier Materials  and  OptoBioTechnology Research Center, Nagoya Institute of Technology, Showa-ku, Nagoya 466-8555, Japan
    More by Hideki Kandori
    Orcidhttp://orcid.org/0000-0002-4922-1344
  • , and 
  • Tahei Tahara*
    Tahei Tahara
    Molecular Spectroscopy Laboratory  and  Ultrafast Spectroscopy Research Team, RIKEN, 2-1 Hirosawa, Wako 351-0198, Japan
    *E-mail: [email protected]
    More by Tahei Tahara
    Orcidhttp://orcid.org/0000-0001-8421-242X
Cite this: J. Phys. Chem. B 2018, 122, 18, 4784–4792
Publication Date (Web):April 30, 2018
https://doi.org/10.1021/acs.jpcb.8b01934
Copyright © 2018 American Chemical Society
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    Abstract

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    KR2 is the first light-driven Na+-pumping rhodopsin discovered. It was reported that the photoexcitation of KR2 generates multiple S1 states, i.e., “reactive” and “nonreactive” S1 states at physiological pH, but their origin remained unclear. In this study, we examined the S1 state dynamics of KR2 using femtosecond time-resolved absorption spectroscopy at different pH′s in the range from 4 to 11. It was found that the reactive S1 state is predominantly formed at pH >9, but its population drastically decreases with decreasing pH while the population of the nonreactive S1 state(s) increases. The pH dependence of the relative population of the reactive S1 state correlates very well with the pH titration curve of Asp116, which is the counterion of the protonated retinal Schiff base (PRSB) in KR2. This strongly indicates that the deprotonation/protonation of Asp116 is directly related to the generation of the multiple S1 states in KR2. The quantitative analysis of the time-resolved absorption data led us to conclude that the reactive and nonreactive S1 states of KR2 originate from KR2 proteins having a hydrogen bond between Asp116 and PRSB or not, respectively. In other words, it is the ground-state inhomogeneity that is the origin of the coexistence of the reactive and nonreactive S1 states in KR2. So far, the generation of multiple S1 states having a different photoreactivity of rhodopsins has been mainly explained with the branching of the relaxation pathway in the Franck–Condon region in the S1 state. The present study shows that the structural inhomogeneity in the ground state, in particular that of the hydrogen-bond network, is the more plausible origin of the reactive and nonreactive S1 states which have been widely observed for various rhodopsins.

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jpcb.8b01934.

    • HPLC analysis of the extracted retinal oxime at pH 8 and 4. Femtosecond time-resolved absorption spectra of wild-type KR2 at all of the pH′s measured as well as those of the D116N mutant. The temporal trace of the time-resolved absorption signal of D116N and the best fit. Tables of the parameters of the best fits for wild-type KR2 at each pH and the D116N mutant (PDF)

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    2. Marvin Asido, Josef Wachtveitl. Photochemistry of the Light-Driven Sodium Pump Krokinobacter eikastus Rhodopsin 2 and Its Implications on Microbial Rhodopsin Research: Retrospective and Perspective. The Journal of Physical Chemistry B 2023, 127 (17) , 3766-3773. https://doi.org/10.1021/acs.jpcb.2c08933
    3. Pavel A. Kusochek, Andrei V. Scherbinin, Anastasia V. Bochenkova. Insights into the Early-Time Excited-State Dynamics of Structurally Inhomogeneous Rhodopsin KR2. The Journal of Physical Chemistry Letters 2021, 12 (35) , 8664-8671. https://doi.org/10.1021/acs.jpclett.1c02312
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    12. Qifan Yang, Deliang Chen. Na+ Binding and Transport: Insights from Light-Driven Na+-Pumping Rhodopsin. Molecules 2023, 28 (20) , 7135. https://doi.org/10.3390/molecules28207135
    13. Mikhail A. Ostrovsky, Olga A. Smitienko, Anastasia V. Bochenkova, Tatiana B. Feldman. Similarities and Differences in Photochemistry of Type I and Type II Rhodopsins. Biochemistry (Moscow) 2023, 88 (10) , 1528-1543. https://doi.org/10.1134/S0006297923100097
    14. Kentaro Mannen, Takashi Nagata, Andrey Rozenberg, Masae Konno, María del Carmen Marín, Reza Bagherzadeh, Oded Béjà, Takayuki Uchihashi, Keiichi Inoue. Multiple Roles of a Conserved Glutamate Residue for Unique Biophysical Properties in a New Group of Microbial Rhodopsins Homologous to TAT Rhodopsin. Journal of Molecular Biology 2023, 134 , 168331. https://doi.org/10.1016/j.jmb.2023.168331
    15. Clara Nassrin Kriebel, Marvin Asido, Jagdeep Kaur, Jennifer Orth, Philipp Braun, Johanna Becker-Baldus, Josef Wachtveitl, Clemens Glaubitz. Structural and functional consequences of the H180A mutation of the light-driven sodium pump KR2. Biophysical Journal 2023, 122 (6) , 1003-1017. https://doi.org/10.1016/j.bpj.2022.12.023
    16. Marie Kurihara, Vera Thiel, Hirona Takahashi, Keiichi Kojima, David M. Ward, Donald A. Bryant, Makoto Sakai, Susumu Yoshizawa, Yuki Sudo. Identification of a Functionally Efficient and Thermally Stable Outward Sodium-Pumping Rhodopsin (BeNaR) from a Thermophilic Bacterium. Chemical and Pharmaceutical Bulletin 2023, 71 (2) , 154-164. https://doi.org/10.1248/cpb.c22-00774
    17. Chun‐Fu Chang, Hikaru Kuramochi, Manish Singh, Rei Abe‐Yoshizumi, Tatsuya Tsukuda, Hideki Kandori, Tahei Tahara. A Unified View on Varied Ultrafast Dynamics of the Primary Process in Microbial Rhodopsins. Angewandte Chemie 2022, 134 (2) https://doi.org/10.1002/ange.202111930
    18. Chun‐Fu Chang, Hikaru Kuramochi, Manish Singh, Rei Abe‐Yoshizumi, Tatsuya Tsukuda, Hideki Kandori, Tahei Tahara. A Unified View on Varied Ultrafast Dynamics of the Primary Process in Microbial Rhodopsins. Angewandte Chemie International Edition 2022, 61 (2) https://doi.org/10.1002/anie.202111930
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    21. Chun-Fu Chang, Hikaru Kuramochi, Manish Singh, Rei Abe-Yoshizumi, Tatsuya Tsukuda, Hideki Kandori, Tahei Tahara. Acid–base equilibrium of the chromophore counterion results in distinct photoisomerization reactivity in the primary event of proteorhodopsin. Physical Chemistry Chemical Physics 2019, 21 (46) , 25728-25734. https://doi.org/10.1039/C9CP04991F
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