Ultrafast Dynamics of Heliorhodopsins
- Shinya TaharaShinya TaharaDepartment of Chemistry, Graduate School of Science, Osaka University, 1-1 Machikaneyama, Toyonaka, Osaka 560-0043, JapanMore by Shinya Tahara
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- Manish SinghManish SinghDepartment of Life Science and Applied Chemistry, Nagoya Institute of Technology, Showa-ku, Nagoya 466-8555, JapanMore by Manish Singh
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- Hikaru KuramochiHikaru KuramochiMolecular Spectroscopy Laboratory, RIKEN, 2-1 Hirosawa, Wako 351-0198, JapanUltrafast Spectroscopy Research Team, RIKEN Center for Advanced Photonics (RAP), 2-1 Hirosawa, Wako 351-0198, JapanPRESTO, Japan Science and Technology Agency, 4-1-8 Honcho Kawaguchi, Saitama 332-0012, JapanMore by Hikaru Kuramochi
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- Wataru ShihoyaWataru ShihoyaDepartment of Biological Sciences, Graduate School of Science, The University of Tokyo, 2-11-16 Yayoi, Bunkyo-ku, Tokyo 113-0032, JapanMore by Wataru Shihoya
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- Keiichi InoueKeiichi InouePRESTO, Japan Science and Technology Agency, 4-1-8 Honcho Kawaguchi, Saitama 332-0012, JapanInstitute for Solid State Physics, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8581, JapanMore by Keiichi Inoue
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- Osamu NurekiOsamu NurekiDepartment of Biological Sciences, Graduate School of Science, The University of Tokyo, 2-11-16 Yayoi, Bunkyo-ku, Tokyo 113-0032, JapanMore by Osamu Nureki
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- Oded BéjàOded BéjàFaculty of Biology, Technion Israel Institute of Technology, Haifa 32000, IsraelMore by Oded Béjà
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- Yasuhisa MizutaniYasuhisa MizutaniDepartment of Chemistry, Graduate School of Science, Osaka University, 1-1 Machikaneyama, Toyonaka, Osaka 560-0043, JapanMore by Yasuhisa Mizutani
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- Hideki KandoriHideki KandoriDepartment of Life Science and Applied Chemistry, Nagoya Institute of Technology, Showa-ku, Nagoya 466-8555, JapanOptoBioTechnology Research Center, Nagoya Institute of Technology, Showa-ku, Nagoya 466-8555, JapanMore by Hideki Kandori
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- Tahei Tahara*Tahei Tahara*E-mail: [email protected]Molecular Spectroscopy Laboratory, RIKEN, 2-1 Hirosawa, Wako 351-0198, JapanUltrafast Spectroscopy Research Team, RIKEN Center for Advanced Photonics (RAP), 2-1 Hirosawa, Wako 351-0198, JapanMore by Tahei Tahara
Abstract
Heliorhodopsins (HeR) constitute a new rhodopsin family and show only <15% sequence identities with type-1 and type-2 rhodopsins. The large difference in amino acid sequence between HeRs and other rhodopsins raises a question whether their biological function is triggered by efficient and rapid photoisomerization of the retinal chromophore as in the case of other rhodopsins. We performed femtosecond time-resolved absorption measurements of two HeRs, HeR 48C12 and HeR from Thermoplasmatales archaeon SG8-52-1. Both HeRs exhibit excited-state absorption around 480 nm and stimulated emission in the >650 nm region, and these transient signals decay concomitantly with appearance of photoproduct absorption on a subpicosecond time scale. The observed spectral change indicates that ultrafast retinal photoisomerization proceeds in the femtosecond time region. The transient spectra and dynamics of HeRs are surprisingly similar to those of type-1 rhodopsins, despite remarkable differences in amino acid arrangement in the hydrophobic region of the retinal binding site.
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(31)
, 7083-7091. https://doi.org/10.1021/acs.jpclett.3c01133
- Partha Malakar, Ishita Das, Sudeshna Bhattacharya, Andrew Harris, Mordechai Sheves, Leonid S. Brown, Sanford Ruhman. Bidirectional Photochemistry of Antarctic Microbial Rhodopsin: Emerging Trend of Ballistic Photoisomerization from the 13-cis Resting State. The Journal of Physical Chemistry Letters 2022, 13
(34)
, 8134-8140. https://doi.org/10.1021/acs.jpclett.2c01974
- Ishita Das, Alina Pushkarev, Mordechai Sheves. Light-Induced Conformational Alterations in Heliorhodopsin Triggered by the Retinal Excited State. The Journal of Physical Chemistry B 2021, 125
(31)
, 8797-8804. https://doi.org/10.1021/acs.jpcb.1c04551
- Steve Meech. Virtual Issue on Ultrafast Spectroscopy. The Journal of Physical Chemistry B 2021, 125
(23)
, 6037-6039. https://doi.org/10.1021/acs.jpcb.1c04148
- Manish Singh, Masanori Hashimoto, Kota Katayama, Yuji Furutani, Hideki Kandori. Internal Proton Transfer in the Activation of Heliorhodopsin. Journal of Molecular Biology 2023, 114 , 168273. https://doi.org/10.1016/j.jmb.2023.168273
- Srividya Ganapathy, Xin Meng, Delizzia Mossel, Mels Jagt, Daan Brinks. Expanding the family of genetically encoded voltage indicators with a candidate Heliorhodopsin exhibiting near-infrared fluorescence. Journal of Biological Chemistry 2023, 299
(6)
, 104771. https://doi.org/10.1016/j.jbc.2023.104771
- Shibuki Suzuki, Sari Kumagai, Toshio Nagashima, Toshio Yamazaki, Takashi Okitsu, Akimori Wada, Akira Naito, Kota Katayama, Keiichi Inoue, Hideki Kandori, Izuru Kawamura. Characterization of retinal chromophore and protonated Schiff base in Thermoplasmatales archaeon heliorhodopsin using solid-state NMR spectroscopy. Biophysical Chemistry 2023, 296 , 106991. https://doi.org/10.1016/j.bpc.2023.106991
- Jessica E. Besaw, Jörg Reichenwallner, Paolo De Guzman, Andrejs Tucs, Anling Kuo, Takefumi Morizumi, Koji Tsuda, Adnan Sljoka, R. J. Dwayne Miller, Oliver P. Ernst. Low pH structure of heliorhodopsin reveals chloride binding site and intramolecular signaling pathway. Scientific Reports 2022, 12
(1)
https://doi.org/10.1038/s41598-022-17716-9
- Willem J. de Grip, Srividya Ganapathy. Rhodopsins: An Excitingly Versatile Protein Species for Research, Development and Creative Engineering. Frontiers in Chemistry 2022, 10 https://doi.org/10.3389/fchem.2022.879609
- Laura Pedraza-González, Leonardo Barneschi, Daniele Padula, Luca De Vico, Massimo Olivucci. Evolution of the Automatic Rhodopsin Modeling (ARM) Protocol. Topics in Current Chemistry 2022, 380
(3)
https://doi.org/10.1007/s41061-022-00374-w
- Se-Hwan Kim, Kimleng Chuon, Shin-Gyu Cho, Ahreum Choi, Seanghun Meas, Hyun-Suk Cho, Kwang-Hwan Jung. Color-tuning of natural variants of heliorhodopsin. Scientific Reports 2021, 11
(1)
https://doi.org/10.1038/s41598-020-72125-0
- Andrey Rozenberg, Keiichi Inoue, Hideki Kandori, Oded Béjà. Microbial Rhodopsins: The Last Two Decades. Annual Review of Microbiology 2021, 75
(1)
, 427-447. https://doi.org/10.1146/annurev-micro-031721-020452
- Akimitsu Higuchi, Wataru Shihoya, Masae Konno, Tatsuya Ikuta, Hideki Kandori, Keiichi Inoue, Osamu Nureki. Crystal structure of schizorhodopsin reveals mechanism of inward proton pumping. Proceedings of the National Academy of Sciences 2021, 118
(14)
https://doi.org/10.1073/pnas.2016328118
- M. A. Ostrovsky, V. A. Nadtochenko. Femtochemistry of Rhodopsins. Russian Journal of Physical Chemistry B 2021, 15
(2)
, 344-351. https://doi.org/10.1134/S1990793121020226
- Tatsuki Tanaka, Manish Singh, Wataru Shihoya, Keitaro Yamashita, Hideki Kandori, Osamu Nureki. Structural basis for unique color tuning mechanism in heliorhodopsin. Biochemical and Biophysical Research Communications 2020, 533
(3)
, 262-267. https://doi.org/10.1016/j.bbrc.2020.06.124
- Tatsuya Ikuta, Wataru Shihoya, Masahiro Sugiura, Kazuho Yoshida, Masahito Watari, Takaya Tokano, Keitaro Yamashita, Kota Katayama, Satoshi P. Tsunoda, Takayuki Uchihashi, Hideki Kandori, Osamu Nureki. Structural insights into the mechanism of rhodopsin phosphodiesterase. Nature Communications 2020, 11
(1)
https://doi.org/10.1038/s41467-020-19376-7
- Hideki Kandori. Retinal Proteins: Photochemistry and Optogenetics. Bulletin of the Chemical Society of Japan 2020, 93
(1)
, 76-85. https://doi.org/10.1246/bcsj.20190292
- Manish Singh, Kota Katayama, Oded Béjà, Hideki Kandori. Anion binding to mutants of the Schiff base counterion in heliorhodopsin 48C12. Physical Chemistry Chemical Physics 2019, 21
(42)
, 23663-23671. https://doi.org/10.1039/C9CP04102H
- Wataru Shihoya, Keiichi Inoue, Manish Singh, Masae Konno, Shoko Hososhima, Keitaro Yamashita, Kento Ikeda, Akimitsu Higuchi, Tamaki Izume, Sae Okazaki, Masanori Hashimoto, Ritsu Mizutori, Sahoko Tomida, Yumeka Yamauchi, Rei Abe-Yoshizumi, Kota Katayama, Satoshi P. Tsunoda, Mikihiro Shibata, Yuji Furutani, Alina Pushkarev, Oded Béjà, Takayuki Uchihashi, Hideki Kandori, Osamu Nureki. Crystal structure of heliorhodopsin. Nature 2019, 574
(7776)
, 132-136. https://doi.org/10.1038/s41586-019-1604-6