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Unusual shift in the visible absorption spectrum of an active ctenophore photoprotein elucidated by time-dependent density functional theory

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Abstract

Active hydromedusan and ctenophore Ca2+-regulated photoproteins form complexes consisting of apoprotein and strongly non-covalently bound 2-hydroperoxycoelenterazine (an oxygenated intermediate of coelenterazine). Whereas the absorption maximum of hydromedusan photoproteins is at 460–470 nm, ctenophore photoproteins absorb at 437 nm. Finding out a physical reason for this blue shift is the main objective of this work, and, to achieve it, the whole structure of the protein–substrate complex was optimized using a linear scaling quantum–mechanical method. Electronic excitations pertinent to the spectra of the 2-hydroperoxy adduct of coelenterazine were simulated with time-dependent density functional theory. The dihedral angle of 60° of the 6-(p-hydroxy)-phenyl group relative to the imidazopyrazinone core of 2-hydroperoxycoelenterazine molecule was found to be the key factor determining the absorption of ctenophore photoproteins at 437 nm. The residues relevant to binding of the substrate and its adopting the particular rotation were also identified.

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Acknowledgements

The ab initio quantum chemical calculations were funded by RFBR and NSFC as the research project No. 19-54-53004 and RFBR research project No. 20-04-00085. The development of structural atomistic model of berovin without calcium ions generated by the I-TASSER server was funded by project 0721-2020-0033 of the Russian Ministry of Science and Education.

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Authors and Affiliations

  1. Kirensky Institute of Physics SB RAS, Federal Research Center “Krasnoyarsk Science Center SB RAS”, Akademgorodok 50/38, Krasnoyarsk, 660036, Russia

    Felix N. Tomilin

  2. Siberian Federal University, Svobodny 79 pr., Krasnoyarsk, 660041, Russia

    Felix N. Tomilin, Anastasia V. Rogova & Ludmila P. Burakova

  3. National Research Tomsk State University, Lenin Avenue 36, Tomsk, 634050, Russia

    Felix N. Tomilin & Olga N. Tchaikovskaya

  4. Photobiology Laboratory, Institute of Biophysics SB RAS, Federal Research Center “Krasnoyarsk Science Center SB RAS”, Akademgorodok 50/50, Krasnoyarsk, 660036, Russia

    Ludmila P. Burakova & Eugene S. Vysotski

  5. Kyungpook National University, 80 Daehakro, Bukgu, Daegu, 41566, South Korea

    Pavel V. Avramov

  6. Research Center for Computational Design of Advanced Functional Materials (CD-FMat), National Institute of Advanced Industrial Science and Technology (AIST), Central 2, Umezono 1-1-1, Tsukuba, 305-8568, Japan

    Dmitri G. Fedorov

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Tomilin, F.N., Rogova, A.V., Burakova, L.P. et al. Unusual shift in the visible absorption spectrum of an active ctenophore photoprotein elucidated by time-dependent density functional theory. Photochem Photobiol Sci 20, 559–570 (2021). https://doi.org/10.1007/s43630-021-00039-5

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