Excitation-Wavelength Dependent Photocycle Initiation Dynamics Resolve Heterogeneity in the Photoactive Yellow Protein from Halorhodospira halophila
Mix, L. T., Carroll, E. C., Morozov, D., Pan, J., Gordon, W. R., Philip, A., Fuzell, J., Kumauchi, M., van Stokkum, I., Groenhof, G., Hoff, W. D., & Larsen, D. S. (2018). Excitation-Wavelength Dependent Photocycle Initiation Dynamics Resolve Heterogeneity in the Photoactive Yellow Protein from Halorhodospira halophila. Biochemistry, 57(1), 1733-1747. https://doi.org/10.1021/acs.biochem.7b01114
Pan, Jie |
© 2018 American Chemical Society. This is a final draft version of an article whose final and definitive form has been published by American Chemical Society. Published in this repository with the kind permission of the publisher
Photoactive yellow proteins (PYPs) make up a diverse class of blue-light-absorbing bacterial photoreceptors. Electronic excitation of the p-coumaric acid chromophore covalently bound within PYP results in triphasic quenching kinetics; however, the molecular basis of this behavior remains unresolved. Here we explore this question by examining the excitation-wavelength dependence of the photodynamics of the PYP from Halorhodospira halophila via a combined experimental and computational approach. The fluorescence quantum yield, steady-state fluorescence emission maximum, and cryotrapping spectra are demonstrated to depend on excitation wavelength. We also compare the femtosecond photodynamics in PYP at two excitation wavelengths (435 and 475 nm) with a dual-excitation-wavelength-interleaved pump–probe technique. Multicompartment global analysis of these data demonstrates that the excited-state photochemistry of PYP depends subtly, but convincingly, on excitation wavelength with similar kinetics with distinctly different spectral features, including a shifted ground-state beach and altered stimulated emission oscillator strengths and peak positions. Three models involving multiple excited states, vibrationally enhanced barrier crossing, and inhomogeneity are proposed to interpret the observed excitation-wavelength dependence of the data. Conformational heterogeneity was identified as the most probable model, which was supported with molecular mechanics simulations that identified two levels of inhomogeneity involving the orientation of the R52 residue and different hydrogen bonding networks with the p-coumaric acid chromophore. Quantum calculations were used to confirm that these inhomogeneities track to altered spectral properties consistent with the experimental results. ...
PublisherAmerican Chemical Society
Publication in research information system
MetadataShow full item record
Related funder(s)Academy of Finland
Funding program(s)Research post as Academy Research Fellow, AoF; Others, AoF; Postdoctoral Researcher, AoF; Academy Project, AoF
Additional information about fundingThis work was supported by a grant from the National Science Foundation (CHE-1413739) to both D.S.L. and W.D.H. Additionally, W.D.H. acknowledges additional support from National Science Foundation Grants MCB-1051590 and MRI-1338097. G.G. and D.M. acknowledge support from the Academy of Finland (Grants 258806, 290677, and 304455 to G.G. and Grant 285481 to D.M.).
Showing items with similar title or keywords.
Photoactive Yellow Protein Chromophore Photoisomerizes around a Single Bond if the Double Bond Is Locked Mustalahti, Satu; Morozov, Dmitry; Luk, Hoi Ling; Pallerla, Rajanish R.; Myllyperkiö, Pasi; Pettersson, Mika; Pihko, Petri M.; Groenhof, Gerrit (American Chemical Society, 2020)Photoactivation in the Photoactive Yellow Protein, a bacterial blue light photoreceptor, proceeds via photo-isomerization of the double C=C bond in the covalently attached chromophore. Quantum chemistry calculations, ...
Observe while it happens : catching photoactive proteins in the act with non-adiabatic molecular dynamics simulations Groenhof, Gerrit; Modi, Vaibhav; Morozov, Dmitry (Elsevier Ltd., 2020)Organisms use photo-receptors to react to light. The first step is usually the absorption of a photon by a prosthetic group embedded inside the photo-receptor, often a conjugated chromophore. The electronic changes in the ...
Gustavsson, Emil; Isaksson, Linnéa; Persson, Cecilia; Mayzel, Maxim; Brath, Ulrika; Vrhovac, Lidija; Ihalainen, Janne A.; Karlsson, B. Göran; Orekhov, Vladislav; Westenhoff, Sebastian (Cell Press, 2020)Phytochromes sense red/far-red light and control many biological processes in plants, fungi, and bacteria. Although crystal structures of dark and light adapted states have been determined, the molecular mechanisms underlying ...
The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser Claesson, Elin; Wahlgren, Weixiao Yuan; Takala, Heikki; Pandey, Suraj; Castillon, Leticia; Kuznetsova, Valentyna; Henry, Léocadie; Panman, Matthijs; Carrillo, Melissa; Kübel, Joachim; Nanekar, Rahul; Isaksson, Linnéa; Nimmrich, Amke; Cellini, Andrea; Morozov, Dmitry; Maj, Michał; Kurttila, Moona; Bosman, Robert; Nango, Eriko; Tanaka, Rie; Tanaka, Tomoyuki; Fangjia, Luo; Iwata, So; Owada, Shigeki; Moffat, Keith; Groenhof, Gerrit; Stojkovic, Emina A.; Ihalainen, Janne A.; Schmidt, Marius; Westenhof, Sebastian (eLife Sciences Publications, 2020)Phytochrome proteins control the growth, reproduction, and photosynthesis of plants, fungi, and bacteria. Light is detected by a bilin cofactor, but it remains elusive how this leads to activation of the protein through ...
Chromophore-Protein Interplay During the Phytochrome Photocycle Revealed by Step-Scan FTIR Spectroscopy Ihalainen, Janne; Gustavsson, Emil; Schröder, Lea; Donnini, Serena; Lehtivuori, Heli; Isaksson, Linnéa; Thöing, Christian; Modi, Vaibhav; Berntsson, Oskar; Stucki-Buchli, Brigitte; Liukkonen, Alli; Häkkänen, Heikki; Kalenius, Elina; Westenhoff, Sebastian; Kottke, Tilman (American Chemical Society, 2018)Phytochrome proteins regulate many photoresponses of plants and microorganisms. Light absorption causes isomerization of the biliverdin chromophore, which triggers a series of structural changes to activate the signaling ...