The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser
Claesson, E., Wahlgren, W. Y., Takala, H., Pandey, S., Castillon, L., Kuznetsova, V., Henry, L., Panman, M., Carrillo, M., Kübel, J., Nanekar, R., Isaksson, L., Nimmrich, A., Cellini, A., Morozov, D., Maj, M., Kurttila, M., Bosman, R., Nango, E., . . . Westenhof, S. (2020). The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser. eLife, 9, Article e53514. https://doi.org/10.7554/eLife.53514
DisciplineSolu- ja molekyylibiologiaFysikaalinen kemiaNanoscience CenterCell and Molecular BiologyPhysical ChemistryNanoscience Center
© Claesson et al
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 structural changes. We present serial femtosecond X-ray crystallographic data of the chromophore-binding domains of a bacterial phytochrome at delay times of 1 ps and 10 ps after photoexcitation. The data reveal a twist of the D-ring, which leads to partial detachment of the chromophore from the protein. Unexpectedly, the conserved so-called pyrrole water is photodissociated from the chromophore, concomitant with movement of the A-ring and a key signalling aspartate. The changes are wired together by ultrafast backbone and water movements around the chromophore, channeling them into signal transduction towards the output domains. We suggest that the observed collective changes are important for the phytochrome photoresponse, explaining the earliest steps of how plants, fungi and bacteria sense red light. ...
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Related funder(s)Academy of Finland
Funding program(s)Academy Project, AoF
Additional information about fundingThe experiments at SACLA were performed at BL3 with the approval of the Japan Synchrotron Radiation Research Institute (JASRI) (Proposal No. 2018A8055 and 2019A8007). S.W. acknowledges the European Research Council for support (grant number: 279944). This work was supported by Academy of Finland grants 285461 and 296135 (H. T. and J.A.I., respectively) and Jane and Aatos Erkko foundation (J.A.I.). This research is partially supported by Platform Project for Supporting Drug Discovery and Life Science Research (Basis for Supporting Innovative Drug Discovery and Life Science Research (BINDS)) from Japan Agency for Medical Research and Development (AMED). We thank Dr. Takanori Nakane for assistance with data processing during the beamtime and Heli Lehtivuori for the spectroscopic measurements with the microcrystals. This work was supported by NSF Science and Technology Centers grant NSF-1231306 (“Biology with X-ray Lasers”), the National Science Foundation (NSF)-MCBRUI 1413360 and NSF-MCB-EAGER 1839513 Research Grants to E.A.S. This work has been done as part of the BioExcel CoE (www.bioexcel.eu), a project funded by the European Union contracts H2020-INFRAEDI-02-2018-823830 and H2020-EINFRA-2015-1-675728. ...
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