TY - JOUR
T1 - High-resolution crystal structures of transient intermediates in the phytochrome photocycle
AU - Carrillo, Melissa
AU - Pandey, Suraj
AU - Sanchez, Juan
AU - Noda, Moraima
AU - Poudyal, Ishwor
AU - Aldama, Luis
AU - Malla, Tek Narsingh
AU - Claesson, Elin
AU - Wahlgren, Weixiao Yuan
AU - Feliz, Denisse
AU - Šrajer, Vukica
AU - Maj, Michał
AU - Castillon, Leticia
AU - Iwata, So
AU - Nango, Eriko
AU - Tanaka, Rie
AU - Tanaka, Tomoyuki
AU - Fangjia, Luo
AU - Tono, Kensuke
AU - Owada, Shigeki
AU - Westenhoff, Sebastian
AU - Stojković, Emina A.
AU - Schmidt, Marius
N1 - Funding Information:
This work was supported by National Science Foundation (NSF) Science and Technology Centers (STC) grant NSF-1231306 (“Biology with X-ray Lasers”). Some results shown are derived from work performed at Argonne National Laboratory, Sector 14 - BioCARS at the Advanced Photon Source. Argonne is operated by UChicago Argonne for the US Department of Energy, Office of Biological and Environmental Research under contract DE-AC02-06CH11 357. The experiments at SACLA were performed at BL2 with the approval of the Japan Synchrotron Radiation Research Institute (proposal nos. 2018A8055 and 2019A8007). E.A.S. was supported by NSF-MCB-RUI 1413360 , NSF-MCB-EAGER grant 1839513 , and NSF STC BioXFEL center award 6227. Training of M.N. and L.A. was supported in part by the National Institute of General Medical Sciences (NIGMS) of the National Institutes of Health (NIH) Maximizing Access to Research Careers T34 GM105549 grant to E.A.S. Use of BioCARS was supported by NIH NIGMS under grant number P41 GM118217 . 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) from the Japan Agency for Medical Research and Development under grant number JP20am0101070 . Molecular graphics and analyses performed with UCSF Chimera, developed by the Resource for Biocomputing, Visualization, and Informatics at the University of California, San Francisco, with support from NIH P41-GM103311 . We thank Takanori Nakane for assistance with data processing.
Funding Information:
This work was supported by National Science Foundation (NSF) Science and Technology Centers (STC) grant NSF-1231306 (?Biology with X-ray Lasers?). Some results shown are derived from work performed at Argonne National Laboratory, Sector 14 - BioCARS at the Advanced Photon Source. Argonne is operated by UChicago Argonne for the US Department of Energy, Office of Biological and Environmental Research under contract DE-AC02-06CH11 357. The experiments at SACLA were performed at BL2 with the approval of the Japan Synchrotron Radiation Research Institute (proposal nos. 2018A8055 and 2019A8007). E.A.S. was supported by NSF-MCB-RUI 1413360, NSF-MCB-EAGER grant 1839513, and NSF STC BioXFEL center award 6227. Training of M.N. and L.A. was supported in part by the National Institute of General Medical Sciences (NIGMS) of the National Institutes of Health (NIH) Maximizing Access to Research Careers T34 GM105549 grant to E.A.S. Use of BioCARS was supported by NIH NIGMS under grant number P41 GM118217. 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) from the Japan Agency for Medical Research and Development under grant number JP20am0101070. Molecular graphics and analyses performed with UCSF Chimera, developed by the Resource for Biocomputing, Visualization, and Informatics at the University of California, San Francisco, with support from NIH P41-GM103311. We thank Takanori Nakane for assistance with data processing. Conceptualization, E.A.S. and M.S.; Methodology, S.W. E.A.S. and M.S.; Samples, M.C. J.S. M.N. L.A. D.F. and E.A.S.; Data collection, M.C. S.P. J.S. M.N. I.P. L.A. T.N.M. E. C. W.Y.W. D.F. V.?. M.M. L.C. S.I. E.N. R.T. T.T. L.F. K.T. S.O. S.W. E.A.S. and M.S.; Data processing, I.P. L.C. and S.P.; Data analysis, S.P. E.A.S. and M.S.; Writing ? original draft, E.A.S. and M.S. with input from all authors; Writing ? review & editing, E.A.S. S.W. and M.S. with input from all authors.; Funding acquisition, S.I. S.W. E.A.S. and M.S.; Resources and supervision, S.I. S.W. E.A.S. and M.S. The authors declare no competing interests. One or more of the authors of this paper self-identifies as an underrepresented ethnic minority in science. One or more of the authors of this paper received support from a program designed to increase minority representation in science.
Publisher Copyright:
© 2021 Elsevier Ltd
PY - 2021/7/1
Y1 - 2021/7/1
N2 - Phytochromes are red/far-red light photoreceptors in bacteria to plants, which elicit a variety of important physiological responses. They display a reversible photocycle between the resting Pr state and the light-activated Pfr state. Light signals are transduced as structural change through the entire protein to modulate its activity. It is unknown how the Pr-to-Pfr interconversion occurs, as the structure of intermediates remains notoriously elusive. Here, we present short-lived crystal structures of the photosensory core modules of the bacteriophytochrome from myxobacterium Stigmatella aurantiaca captured by an X-ray free electron laser 5 ns and 33 ms after light illumination of the Pr state. We observe large structural displacements of the covalently bound bilin chromophore, which trigger a bifurcated signaling pathway that extends through the entire protein. The snapshots show with atomic precision how the signal progresses from the chromophore, explaining how plants, bacteria, and fungi sense red light.
AB - Phytochromes are red/far-red light photoreceptors in bacteria to plants, which elicit a variety of important physiological responses. They display a reversible photocycle between the resting Pr state and the light-activated Pfr state. Light signals are transduced as structural change through the entire protein to modulate its activity. It is unknown how the Pr-to-Pfr interconversion occurs, as the structure of intermediates remains notoriously elusive. Here, we present short-lived crystal structures of the photosensory core modules of the bacteriophytochrome from myxobacterium Stigmatella aurantiaca captured by an X-ray free electron laser 5 ns and 33 ms after light illumination of the Pr state. We observe large structural displacements of the covalently bound bilin chromophore, which trigger a bifurcated signaling pathway that extends through the entire protein. The snapshots show with atomic precision how the signal progresses from the chromophore, explaining how plants, bacteria, and fungi sense red light.
KW - Lumi-R
KW - Pfr
KW - Pr
KW - X-ray free electron lasers
KW - bacteriophytochrome
KW - infrared fluorescent protein tissue markers
KW - photoconversion
KW - photocycle
KW - photosensory core module
KW - time-resolved serial femtosecond crystallography
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U2 - 10.1016/j.str.2021.03.004
DO - 10.1016/j.str.2021.03.004
M3 - Article
C2 - 33756101
AN - SCOPUS:85103974170
VL - 29
SP - 743-754.e4
JO - Structure with Folding & design
JF - Structure with Folding & design
SN - 0969-2126
IS - 7
ER -