Observation of early events in the photoactivation of Myxobacterial phytochrome using time-resolved serial femtosecond crystallography

Abstract Myxobacteria are non-photosynthetic, soil-dwelling bacteria distinguished by a multicellular stage in their life cycle known as fruiting bodies that are stimulated by light. Myxobacterial phytochromes are candidates for the perception of red-light. The mechanism how light is perceived and c...

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Main Authors: Tek Narsingh Malla, Luis Aldama, Viridiana Leon, Denisse Feliz, Hao Hu, Isaiah Thomas, Andrea Cellini, Weixiao Y. Wahlgren, Amke Nimmrich, Sabine Botha, Ray Sierra, Mark S. Hunter, Frédéric Poitevin, Stella Lisova, Alexander Batyuk, Gregory Gate, Rebecca Jernigan, Christopher J. Kupitz, Piotr Maj, Petra Meszaros, Moona Kurttila, Leonardo Monrroy, Fangjia Luo, Shigeki Owada, Jungmin Kang, Chavdar Slavov, Michal Maj, Candice Gautier, Maithri Kashipathy, Alexandra Tolstikova, Valerio Mariani, Anton Barty, Frank Moss, Peter Schwander, Haiguang Liu, Sébastien Boutet, Petra Fromme, Heikki Takala, Janne A. Ihalainen, Uwe Weierstall, Sebastian Westenhoff, Emina A. Stojković, Marius Schmidt
Format: Article
Language:English
Published: Nature Portfolio 2025-06-01
Series:Communications Chemistry
Online Access:https://doi.org/10.1038/s42004-025-01578-z
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author Tek Narsingh Malla
Luis Aldama
Viridiana Leon
Denisse Feliz
Hao Hu
Isaiah Thomas
Andrea Cellini
Weixiao Y. Wahlgren
Amke Nimmrich
Sabine Botha
Ray Sierra
Mark S. Hunter
Frédéric Poitevin
Stella Lisova
Alexander Batyuk
Gregory Gate
Rebecca Jernigan
Christopher J. Kupitz
Piotr Maj
Petra Meszaros
Moona Kurttila
Leonardo Monrroy
Fangjia Luo
Shigeki Owada
Jungmin Kang
Chavdar Slavov
Michal Maj
Candice Gautier
Maithri Kashipathy
Alexandra Tolstikova
Valerio Mariani
Anton Barty
Frank Moss
Peter Schwander
Haiguang Liu
Sébastien Boutet
Petra Fromme
Heikki Takala
Janne A. Ihalainen
Uwe Weierstall
Sebastian Westenhoff
Emina A. Stojković
Marius Schmidt
author_facet Tek Narsingh Malla
Luis Aldama
Viridiana Leon
Denisse Feliz
Hao Hu
Isaiah Thomas
Andrea Cellini
Weixiao Y. Wahlgren
Amke Nimmrich
Sabine Botha
Ray Sierra
Mark S. Hunter
Frédéric Poitevin
Stella Lisova
Alexander Batyuk
Gregory Gate
Rebecca Jernigan
Christopher J. Kupitz
Piotr Maj
Petra Meszaros
Moona Kurttila
Leonardo Monrroy
Fangjia Luo
Shigeki Owada
Jungmin Kang
Chavdar Slavov
Michal Maj
Candice Gautier
Maithri Kashipathy
Alexandra Tolstikova
Valerio Mariani
Anton Barty
Frank Moss
Peter Schwander
Haiguang Liu
Sébastien Boutet
Petra Fromme
Heikki Takala
Janne A. Ihalainen
Uwe Weierstall
Sebastian Westenhoff
Emina A. Stojković
Marius Schmidt
author_sort Tek Narsingh Malla
collection DOAJ
description Abstract Myxobacteria are non-photosynthetic, soil-dwelling bacteria distinguished by a multicellular stage in their life cycle known as fruiting bodies that are stimulated by light. Myxobacterial phytochromes are candidates for the perception of red-light. The mechanism how light is perceived and converted to a physiological response is unknown. Here, time-resolved serial femtosecond crystallographic (TR-SFX) experiments were conducted on microcrystals of the photosensory core module of the Stigmatella aurantiaca bacteriophytochrome 2 (SaBphP2). Initial events of the Z to E isomerization reaction of the covalently bound, open-chain tetrapyrrole biliverdin (BV) chromophore were determined. At 3 ps after light activation, the BV ring-D assumes a configuration needed for the isomerization. At 100 ps, a mixture of BV in the Z or E configuration is observed in subunit A, while in the other subunit the chromophore remains in the Z configuration. In conjunction with prior results, these structures reveal the molecular mechanism of phytochrome activation in the photomorphogenesis of the myxobacteria and provide the molecular foundation for physiological responses to red light in other bacteria.
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spelling doaj-art-7f24dd0fa5ed4b7897ca5e985b8211f62025-08-20T02:06:28ZengNature PortfolioCommunications Chemistry2399-36692025-06-018111010.1038/s42004-025-01578-zObservation of early events in the photoactivation of Myxobacterial phytochrome using time-resolved serial femtosecond crystallographyTek Narsingh Malla0Luis Aldama1Viridiana Leon2Denisse Feliz3Hao Hu4Isaiah Thomas5Andrea Cellini6Weixiao Y. Wahlgren7Amke Nimmrich8Sabine Botha9Ray Sierra10Mark S. Hunter11Frédéric Poitevin12Stella Lisova13Alexander Batyuk14Gregory Gate15Rebecca Jernigan16Christopher J. Kupitz17Piotr Maj18Petra Meszaros19Moona Kurttila20Leonardo Monrroy21Fangjia Luo22Shigeki Owada23Jungmin Kang24Chavdar Slavov25Michal Maj26Candice Gautier27Maithri Kashipathy28Alexandra Tolstikova29Valerio Mariani30Anton Barty31Frank Moss32Peter Schwander33Haiguang Liu34Sébastien Boutet35Petra Fromme36Heikki Takala37Janne A. Ihalainen38Uwe Weierstall39Sebastian Westenhoff40Emina A. Stojković41Marius Schmidt42Department of Physics, University of Wisconsin-MilwaukeeDepartment of Biology, Northeastern Illinois UniversityDepartment of Biology, Northeastern Illinois UniversityDepartment of Biology, Northeastern Illinois UniversityDepartment of Physics, Arizona State UniversityDepartment of Biology, Northeastern Illinois UniversityDepartment of Chemistry and Molecular Biology, University of GothenburgDepartment of Chemistry and Molecular Biology, University of GothenburgDepartment of Chemistry, University of WashingtonDepartment of Physics, Arizona State UniversityLinac Coherent Light Source, SLAC National Accelerator LaboratoryLinac Coherent Light Source, SLAC National Accelerator LaboratoryLinac Coherent Light Source, SLAC National Accelerator LaboratoryLinac Coherent Light Source, SLAC National Accelerator LaboratoryLinac Coherent Light Source, SLAC National Accelerator LaboratoryLinac Coherent Light Source, SLAC National Accelerator LaboratorySchool of Molecular Sciences and Biodesign Center for Applied Structural Discovery, Arizona State UniversityLinac Coherent Light Source, SLAC National Accelerator LaboratoryDepartment of Chemistry-BMC, Uppsala UniversityDepartment of Chemistry-BMC, Uppsala UniversityNanoscience Center, Department of Biological and Environmental Science, University of JyväskyläDepartment of Chemistry-BMC, Uppsala UniversityJapan Synchrotron Radiation Research InstituteJapan Synchrotron Radiation Research InstituteJapan Synchrotron Radiation Research InstituteDepartment of Chemistry, University of South FloridaDepartment of Chemistry- Ångström, Uppsala UniversityDepartment of Chemistry-BMC, Uppsala UniversityLinac Coherent Light Source, SLAC National Accelerator LaboratoryCenter for Free-Electron Laser Science, Deutsches Elektronen SynchrotronLinac Coherent Light Source, SLAC National Accelerator LaboratoryCenter for Free-Electron Laser Science, Deutsches Elektronen SynchrotronLinac Coherent Light Source, SLAC National Accelerator LaboratoryDepartment of Physics, University of Wisconsin-MilwaukeeMicrosoft Research AI4ScienceLinac Coherent Light Source, SLAC National Accelerator LaboratorySchool of Molecular Sciences and Biodesign Center for Applied Structural Discovery, Arizona State UniversityNanoscience Center, Department of Biological and Environmental Science, University of JyväskyläNanoscience Center, Department of Biological and Environmental Science, University of JyväskyläDepartment of Physics, Arizona State UniversityDepartment of Chemistry and Molecular Biology, University of GothenburgDepartment of Biology, Northeastern Illinois UniversityDepartment of Physics, University of Wisconsin-MilwaukeeAbstract Myxobacteria are non-photosynthetic, soil-dwelling bacteria distinguished by a multicellular stage in their life cycle known as fruiting bodies that are stimulated by light. Myxobacterial phytochromes are candidates for the perception of red-light. The mechanism how light is perceived and converted to a physiological response is unknown. Here, time-resolved serial femtosecond crystallographic (TR-SFX) experiments were conducted on microcrystals of the photosensory core module of the Stigmatella aurantiaca bacteriophytochrome 2 (SaBphP2). Initial events of the Z to E isomerization reaction of the covalently bound, open-chain tetrapyrrole biliverdin (BV) chromophore were determined. At 3 ps after light activation, the BV ring-D assumes a configuration needed for the isomerization. At 100 ps, a mixture of BV in the Z or E configuration is observed in subunit A, while in the other subunit the chromophore remains in the Z configuration. In conjunction with prior results, these structures reveal the molecular mechanism of phytochrome activation in the photomorphogenesis of the myxobacteria and provide the molecular foundation for physiological responses to red light in other bacteria.https://doi.org/10.1038/s42004-025-01578-z
spellingShingle Tek Narsingh Malla
Luis Aldama
Viridiana Leon
Denisse Feliz
Hao Hu
Isaiah Thomas
Andrea Cellini
Weixiao Y. Wahlgren
Amke Nimmrich
Sabine Botha
Ray Sierra
Mark S. Hunter
Frédéric Poitevin
Stella Lisova
Alexander Batyuk
Gregory Gate
Rebecca Jernigan
Christopher J. Kupitz
Piotr Maj
Petra Meszaros
Moona Kurttila
Leonardo Monrroy
Fangjia Luo
Shigeki Owada
Jungmin Kang
Chavdar Slavov
Michal Maj
Candice Gautier
Maithri Kashipathy
Alexandra Tolstikova
Valerio Mariani
Anton Barty
Frank Moss
Peter Schwander
Haiguang Liu
Sébastien Boutet
Petra Fromme
Heikki Takala
Janne A. Ihalainen
Uwe Weierstall
Sebastian Westenhoff
Emina A. Stojković
Marius Schmidt
Observation of early events in the photoactivation of Myxobacterial phytochrome using time-resolved serial femtosecond crystallography
Communications Chemistry
title Observation of early events in the photoactivation of Myxobacterial phytochrome using time-resolved serial femtosecond crystallography
title_full Observation of early events in the photoactivation of Myxobacterial phytochrome using time-resolved serial femtosecond crystallography
title_fullStr Observation of early events in the photoactivation of Myxobacterial phytochrome using time-resolved serial femtosecond crystallography
title_full_unstemmed Observation of early events in the photoactivation of Myxobacterial phytochrome using time-resolved serial femtosecond crystallography
title_short Observation of early events in the photoactivation of Myxobacterial phytochrome using time-resolved serial femtosecond crystallography
title_sort observation of early events in the photoactivation of myxobacterial phytochrome using time resolved serial femtosecond crystallography
url https://doi.org/10.1038/s42004-025-01578-z
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