Structural basis for light control of cell development revealed by crystal structures of a myxobacterial phytochrome
Phytochromes are red-light photoreceptors that were first characterized in plants, with homologs in photosynthetic and non-photosynthetic bacteria known as bacteriophytochromes (BphPs). Upon absorption of light, BphPs interconvert between two states denoted Pr and Pfr with distinct absorption spectr...
Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
International Union of Crystallography
2018-09-01
|
Series: | IUCrJ |
Subjects: | |
Online Access: | http://scripts.iucr.org/cgi-bin/paper?S2052252518010631 |
id |
doaj-a56c4f1741084155bcfa230773aaee98 |
---|---|
record_format |
Article |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Nicole C. Woitowich Andrei S. Halavaty Patricia Waltz Christopher Kupitz Joseph Valera Gregory Tracy Kevin D. Gallagher Elin Claesson Takanori Nakane Suraj Pandey Garrett Nelson Rie Tanaka Eriko Nango Eiichi Mizohata Shigeki Owada Kensure Tono Yasumasa Joti Angela C. Nugent Hardik Patel Ayesha Mapara James Hopkins Phu Duong Dorina Bizhga Svetlana E. Kovaleva Rachael St. Peter Cynthia N. Hernandez Wesley B. Ozarowski Shatabdi Roy-Chowdhuri Jay-How Yang Petra Edlund Heikki Takala Janne Ihalainen Jennifer Brayshaw Tyler Norwood Ishwor Poudyal Petra Fromme John C. H. Spence Keith Moffat Sebastian Westenhoff Marius Schmidt Emina A. Stojković |
spellingShingle |
Nicole C. Woitowich Andrei S. Halavaty Patricia Waltz Christopher Kupitz Joseph Valera Gregory Tracy Kevin D. Gallagher Elin Claesson Takanori Nakane Suraj Pandey Garrett Nelson Rie Tanaka Eriko Nango Eiichi Mizohata Shigeki Owada Kensure Tono Yasumasa Joti Angela C. Nugent Hardik Patel Ayesha Mapara James Hopkins Phu Duong Dorina Bizhga Svetlana E. Kovaleva Rachael St. Peter Cynthia N. Hernandez Wesley B. Ozarowski Shatabdi Roy-Chowdhuri Jay-How Yang Petra Edlund Heikki Takala Janne Ihalainen Jennifer Brayshaw Tyler Norwood Ishwor Poudyal Petra Fromme John C. H. Spence Keith Moffat Sebastian Westenhoff Marius Schmidt Emina A. Stojković Structural basis for light control of cell development revealed by crystal structures of a myxobacterial phytochrome IUCrJ phytochromes photoreceptors photosynthetic bacteria myxobacteria absorption spectra |
author_facet |
Nicole C. Woitowich Andrei S. Halavaty Patricia Waltz Christopher Kupitz Joseph Valera Gregory Tracy Kevin D. Gallagher Elin Claesson Takanori Nakane Suraj Pandey Garrett Nelson Rie Tanaka Eriko Nango Eiichi Mizohata Shigeki Owada Kensure Tono Yasumasa Joti Angela C. Nugent Hardik Patel Ayesha Mapara James Hopkins Phu Duong Dorina Bizhga Svetlana E. Kovaleva Rachael St. Peter Cynthia N. Hernandez Wesley B. Ozarowski Shatabdi Roy-Chowdhuri Jay-How Yang Petra Edlund Heikki Takala Janne Ihalainen Jennifer Brayshaw Tyler Norwood Ishwor Poudyal Petra Fromme John C. H. Spence Keith Moffat Sebastian Westenhoff Marius Schmidt Emina A. Stojković |
author_sort |
Nicole C. Woitowich |
title |
Structural basis for light control of cell development revealed by crystal structures of a myxobacterial phytochrome |
title_short |
Structural basis for light control of cell development revealed by crystal structures of a myxobacterial phytochrome |
title_full |
Structural basis for light control of cell development revealed by crystal structures of a myxobacterial phytochrome |
title_fullStr |
Structural basis for light control of cell development revealed by crystal structures of a myxobacterial phytochrome |
title_full_unstemmed |
Structural basis for light control of cell development revealed by crystal structures of a myxobacterial phytochrome |
title_sort |
structural basis for light control of cell development revealed by crystal structures of a myxobacterial phytochrome |
publisher |
International Union of Crystallography |
series |
IUCrJ |
issn |
2052-2525 |
publishDate |
2018-09-01 |
description |
Phytochromes are red-light photoreceptors that were first characterized in plants, with homologs in photosynthetic and non-photosynthetic bacteria known as bacteriophytochromes (BphPs). Upon absorption of light, BphPs interconvert between two states denoted Pr and Pfr with distinct absorption spectra in the red and far-red. They have recently been engineered as enzymatic photoswitches for fluorescent-marker applications in non-invasive tissue imaging of mammals. This article presents cryo- and room-temperature crystal structures of the unusual phytochrome from the non-photosynthetic myxobacterium Stigmatella aurantiaca (SaBphP1) and reveals its role in the fruiting-body formation of this photomorphogenic bacterium. SaBphP1 lacks a conserved histidine (His) in the chromophore-binding domain that stabilizes the Pr state in the classical BphPs. Instead it contains a threonine (Thr), a feature that is restricted to several myxobacterial phytochromes and is not evolutionarily understood. SaBphP1 structures of the chromophore binding domain (CBD) and the complete photosensory core module (PCM) in wild-type and Thr-to-His mutant forms reveal details of the molecular mechanism of the Pr/Pfr transition associated with the physiological response of this myxobacterium to red light. Specifically, key structural differences in the CBD and PCM between the wild-type and the Thr-to-His mutant involve essential chromophore contacts with proximal amino acids, and point to how the photosignal is transduced through the rest of the protein, impacting the essential enzymatic activity in the photomorphogenic response of this myxobacterium. |
topic |
phytochromes photoreceptors photosynthetic bacteria myxobacteria absorption spectra |
url |
http://scripts.iucr.org/cgi-bin/paper?S2052252518010631 |
work_keys_str_mv |
AT nicolecwoitowich structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT andreishalavaty structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT patriciawaltz structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT christopherkupitz structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT josephvalera structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT gregorytracy structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT kevindgallagher structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT elinclaesson structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT takanorinakane structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT surajpandey structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT garrettnelson structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT rietanaka structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT erikonango structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT eiichimizohata structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT shigekiowada structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT kensuretono structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT yasumasajoti structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT angelacnugent structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT hardikpatel structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT ayeshamapara structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT jameshopkins structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT phuduong structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT dorinabizhga structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT svetlanaekovaleva structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT rachaelstpeter structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT cynthianhernandez structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT wesleybozarowski structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT shatabdiroychowdhuri structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT jayhowyang structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT petraedlund structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT heikkitakala structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT janneihalainen structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT jenniferbrayshaw structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT tylernorwood structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT ishworpoudyal structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT petrafromme structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT johnchspence structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT keithmoffat structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT sebastianwestenhoff structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT mariusschmidt structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome AT eminaastojkovic structuralbasisforlightcontrolofcelldevelopmentrevealedbycrystalstructuresofamyxobacterialphytochrome |
_version_ |
1725498390564831232 |
spelling |
doaj-a56c4f1741084155bcfa230773aaee982020-11-24T23:44:27ZengInternational Union of CrystallographyIUCrJ2052-25252018-09-015561963410.1107/S2052252518010631jt5025Structural basis for light control of cell development revealed by crystal structures of a myxobacterial phytochromeNicole C. Woitowich0Andrei S. Halavaty1Patricia Waltz2Christopher Kupitz3Joseph Valera4Gregory Tracy5Kevin D. Gallagher6Elin Claesson7Takanori Nakane8Suraj Pandey9Garrett Nelson10Rie Tanaka11Eriko Nango12Eiichi Mizohata13Shigeki Owada14Kensure Tono15Yasumasa Joti16Angela C. Nugent17Hardik Patel18Ayesha Mapara19James Hopkins20Phu Duong21Dorina Bizhga22Svetlana E. Kovaleva23Rachael St. Peter24Cynthia N. Hernandez25Wesley B. Ozarowski26Shatabdi Roy-Chowdhuri27Jay-How Yang28Petra Edlund29Heikki Takala30Janne Ihalainen31Jennifer Brayshaw32Tyler Norwood33Ishwor Poudyal34Petra Fromme35John C. H. Spence36Keith Moffat37Sebastian Westenhoff38Marius Schmidt39Emina A. Stojković40Department of Biology, Northeastern Illinois University, Chicago, IL, USADepartment of Biochemistry and Molecular Genetics, Feinberg School of Medicine, Northwestern University, Chicago, IL, USADepartment of Biology, Northeastern Illinois University, Chicago, IL, USADepartment of Physics, University of Wisconsin, Milwaukee, WI, USADepartment of Biology, Northeastern Illinois University, Chicago, IL, USADepartment of Biology, Northeastern Illinois University, Chicago, IL, USADepartment of Biology, Northeastern Illinois University, Chicago, IL, USADepartment of Chemistry and Molecular Biology, University of Gothenburg, 40530 Gothenburg, SwedenDepartment of Biological Sciences, Graduate School of Science, University of Tokyo, 2-11-16 Yayoi, Bunkyo-ku, Tokyo, 113-0032, JapanDepartment of Physics, University of Wisconsin, Milwaukee, WI, USACenter for Applied Structural Discovery, Arizona State University, 85287 Tempe, AZ, USARIKEN SPring-8 Center, 1-1-1 Kouto, Sayo-cho, Sayo-gun, 679-5148 Hyogo, JapanRIKEN SPring-8 Center, 1-1-1 Kouto, Sayo-cho, Sayo-gun, 679-5148 Hyogo, JapanDepartment of Applied Chemistry, Graduate School of Engineering, Osaka University, 2-1 Yamadaoka, Suita, Osaka 565-0871, JapanRIKEN SPring-8 Center, 1-1-1 Kouto, Sayo-cho, Sayo-gun, 679-5148 Hyogo, JapanRIKEN SPring-8 Center, 1-1-1 Kouto, Sayo-cho, Sayo-gun, 679-5148 Hyogo, JapanRIKEN SPring-8 Center, 1-1-1 Kouto, Sayo-cho, Sayo-gun, 679-5148 Hyogo, JapanDepartment of Biology, Northeastern Illinois University, Chicago, IL, USADepartment of Biology, Northeastern Illinois University, Chicago, IL, USADepartment of Biology, Northeastern Illinois University, Chicago, IL, USADepartment of Biology, Northeastern Illinois University, Chicago, IL, USADepartment of Biology, Northeastern Illinois University, Chicago, IL, USADepartment of Biology, Northeastern Illinois University, Chicago, IL, USADepartment of Biology, Northeastern Illinois University, Chicago, IL, USADepartment of Biology, Northeastern Illinois University, Chicago, IL, USADepartment of Biology, Northeastern Illinois University, Chicago, IL, USADepartment of Biology, Northeastern Illinois University, Chicago, IL, USACenter for Applied Structural Discovery, Arizona State University, 85287 Tempe, AZ, USACenter for Applied Structural Discovery, Arizona State University, 85287 Tempe, AZ, USADepartment of Chemistry and Molecular Biology, University of Gothenburg, 40530 Gothenburg, SwedenFaculty of Medicine, Anatomy, University of Helsinki, 00014 Helsinki, FinlandNanoscience Center, Department of Biological and Environmental Sciences, University of Jyvaskyla, 40014 Jyvaskyla, FinlandDepartment of Physics, University of Wisconsin, Milwaukee, WI, USADepartment of Physics, University of Wisconsin, Milwaukee, WI, USADepartment of Physics, University of Wisconsin, Milwaukee, WI, USACenter for Applied Structural Discovery, Arizona State University, 85287 Tempe, AZ, USACenter for Applied Structural Discovery, Arizona State University, 85287 Tempe, AZ, USADepartment of Biochemistry and Molecular Biology, The University of Chicago, Chicago, IL, USADepartment of Chemistry and Molecular Biology, University of Gothenburg, 40530 Gothenburg, SwedenDepartment of Physics, University of Wisconsin, Milwaukee, WI, USADepartment of Biology, Northeastern Illinois University, Chicago, IL, USAPhytochromes are red-light photoreceptors that were first characterized in plants, with homologs in photosynthetic and non-photosynthetic bacteria known as bacteriophytochromes (BphPs). Upon absorption of light, BphPs interconvert between two states denoted Pr and Pfr with distinct absorption spectra in the red and far-red. They have recently been engineered as enzymatic photoswitches for fluorescent-marker applications in non-invasive tissue imaging of mammals. This article presents cryo- and room-temperature crystal structures of the unusual phytochrome from the non-photosynthetic myxobacterium Stigmatella aurantiaca (SaBphP1) and reveals its role in the fruiting-body formation of this photomorphogenic bacterium. SaBphP1 lacks a conserved histidine (His) in the chromophore-binding domain that stabilizes the Pr state in the classical BphPs. Instead it contains a threonine (Thr), a feature that is restricted to several myxobacterial phytochromes and is not evolutionarily understood. SaBphP1 structures of the chromophore binding domain (CBD) and the complete photosensory core module (PCM) in wild-type and Thr-to-His mutant forms reveal details of the molecular mechanism of the Pr/Pfr transition associated with the physiological response of this myxobacterium to red light. Specifically, key structural differences in the CBD and PCM between the wild-type and the Thr-to-His mutant involve essential chromophore contacts with proximal amino acids, and point to how the photosignal is transduced through the rest of the protein, impacting the essential enzymatic activity in the photomorphogenic response of this myxobacterium.http://scripts.iucr.org/cgi-bin/paper?S2052252518010631phytochromesphotoreceptorsphotosynthetic bacteriamyxobacteriaabsorption spectra |