IUCrJ (Sep 2018)
Structural basis for light control of cell development revealed by crystal structures of a myxobacterial phytochrome
- 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
Affiliations
- Nicole C. Woitowich
- Department of Biology, Northeastern Illinois University, Chicago, IL, USA
- Andrei S. Halavaty
- Department of Biochemistry and Molecular Genetics, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA
- Patricia Waltz
- Department of Biology, Northeastern Illinois University, Chicago, IL, USA
- Christopher Kupitz
- Department of Physics, University of Wisconsin, Milwaukee, WI, USA
- Joseph Valera
- Department of Biology, Northeastern Illinois University, Chicago, IL, USA
- Gregory Tracy
- Department of Biology, Northeastern Illinois University, Chicago, IL, USA
- Kevin D. Gallagher
- Department of Biology, Northeastern Illinois University, Chicago, IL, USA
- Elin Claesson
- Department of Chemistry and Molecular Biology, University of Gothenburg, 40530 Gothenburg, Sweden
- Takanori Nakane
- Department of Biological Sciences, Graduate School of Science, University of Tokyo, 2-11-16 Yayoi, Bunkyo-ku, Tokyo, 113-0032, Japan
- Suraj Pandey
- Department of Physics, University of Wisconsin, Milwaukee, WI, USA
- Garrett Nelson
- Center for Applied Structural Discovery, Arizona State University, 85287 Tempe, AZ, USA
- Rie Tanaka
- RIKEN SPring-8 Center, 1-1-1 Kouto, Sayo-cho, Sayo-gun, 679-5148 Hyogo, Japan
- Eriko Nango
- RIKEN SPring-8 Center, 1-1-1 Kouto, Sayo-cho, Sayo-gun, 679-5148 Hyogo, Japan
- Eiichi Mizohata
- Department of Applied Chemistry, Graduate School of Engineering, Osaka University, 2-1 Yamadaoka, Suita, Osaka 565-0871, Japan
- Shigeki Owada
- RIKEN SPring-8 Center, 1-1-1 Kouto, Sayo-cho, Sayo-gun, 679-5148 Hyogo, Japan
- Kensure Tono
- RIKEN SPring-8 Center, 1-1-1 Kouto, Sayo-cho, Sayo-gun, 679-5148 Hyogo, Japan
- Yasumasa Joti
- RIKEN SPring-8 Center, 1-1-1 Kouto, Sayo-cho, Sayo-gun, 679-5148 Hyogo, Japan
- Angela C. Nugent
- Department of Biology, Northeastern Illinois University, Chicago, IL, USA
- Hardik Patel
- Department of Biology, Northeastern Illinois University, Chicago, IL, USA
- Ayesha Mapara
- Department of Biology, Northeastern Illinois University, Chicago, IL, USA
- James Hopkins
- Department of Biology, Northeastern Illinois University, Chicago, IL, USA
- Phu Duong
- Department of Biology, Northeastern Illinois University, Chicago, IL, USA
- Dorina Bizhga
- Department of Biology, Northeastern Illinois University, Chicago, IL, USA
- Svetlana E. Kovaleva
- Department of Biology, Northeastern Illinois University, Chicago, IL, USA
- Rachael St. Peter
- Department of Biology, Northeastern Illinois University, Chicago, IL, USA
- Cynthia N. Hernandez
- Department of Biology, Northeastern Illinois University, Chicago, IL, USA
- Wesley B. Ozarowski
- Department of Biology, Northeastern Illinois University, Chicago, IL, USA
- Shatabdi Roy-Chowdhuri
- Center for Applied Structural Discovery, Arizona State University, 85287 Tempe, AZ, USA
- Jay-How Yang
- Center for Applied Structural Discovery, Arizona State University, 85287 Tempe, AZ, USA
- Petra Edlund
- Department of Chemistry and Molecular Biology, University of Gothenburg, 40530 Gothenburg, Sweden
- Heikki Takala
- Faculty of Medicine, Anatomy, University of Helsinki, 00014 Helsinki, Finland
- Janne Ihalainen
- Nanoscience Center, Department of Biological and Environmental Sciences, University of Jyvaskyla, 40014 Jyvaskyla, Finland
- Jennifer Brayshaw
- Department of Physics, University of Wisconsin, Milwaukee, WI, USA
- Tyler Norwood
- Department of Physics, University of Wisconsin, Milwaukee, WI, USA
- Ishwor Poudyal
- Department of Physics, University of Wisconsin, Milwaukee, WI, USA
- Petra Fromme
- Center for Applied Structural Discovery, Arizona State University, 85287 Tempe, AZ, USA
- John C. H. Spence
- Center for Applied Structural Discovery, Arizona State University, 85287 Tempe, AZ, USA
- Keith Moffat
- Department of Biochemistry and Molecular Biology, The University of Chicago, Chicago, IL, USA
- Sebastian Westenhoff
- Department of Chemistry and Molecular Biology, University of Gothenburg, 40530 Gothenburg, Sweden
- Marius Schmidt
- Department of Physics, University of Wisconsin, Milwaukee, WI, USA
- Emina A. Stojković
- Department of Biology, Northeastern Illinois University, Chicago, IL, USA
- DOI
- https://doi.org/10.1107/S2052252518010631
- Journal volume & issue
-
Vol. 5,
no. 5
pp. 619 – 634
Abstract
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.
Keywords
