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Structural basis for light control of cell development revealed by crystal structures of a myxobacterial phytochrome

By Nicole C. Woitowich, Andrei S. Halavaty, Patricia Waltz, Christopher Kupitz1, Joseph Valera, Gregory Tracy, Kevin D. Gallagher, Elin Claesson, Takanori Nakane, Suraj Pandey2, Garrett Charles Nelson3, 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 Yang3, Petra Edlund, Heikki Takala, Janne Ihalainen, Jennifer Brayshaw, Tyler Norwood, Ishwor Poudyal2, Petra Fromme3, John Spence3, Keith Moffat, Sebastian Westenhoff, Marius Schmidt2, Emina A. Stojković

1. SLAC National Accelerator Laboratory 2. University of Wisconsin - Milwaukee 3. Arizona State University

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Category

BioXFEL Publications

Published on

Type

journal-article

Author

Nicole C. Woitowich and Andrei S. Halavaty and Patricia Waltz and Christopher Kupitz and Joseph Valera and Gregory Tracy and Kevin D. Gallagher and Elin Claesson and Takanori Nakane and Suraj Pandey and Garrett Nelson and Rie Tanaka and Eriko Nango and Eiichi Mizohata and Shigeki Owada and Kensure Tono and Yasumasa Joti and Angela C. Nugent and Hardik Patel and Ayesha Mapara and James Hopkins and Phu Duong and Dorina Bizhga and Svetlana E. Kovaleva and Rachael St. Peter and Cynthia N. Hernandez and Wesley B. Ozarowski and Shatabdi Roy-Chowdhuri and Jay-How Yang and Petra Edlund and Heikki Takala and Janne Ihalainen and Jennifer Brayshaw and Tyler Norwood and Ishwor Poudyal and Petra Fromme and John C. H. Spence and Keith Moffat and Sebastian Westenhoff and Marius Schmidt and Emina A. Stojković

Citation

Woitowich, N.C. et al., 2018. Structural basis for light control of cell development revealed by crystal structures of a myxobacterial phytochrome. IUCrJ, 5(5), pp.619–634. Available at: http://dx.doi.org/10.1107/s2052252518010631.

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.

DOI

http://dx.doi.org/10.1107/s2052252518010631

Funding

NSF-STC Biology with X-ray Lasers (NSF-1231306)