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 & 21 others 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 Spence, Keith Moffat, Sebastian Westenhoff, Marius Schmidt, Emina A. Stojković

Research output: Contribution to journalArticle

2 Citations (Scopus)

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 myxo-bacterium 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.

Original languageEnglish (US)
Pages (from-to)619-634
Number of pages16
JournalIUCrJ
Volume5
DOIs
StatePublished - Jan 1 2018

Fingerprint

phytochrome
Phytochrome
Threonine
Chromophores
Myxococcales
Histidine
chromophores
histidine
Crystal structure
bacteria
Bacteria
Light
crystal structure
Stigmatella aurantiaca
cells
modules
physiological responses
photoreceptors
mammals
Mammals

Keywords

  • Absorption spectra
  • Myxobacteria
  • Photoreceptors
  • Photosynthetic bacteria
  • Phytochromes

ASJC Scopus subject areas

  • Chemistry(all)
  • Biochemistry
  • Materials Science(all)
  • Condensed Matter Physics

Cite this

Woitowich, N. C., Halavaty, A. S., Waltz, P., Kupitz, C., Valera, J., Tracy, G., ... Stojković, E. A. (2018). Structural basis for light control of cell development revealed by crystal structures of a myxobacterial phytochrome. IUCrJ, 5, 619-634. https://doi.org/10.1107/S2052252518010631

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

In: IUCrJ, Vol. 5, 01.01.2018, p. 619-634.

Research output: Contribution to journalArticle

Woitowich, NC, Halavaty, AS, Waltz, P, Kupitz, C, Valera, J, Tracy, G, Gallagher, KD, Claesson, E, Nakane, T, Pandey, S, Nelson, G, Tanaka, R, Nango, E, Mizohata, E, Owada, S, Tono, K, Joti, Y, Nugent, AC, Patel, H, Mapara, A, Hopkins, J, Duong, P, Bizhga, D, Kovaleva, SE, Peter, RS, Hernandez, CN, Ozarowski, WB, Roy-Chowdhuri, S, Yang, JH, Edlund, P, Takala, H, Ihalainen, J, Brayshaw, J, Norwood, T, Poudyal, I, Fromme, P, Spence, J, Moffat, K, Westenhoff, S, Schmidt, M & Stojković, EA 2018, 'Structural basis for light control of cell development revealed by crystal structures of a myxobacterial phytochrome' IUCrJ, vol. 5, pp. 619-634. https://doi.org/10.1107/S2052252518010631
Woitowich, Nicole C. ; Halavaty, Andrei S. ; Waltz, Patricia ; Kupitz, Christopher ; Valera, Joseph ; Tracy, Gregory ; Gallagher, Kevin D. ; Claesson, Elin ; Nakane, Takanori ; Pandey, Suraj ; Nelson, Garrett ; Tanaka, Rie ; Nango, Eriko ; Mizohata, Eiichi ; Owada, Shigeki ; Tono, Kensure ; Joti, Yasumasa ; Nugent, Angela C. ; Patel, Hardik ; Mapara, Ayesha ; Hopkins, James ; Duong, Phu ; Bizhga, Dorina ; Kovaleva, Svetlana E. ; Peter, Rachael St ; Hernandez, Cynthia N. ; Ozarowski, Wesley B. ; Roy-Chowdhuri, Shatabdi ; Yang, Jay How ; Edlund, Petra ; Takala, Heikki ; Ihalainen, Janne ; Brayshaw, Jennifer ; Norwood, Tyler ; Poudyal, Ishwor ; Fromme, Petra ; Spence, John ; Moffat, Keith ; Westenhoff, Sebastian ; Schmidt, Marius ; Stojković, Emina A. / Structural basis for light control of cell development revealed by crystal structures of a myxobacterial phytochrome. In: IUCrJ. 2018 ; Vol. 5. pp. 619-634.
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AU - Tracy, Gregory

AU - Gallagher, Kevin D.

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AU - Joti, Yasumasa

AU - Nugent, Angela C.

AU - Patel, Hardik

AU - Mapara, Ayesha

AU - Hopkins, James

AU - Duong, Phu

AU - Bizhga, Dorina

AU - Kovaleva, Svetlana E.

AU - Peter, Rachael St

AU - Hernandez, Cynthia N.

AU - Ozarowski, Wesley B.

AU - Roy-Chowdhuri, Shatabdi

AU - Yang, Jay How

AU - Edlund, Petra

AU - Takala, Heikki

AU - Ihalainen, Janne

AU - Brayshaw, Jennifer

AU - Norwood, Tyler

AU - Poudyal, Ishwor

AU - Fromme, Petra

AU - Spence, John

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