A Photo-Labile Thioether Linkage to Phycoviolobilin Provides the Foundation for the Blue/Green Photocycles in DXCF-Cyanobacteriochromes

• Published in: Acta crystallographica. Section E, Structure reports online Vol. 21; no. 1; pp. 88 - 97
• Main Authors: Burgie, E. Sethe, Walker, Joseph M., Phillips, George N., Vierstra, Richard D.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Ltd 08.01.2013; International Union of Crystallography
• Subjects: Amino Acid Motifs; Bacterial Proteins - chemistry; Carbon; Crystallography, X-Ray; Cyanobacteria; Driving; Elongated structure; Foundations; Half-Life; Hydrogen Bonding; Kinetics; Linkages; Microorganisms; Models, Molecular; Perception; Photolysis; Photoreceptors; Photoreceptors, Microbial - chemistry; Photosynthesis; Phycobilins - chemistry; Protein Binding; Protein Structure, Tertiary; Structural Homology, Protein; Sulfides - chemistry; Thermodynamics; Thermosynechococcus elongatus
• ISSN: 0969-2126; 1878-4186; 1600-5368; 1878-4186; 1600-5368
• DOI: 10.1016/j.str.2012.11.001

The phytochrome superfamily encompasses a diverse collection of photochromic photoreceptors in plants and microorganisms that employ a covalently linked bilin cradled in a cGMP-phosphodiesterase/adenylyl-cyclase/FhlA (GAF) domain to detect light. Whereas most interconvert between red- and far-red-light-absorbing states, cyanobacteria also express variants called cyanobacteriochromes (CBCRs) that modify bilin absorption to collectively perceive the entire visible spectrum. Here, we present two X-ray crystallographic structures of the GAF domain from the blue/green photochromic CBCR PixJ from Thermosynechococcus elongatus. These structures confirm the hypothesis that CBCRs variably manipulate the chromophore π-conjugation system through isomerization and a second thioether linkage, in this case involving the bilin C10 carbon and Cys494 within a DXCF sequence characteristic of blue/green CBCRs. Biochemical studies support a mechanism for photoconversion whereby the second linkage ruptures on route to the green-light-absorbing state. Collectively, the TePixJ(GAF) models illustrate the remarkable structural and photochemical versatility among phytochromes and CBCRs in driving light perception. ▸ The Te-PixJ structure reveals the positions of the two DXCF-CBCR thioether linkages ▸ For blue/green photocycling, Te-PixJ utilizes a phycoviolobilin chromophore ▸ Rupture of the noncanonical DXCF thioether coincides with Pb/Pg photoconversion ▸ Te-PixJ bilin-binding and photochemistry diverge greatly from canonical phytochromes Phytochromes use a thioether-linked bilin to interconvert between red- and far-red light-absorbing states. Burgie et al. describe structures of PixJ, a cyanobacteriochrome, and how it enforces a blue/green photocycles by manipulating bilin π-conjugation through isomerization and a photo-labile thioether-linkage.