Diverse light responses of cyanobacteria mediated by phytochrome superfamily photoreceptors

Wiltbank, Lisa B.; Kehoe, David M.

doi:10.1038/s41579-018-0110-4

Cited by 118 publications

(75 citation statements)

References 155 publications

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“…Photoreceptors in the phytochrome superfamily utilize a specific lineage of the GAF (cGMP phosphodiesterase, Adenylyl cyclase and FhlA) signaling module to bind a thioether-linked linear tetrapyrrole (bilin) chromophore for light perception via 15,16-photoisomerization (6)(7)(8)(9)(10)(11). Such photoreceptors play critical roles in plant development as well as in regulating cyanobacterial phototaxis, development and light harvesting (2,3,(12)(13)(14)(15)(16)(17). Protein structural changes following the primary photochemical event then alter the downstream enzymatic activities and/or protein-protein interactions via an interdomain allosteric mechanism (18).…”

Section: /Bodymentioning

confidence: 99%

Molecular Basis of Far-red Sensing in Cyanobacteriochrome

Bandara

Rockwell

Zeng

et al. 2020

Preprint

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Author contributionsXY designed the project; SB, SSM and XZ carried out cloning, purification, and crystallization; SB, XZ, SSM and NR conducted mutagenesis and spectroscopic experiments; SB, XZ, ZR, HS and XY collected monochromatic diffraction data; HS, CW and ZR collected Laue diffraction data; ZR processed the Laue data and carried out singlecrystal spectroscopic experiments; SB and XY determined, refined and analyzed crystal structures; NR carried out phylogenetic analysis; SB, XY, NR, MVM, and JCL interpreted the data; XY, NR, and JCL wrote the paper with inputs from all authors. Abstract (156 words)Cyanobacteriochromes are small, panchromatic photoreceptors in the phytochrome superfamily that regulate diverse light-mediated adaptive processes in cyanobacteria. The molecular basis of far-red (FR) light perception by cyanobacteriochromes is currently unknown. Here we report the crystal structure of a far-red-sensing cyanobacteriochrome from Anabaena cylindrica PCC 7122, which exhibits a reversible far-red/orange photocycle.The 2.7 Å structure of its FR-absorbing dark state, determined by room temperature serial crystallography and cryo-crystallography, reveals an all-Z,syn configuration of its bound linear tetrapyrrole (bilin) chromophore that is less extended than the bilin chromophores of all known phytochromes. Based on structural comparisons with other bilin-binding proteins and extensive spectral analyses on mutants, we identify key proteinchromophore interactions that enable far-red sensing in bilin-binding proteins. We propose that FR-CBCRs employ two distinct tuning mechanisms, which work together to produce a large batho-chromatic shift. Findings of this work have important implications for development and improvement of photoproteins with far-red absorption and fluorescence. Significance Statement (99 words)Phytochromes are well known far-red-light sensors found in plants that trigger adaptive responses to facilitate competition for light capture with neighboring plants. Red-and farred-sensing are critical to cyanobacteria living in the far-red-enriched shade of plants.Here we report the crystal structure of a far-red-sensing cyanobacteriochrome, a distant cyanobacterial relative of phytochrome. These studies shed insight into the poorly understood molecular basis of far-red-sensing by phytobilin-based photoreceptors.Owing to the deep tissue penetration of far-red light, far-red-sensing photoreceptors offer promising protein scaffolds for developing gene-based photoswitches, optoacoustic contrast agents and fluorescent probes for in situ imaging and optogenetic applications.

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Section: /Bodymentioning

confidence: 99%

Molecular Basis of Far-red Sensing in Cyanobacteriochrome

Bandara

Rockwell

Zeng

et al. 2020

Preprint

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“…This is exemplified by abilities for metabolic switching (i.e. CO 2 /N 2 fixation), maintaining photoreceptors of various wavelength sensitivities for binary programs of circadian rhythm, and forming specialized cells which can sometimes be terminally differentiated and lead to multicellularity [9,10]. To regulate these complex programs, cyanobacteria have an extensive repertoire of genes governing signal transduction including proteases, kinases, and nucleases.…”

Section: Introductionmentioning

confidence: 99%

Role of diversity-generating retroelements for regulatory pathway tuning in cyanobacteria

et al. 2020

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Background Cyanobacteria maintain extensive repertoires of regulatory genes that are vital for adaptation to environmental stress. Some cyanobacterial genomes have been noted to encode diversity-generating retroelements (DGRs), which promote protein hypervariation through localized retrohoming and codon rewriting in target genes. Past research has shown DGRs to mainly diversify proteins involved in cell-cell attachment or viral-host attachment within viral, bacterial, and archaeal lineages. However, these elements may be critical in driving variation for proteins involved in other core cellular processes. Results Members of 31 cyanobacterial genera encode at least one DGR, and together, their retroelements form a monophyletic clade of closely-related reverse transcriptases. This class of retroelements diversifies target proteins with unique domain architectures: modular ligand-binding domains often paired with a second domain that is linked to signal response or regulation. Comparative analysis indicates recent intragenomic duplication of DGR targets as paralogs, but also apparent intergenomic exchange of DGR components. The prevalence of DGRs and the paralogs of their targets is disproportionately high among colonial and filamentous strains of cyanobacteria. Conclusion We find that colonial and filamentous cyanobacteria have recruited DGRs to optimize a ligand-binding module for apparent function in signal response or regulation. These represent a unique class of hypervariable proteins, which might offer cyanobacteria a form of plasticity to adapt to environmental stress. This analysis supports the hypothesis that DGR-driven mutation modulates signaling and regulatory networks in cyanobacteria, suggestive of a new framework for the utility of localized genetic hypervariation.

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“…Phytochrome is a photoreceptor protein, which exists in diverse organisms from bacteria to land plants . Five phytochromes (phyA, B, C, D, and E) have been identified in most land plants , and the occurrence of phytochrome is known in several prokaryotes, which possess bacteriophytochromes and also canonical phytochromes . Phytochrome is photo‐interconvertible between the red light‐absorbing (Pr) and far‐red light‐absorbing (Pfr) forms and is involved in red/far‐red light responses .…”

Section: Introductionmentioning

confidence: 99%

Molecular shape under far‐red light and red light‐induced association of Arabidopsis phytochrome B

et al. 2019

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Phytochrome B (phyB) is a plant photoreceptor protein that regulates various photomorphogenic responses to optimize plant growth and development. PhyB exists in two photoconvertible forms: a red light-absorbing (Pr) and a far-red light-absorbing (Pfr) form. Therefore, to understand the mechanism of phototransformation, the structural characterization of fulllength phyB in these two forms is necessary. Here, we report the molecular structure of Arabidopsis thaliana phyB in Pr form and the molecular properties of the Pfr form determined by small-angle X-ray scattering coupled with size-exclusion chromatography. In solution, the Pr form associated as a dimer with a radius of gyration of 50 A. The molecular shape was a crossed shape, in which the orientation of the photosensory modules differed from that in the crystal structure of dimeric photosensory module. PhyB exhibited structural reversibility in the Pfr-to-Pr phototransformation and thermal reversion from Pfr to Pr in the dark. In addition, Pfr only exhibited nonspecific association, which distinguished molecular properties of Pfr form from those of the inactive Pr form.

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Diverse light responses of cyanobacteria mediated by phytochrome superfamily photoreceptors

Cited by 118 publications

References 155 publications

Molecular Basis of Far-red Sensing in Cyanobacteriochrome

Molecular Basis of Far-red Sensing in Cyanobacteriochrome

Role of diversity-generating retroelements for regulatory pathway tuning in cyanobacteria

Molecular shape under far‐red light and red light‐induced association of Arabidopsis phytochrome B

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