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NpR3784 is the prototype for a distinctive group of red/green cyanobacteriochromes using alternative Phe residues for photoproduct tuning

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Abstract

Cyanobacteriochromes (CBCRs) are photosensory proteins found in cyanobacteria and are distantly related to the widespread phytochromes. Whereas plant phytochromes exhibit responses to red and far-red light, CBCRs use the same photoisomerization of a linear tetrapyrrole (bilin) chromophore to respond to a wide range of colors. NpR6012g4 from Nostoc punctiforme and AnPixJ from Anabaena sp. PCC 7120 belong to a large subfamily of red/green CBCRs that exhibit a red-absorbing dark state similar to that of phytochrome but a green-absorbing photoproduct rather than a far-red-absorbing one. In these canonical red/green CBCRs, the photoproduct is blue-shifted relative to the orange absorption observed in the absence of native protein structure. This spectral tuning of the photoproduct requires a conserved Phe residue on the second β strand of the CBCR GAF domain, consistent with a trapped-twist mechanism in which the bilin is sterically constrained in the photoproduct. N. punctiforme also produces NpR3784, a CBCR with a similar red/green photocycle to that of NpR6012g4. NpR3784 lacks both the β2 Phe and other residues characteristic of the canonical red/green CBCRs. In the current work, we identify NpR3784 homologs with red/green photocycles in other cyanobacteria. Spectral tuning in this NpR3784 group is accomplished by a different set of conserved Phe residues, including a characteristic Phe residue on β1. This set of Phe residues cannot be interchanged with the Phe residues found in canonical red/green CBCRs such as NpR6012g4. Our results provide new insights into the flexible protein–chromophore interactions used by CBCRs to generate their remarkable spectral diversity.

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Authors and Affiliations

  1. Department of Molecular and Cell Biology, University of California at Davis, Davis, CA, 95616, USA

    Nathan C. Rockwell, Shelley S. Martin & J. Clark Lagarias

  2. Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, PA 16802, USA

    Fei Gan & Donald A. Bryant

  3. Department of Chemistry and Biochemistry, Montana State University, Bozeman, MT, 59717, USA

    Donald A. Bryant

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  1. Nathan C. Rockwell
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Rockwell, N.C., Martin, S.S., Gan, F. et al. NpR3784 is the prototype for a distinctive group of red/green cyanobacteriochromes using alternative Phe residues for photoproduct tuning. Photochem Photobiol Sci 14, 258–269 (2015). https://doi.org/10.1039/c4pp00336e

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