Cyanobacteriochrome Photoreceptors Lacking the Canonical Cys Residue
- Fushimi, Keiji [ Department of Biological Science, Faculty of Science, Shizuoka University, Ohya, Suruga-ku, Shizuoka 422-8529, Japan ]
- Rockwell, Nathan C [ Department of Molecular and Cellular Biology, University of California, Davis California 95616, United States ]
- Enomoto, Gen [ Department of Life Sciences (Biology), Graduate School of Arts and Sciences, University of Tokyo, Komaba, Meguro, Tokyo 153-8902, Japan ]
- Ni-Ni-Win [ Department of Life Sciences (Biology), Graduate School of Arts and Sciences, University of Tokyo, Komaba, Meguro, Tokyo 153-8902, Japan ]
- Martin, Shelley S [ Department of Molecular and Cellular Biology, University of California, Davis California 95616, United States ]
- Gan, Fei [ Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, Pennsylvania 16802 United States ]
- Bryant, Donald A [ Montana State University: Chemistry & Biochemistry ] [ Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, Pennsylvania 16802 United States ]
- Ikeuchi, Masahiko [ Department of Life Sciences (Biology), Graduate School of Arts and Sciences, University of Tokyo, Komaba, Meguro, Tokyo 153-8902, Japan ] [ Core Research for Evolutional Science and Technology, Japan Science and Technology Agency, 4-1-8 Honcho Kawaguchi, Saitama 332-0012 Japan ]
- Lagarias, J Clark [ Department of Molecular and Cellular Biology, University of California, Davis California 95616, United States ]
- Narikawa, Rei [ Department of Biological Science, Faculty of Science, Shizuoka University, Ohya, Suruga-ku, Shizuoka 422-8529, Japan ]
Cyanobacteriochromes (CBCRs) are cyanobacterial photoreceptors that sense near-ultraviolet to far-red light. Like the distantly related phytochromes, all CBCRs reported to date have a conserved Cys residue (the "canonical Cys" or "first Cys") that forms a thioether linkage to C31 of the linear tetrapyrrole (bilin) chromophore. Detection of ultraviolet, violet, and blue light is performed by at least three subfamilies of two-Cys CBCRs that require both the first Cys and a second Cys that forms a second covalent linkage to C10 of the bilin. In the well-characterized DXCF subfamily, the second Cys is part of a conserved Asp-Xaa-Cys-Phe motif. We here report novel CBCRs lacking the first Cys but retaining the DXCF Cys as part of a conserved Asp-Xaa-Cys-Ile-Pro (DXCIP) motif. Phylogenetic analysis demonstrates that DXCIP CBCRs are a sister to a lineage of DXCF CBCR domains from phototaxis sensors. Three such DXCIP CBCR domains (cce_4193g1, Cyan8802_2776g1, and JSC1_24240) were characterized after recombinant expression in Escherichia coli engineered to produce phycocyanobilin. All three covalently bound bilin and showed unidirectional photoconversion in response to green light. Spectra of acid-denatured proteins in the dark-adapted state do not correspond to those of known bilins. One DXCIP CBCR, cce_4193g1, exhibited very rapid dark reversion consistent with a function as a power sensor. However, Cyan8802_2776g1 exhibited slower dark reversion and would not have such a function. The full-length cce_4193 protein also possesses a DXCF CBCR GAF domain (cce_4193g2) with a covalently bound phycoviolobilin chromophore and a blue/green photocycle. Our studies indicate that CBCRs need not contain the canonical Cys residue to function as photochromic light sensors and that phototaxis proteins containing DXCIP CBCRs may potentially perceive both light quality and light intensity.