Cyanobacteriochrome Photoreceptors Lacking the Canonical Cys Residue

Keiji Fushimi, Nathan C. Rockwell, Gen Enomoto, Ni-Ni-Win, Shelley S. Martin, Fei Gan, Donald A. Bryant, Masahiko Ikeuchi, J. Clark Lagarias, Rei Narikawa

Research output: Contribution to journalArticle

15 Citations (Scopus)

Abstract

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.

Original languageEnglish (US)
Pages (from-to)6981-6995
Number of pages15
JournalBiochemistry
Volume55
Issue number50
DOIs
StatePublished - Dec 20 2016

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Bile Pigments
Light
Chromophores
Sensors
Tetrapyrroles
Phytochrome
Methyl Green
Proteins
Sulfides
Escherichia coli
Acids

All Science Journal Classification (ASJC) codes

  • Biochemistry

Cite this

Fushimi, K., Rockwell, N. C., Enomoto, G., Ni-Ni-Win, Martin, S. S., Gan, F., ... Narikawa, R. (2016). Cyanobacteriochrome Photoreceptors Lacking the Canonical Cys Residue. Biochemistry, 55(50), 6981-6995. https://doi.org/10.1021/acs.biochem.6b00940
Fushimi, Keiji ; Rockwell, Nathan C. ; Enomoto, Gen ; Ni-Ni-Win ; Martin, Shelley S. ; Gan, Fei ; Bryant, Donald A. ; Ikeuchi, Masahiko ; Lagarias, J. Clark ; Narikawa, Rei. / Cyanobacteriochrome Photoreceptors Lacking the Canonical Cys Residue. In: Biochemistry. 2016 ; Vol. 55, No. 50. pp. 6981-6995.
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Fushimi, K, Rockwell, NC, Enomoto, G, Ni-Ni-Win, Martin, SS, Gan, F, Bryant, DA, Ikeuchi, M, Lagarias, JC & Narikawa, R 2016, 'Cyanobacteriochrome Photoreceptors Lacking the Canonical Cys Residue', Biochemistry, vol. 55, no. 50, pp. 6981-6995. https://doi.org/10.1021/acs.biochem.6b00940

Cyanobacteriochrome Photoreceptors Lacking the Canonical Cys Residue. / Fushimi, Keiji; Rockwell, Nathan C.; Enomoto, Gen; Ni-Ni-Win; Martin, Shelley S.; Gan, Fei; Bryant, Donald A.; Ikeuchi, Masahiko; Lagarias, J. Clark; Narikawa, Rei.

In: Biochemistry, Vol. 55, No. 50, 20.12.2016, p. 6981-6995.

Research output: Contribution to journalArticle

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AU - Rockwell, Nathan C.

AU - Enomoto, Gen

AU - Ni-Ni-Win,

AU - Martin, Shelley S.

AU - Gan, Fei

AU - Bryant, Donald A.

AU - Ikeuchi, Masahiko

AU - Lagarias, J. Clark

AU - Narikawa, Rei

PY - 2016/12/20

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N2 - 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.

AB - 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.

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Fushimi K, Rockwell NC, Enomoto G, Ni-Ni-Win, Martin SS, Gan F et al. Cyanobacteriochrome Photoreceptors Lacking the Canonical Cys Residue. Biochemistry. 2016 Dec 20;55(50):6981-6995. https://doi.org/10.1021/acs.biochem.6b00940