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.
Similar content being viewed by others
References
M. A. van der Horst, J. Key and K. J. Hellingwerf, Photosensing in chemotrophic, non-phototrophic bacteria: let there be light sensing too Trends Microbiol. 2007 15 554–562.
A. Möglich, X. Yang, R. A. Ayers and K. Moffat, Structure and function of plant photoreceptors Annu. Rev. Plant Biol. 2010 61 21–47.
S. M. Harper, L. C. Neil and K. H. Gardner, Structural basis of a phototropin light switch Science 2003 301 1541–1544.
J. M. Christie, Phototropin blue-light receptors Annu. Rev. Plant Biol. 2007 58 21–45.
N. C. Rockwell, Y. S. Su and J. C. Lagarias, Phytochrome structure and signaling mechanisms Annu. Rev. Plant Biol. 2006 57 837–858.
K. A. Franklin and P. H. Quail, Phytochrome functions in Arabidopsis development J. Exp. Bot. 2010 61 11–24.
J. J. Casal, Photoreceptor signaling networks in plant responses to shade Annu. Rev. Plant Biol. 2013 64 403–427.
J. Hughes, Phytochrome cytoplasmic signaling Annu. Rev. Plant Biol. 2013 64 377–402.
N. F. Frankenberg, and J. C. Lagarias, in The Porphyrin Handbook. Chlorophylls and Bilins: Biosynthesis Structure and Degradation, ed. K. M. Kadish, K. M. Smith and R. Guilard, Academic Press, New York, 2003, pp. 211235.
J. Hughes, Phytochrome three-dimensional structures and functions Biochem. Soc. Trans. 2010 38 710–716.
N. C. Rockwell and J. C. Lagarias, A brief history of phytochromes ChemPhysChem 2010 11 1172–1180.
L. Li and J. C. Lagarias, Phytochrome assembly–Defining chromophore structural requirements for covalent attachment and photoreversibility J. Biol. Chem. 1992 267 19204–19210.
B. Borucki, H. Otto, G. Rottwinkel, J. Hughes, M. P. Heyn and T. Lamparter, Mechanism of Cph1 phytochrome assembly from stopped-flow kinetics and circular dichroism Biochemistry 2003 42 13684–13697.
Y. Hirose, R. Narikawa, M. Katayama and M. Ikeuchi, Cyanobacteriochrome CcaS regulates phycoerythrin accumulation in Nostoc punctiforme, a group II chromatic adapter Proc. Natl. Acad. Sci. U. S. A. 2010 107 8854–8859.
N. C. Rockwell, S. S. Martin, K. Feoktistova and J. C. Lagarias, Diverse two-cysteine photocycles in phytochromes and cyanobacteriochromes Proc. Natl. Acad. Sci. U. S. A. 2011 108 11854–11859.
N. C. Rockwell, S. S. Martin, A. G. Gulevich and J. C. Lagarias, Phycoviolobilin formation and spectral tuning in the DXCF cyanobacteriochrome subfamily Biochemistry 2012 51 1449–1463.
N. C. Rockwell, S. S. Martin and J. C. Lagarias, Red/Green Cyanobacteriochromes: Sensors of Color and Power Biochemistry 2012 51 9667–9677.
M. Ikeuchi and T. Ishizuka, Cyanobacteriochromes: a new superfamily of tetrapyrrole-binding photoreceptors in cyanobacteria Photochem. Photobiol. Sci. 2008 7 1159–1167.
E. S. Burgie, J. M. Walker, G. N. Phillips Jr. and R. D. Vierstra, A photo-labile thioether linkage to phycoviolobilin provides the foundation for the blue/green photocycles in DXCF-cyanobacteriochromes Structure 2013 21 88–97.
C. C. Cornilescu, G. Cornilescu, E. S. Burgie, J. L. Markley, A. T. Ulijasz and R. D. Vierstra, Dynamic Structural Changes Underpin Photoconversion of a Blue/Green Cyanobacteriochrome Between its Dark and Photoactivated States J. Biol. Chem. 2014 289 3055–3065.
R. Narikawa, T. Ishizuka, N. Muraki, T. Shiba, G. Kurisu and M. Ikeuchi, Structures of cyanobacteriochromes from phototaxis regulators AnPixJ and TePixJ reveal general and specific photoconversion mechanism Proc. Natl. Acad. Sci. U. S. A. 2013 110 918–923.
G. Enomoto, Y. Hirose, R. Narikawa and M. Ikeuchi, Thiol-based photocycle of the blue and teal light-sensing cyanobacteriochrome Tlr1999 Biochemistry 2012 51 3050–3058.
N. C. Rockwell, S. L. Njuguna, L. Roberts, E. Castillo, V. L. Parson, S. Dwojak, J. C. Lagarias and S. C. Spiller, A second conserved GAF domain cysteine is required for the blue/green photoreversibility of cyanobacteriochrome Tlr0924 from Thermosynechococcus elongatus Biochemistry 2008 47 7304–7316.
T. Ishizuka, A. Kamiya, H. Suzuki, R. Narikawa, T. Noguchi, T. Kohchi, K. Inomata and M. Ikeuchi, The cyanobacteriochrome, TePixJ, isomerizes its own chromophore by converting phycocyanobilin to phycoviolobilin Biochemistry 2011 50 953–961.
N. C. Rockwell, S. S. Martin and J. C. Lagarias, Mechanistic Insight into the Photosensory Versatility of DXCF Cyanobacteriochromes Biochemistry 2012 51 3576–3585.
Y. Hirose, N. C. Rockwell, K. Nishiyama, R. Narikawa, Y. Ukaji, K. Inomata, J. C. Lagarias and M. Ikeuchi, Green/red cyanobacteriochromes regulate complementary chromatic acclimation via a protochromic photocycle Proc. Natl. Acad. Sci. U. S. A. 2013 110 4974–4979.
S. Lim, N. C. Rockwell, S. S. Martin, J. L. Dallas, J. C. Lagarias and J. B. Ames, Photoconversion changes bilin chromophore conjugation and protein secondary structure in the violet/orange cyanobacteriochrome NpF2163g3 Photochem. Photobiol. Sci. 2014 13 951–962.
R. Narikawa, G. Enomoto, W. Ni Ni, K. Fushimi and M. Ikeuchi, A New Type of Dual-Cys Cyanobacteriochrome GAF Domain Found in Cyanobacterium Acaryochloris marina, Which Has an Unusual Red/Blue Reversible Photoconversion Cycle Biochemistry 2014 53 5051–5059.
N. C. Rockwell, S. S. Martin, A. G. Gulevich and J. C. Lagarias, Conserved phenylalanine residues are required for blue-shifting of cyanobacteriochrome photoproducts Biochemistry 2014 53 3118–3130.
C. Mandalari, A. Losi, W. Gärtner, Distance-tree analysis, distribution and co-presence of bilin- and flavin-binding prokaryotic photoreceptors for visible light Photochem. Photobiol. Sci. 2013 12 1144–1157.
J. R. Wagner, J. S. Brunzelle, K. T. Forest and R. D. Vierstra, A light-sensing knot revealed by the structure of the chromophore binding domain of phytochrome Nature 2005 438 325–331.
L. O. Essen, J. Mailliet and J. Hughes, The structure of a complete phytochrome sensory module in the Pr ground state Proc. Natl. Acad. Sci. U. S. A. 2008 105 14709–14714.
K. Anders, G. Daminelli-Widany, M. A. Mroginski, D. von Stetten and L. O. Essen, Structure of the cyanobacterial phytochrome 2 photosensor implies a tryptophan switch for phytochrome signaling J. Biol. Chem. 2013 288 35714–35725.
P. W. Kim, L. H. Freer, N. C. Rockwell, S. S. Martin, J. C. Lagarias and D. S. Larsen, Second-Chance Initiation Dynamics of the Cyanobacterial Photocycle in the NpR6012 GAF4 Domain of Nostoc Punctiforme J. Am. Chem. Soc. 2012 134 130–133.
P. W. Kim, L. H. Freer, N. C. Rockwell, S. S. Martin, J. C. Lagarias and D. S. Larsen, Femtosecond Photodynamics of the Red/Green Cyanobacteriochrome NpR6012g4 from Nostoc punctiforme. 2. Reverse Dynamics Biochemistry 2012 51 619–630.
P. W. Kim, L. H. Freer, N. C. Rockwell, S. S. Martin, J. C. Lagarias and D. S. Larsen, Femtosecond Photodynamics of the Red/Green Cyanobacteriochrome NpR6012g4 from Nostoc punctiforme. 1. Forward Dynamics Biochemistry 2012 51 608–618.
R. Narikawa, Y. Fukushima, T. Ishizuka, S. Itoh and M. Ikeuchi, A novel photoactive GAF domain of cyanobacteriochrome AnPixJ that shows reversible green/red photoconversion J. Mol. Biol. 2008 380 844–855.
Y. Chen, J. Zhang, J. Luo, J. M. Tu, X. L. Zeng, J. **e, M. Zhou, J. Q. Zhao, H. Scheer and K. H. Zhao, Photophysical diversity of two novel cyanobacteriochromes with phycocyanobilin chromophores: photochemistry and dark reversion kinetics FEBS J. 2012 279 40–54.
X. L. Xu, A. Gutt, J. Mechelke, S. Raffelberg, K. Tang, D. Miao, L. Valle, C. D. Borsarelli, K. H. Zhao and W. Gartner, Combined mutagenesis and kinetics characterization of the bilin-binding GAF domain of the protein Slr1393 from the Cyanobacterium Synechocystis PCC6803 ChemBioChem 2014 15 1190–1199.
L. Shang, N. C. Rockwell, S. S. Martin and J. C. Lagarias, Biliverdin amides reveal roles for propionate side chains in bilin reductase recognition and in holophytochrome assembly and photoconversion Biochemistry 2010 49 6070–6082.
T. Dagan, M. Roettger, K. Stucken, G. Landan, R. Koch, P. Major, S. B. Gould, V. V. Goremykin, R. Rippka, N. Tandeau de Marsac, M. Gugger, P. J. Lockhart, J. F. Allen, I. Brune, I. Maus, A. Puhler and W. F. Martin, Genomes of Stigonematalean cyanobacteria (subsection V) and the evolution of oxygenic photosynthesis from prokaryotes to plastids Genome Biol. Evol. 2013 5 31–44.
P. M. Shih, D. Wu, A. Latifi, S. D. Axen, D. P. Fewer, E. Talla, A. Calteau, F. Cai, N. Tandeau de Marsac, R. Rippka, M. Herdman, K. Sivonen, T. Coursin, T. Laurent, L. Goodwin, M. Nolan, K. W. Davenport, C. S. Han, E. M. Rubin, J. A. Eisen, T. Woyke, M. Gugger and C. A. Kerfeld, Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing Proc. Natl. Acad. Sci. U. S. A. 2013 110 1053–1058.
S. F. Altschul, T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller and D. J. Lipman, Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic. Acids Res. 1997 25 3389–3402.
T. Ishizuka, R. Narikawa, T. Kohchi, M. Katayama and M. Ikeuchi, Cyanobacteriochrome TePixJ of Thermosynechococcus elongatus harbors phycoviolobilin as a chromophore Plant Cell Physiol. 2007 48 1385–1390.
F. Velazquez Escobar, T. Utesch, R. Narikawa, M. Ikeuchi, M. A. Mroginski, W. Gartner and P. Hildebrandt, Photoconversion Mechanism of the Second GAF Domain of Cyanobacteriochrome AnPixJ and the Cofactor Structure of Its Green-Absorbing State Biochemistry 2013 52 4871–4880.
S. Yoshihara, M. Katayama, X. Geng and M. Ikeuchi, Cyanobacterial Phytochrome-like PixJ1 Holoprotein Shows Novel Reversible Photoconversion Between Blue- and Green-absorbing Forms Plant Cell Physiol. 2004 45 1729–1737.
R. Narikawa, F. Suzuki, S. Yoshihara, S. I. Higashi, M. Watanabe and M. Ikeuchi, Novel Photosensory Two-Component System (PixA-NixB-NixC) Involved in the Regulation of Positive and Negative Phototaxis of Cyanobacterium Synechocystis sp. PCC 6803 Plant Cell Physiol. 2011 52 2214–2224.
J. Y. Song, H. S. Cho, J. I. Cho, J. S. Jeon, J. C. Lagarias and Y. I. Park, Near-UV cyanobacteriochrome signaling system elicits negative phototaxis in the cyanobacterium Synechocystis sp. PCC 6803 Proc. Natl. Acad. Sci. U. S. A. 2011 108 10780–10785.
S. H. Wu and J. C. Lagarias, Defining the bilin lyase domain: Lessons from the extended phytochrome superfamily Biochemistry 2000 39 13487–13495.
K. Anders, D. von Stetten, J. Mailliet, S. Kiontke, V. A. Sineshchekov, P. Hildebrandt, J. Hughes and L. O. Essen, Spectroscopic and photochemical characterization of the red-light sensitive photosensory module of Cph2 from Synechocystis PCC 6803 Photochem. Photobiol. 2011 87 160–173.
P. Savakis, S. de Causmaecker, V. Angerer, U. Ruppert, K. Anders, L. O. Essen and A. Wilde, Light-induced alteration of c-di-GMP level controls motility of Synechocystis sp. PCC 6803 Mol. Microbiol. 2012 85 239–251.
I. I. Brown, D. A. Bryant, D. Casamatta, K. L. Thomas-Keprta, S. A. Sarkisova, G. Shen, J. E. Graham, E. S. Boyd, J. W. Peters, D. H. Garrison and D. S. McKay, Polyphasic characterization of a thermotolerant siderophilic filamentous cyanobacterium that produces intracellular iron deposits Appl. Environ. Microbiol. 2010 76 6664–6672.
P. Duggan, T. Thiel and D. Adams, Symbiosis between the cyanobacterium Nostoc and the liverwort Blasia requires a CheR-type MCP methyltransferase Symbiosis 2013 59 111–120.
E. L. Campbell, H. Christman and J. C. Meeks, DNA microarray comparisons of plant factor- and nitrogen deprivation-induced Hormogonia reveal decision-making transcriptional regulation patterns in Nostoc punctiforme J. Bacteriol. 2008 190 7382–7391.
F. Gan, S. Zhang, N. C. Rockwell, S. S. Martin, J. C. Lagarias and D. A. Bryant, Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light Science 2014 345 1312–1317.
U. K. Aryal, S. J. Callister, S. Mishra, X. Zhang, J. I. Shutthanandan, T. E. Angel, A. K. Shukla, M. E. Monroe, R. J. Moore, D. W. Koppenaal, R. D. Smith and L. Sherman, Proteome analyses of strains ATCC 51142 and PCC 7822 of the diazotrophic cyanobacterium Cyanothece sp. under culture conditions resulting in enhanced H(2) production Appl. Environ. Microbiol. 2013 79 1070–1077.
D. M. Kehoe and A. R. Grossman, Similarity of a Chromatic Adaptation Sensor to Phytochrome and Ethylene Receptors Science 1996 273 1409–1412.
D. M. Kehoe and A. Gutu, Responding to color: the regulation of complementary chromatic adaptation Annu. Rev. Plant Biol. 2006 57 127–150.
Y. Hirose, T. Shimada, R. Narikawa, M. Katayama and M. Ikeuchi, Cyanobacteriochrome CcaS is the green light receptor that induces the expression of phycobilisome linker protein Proc. Natl. Acad. Sci. U. S. A. 2008 105 9528–9533.
N. C. Rockwell, L. Shang, S. S. Martin and J. C. Lagarias, Distinct classes of red/far-red photochemistry within the phytochrome superfamily Proc. Natl. Acad. Sci. U. S. A. 2009 106 6123–6127.
G. A. Gambetta and J. C. Lagarias, Genetic engineering of phytochrome biosynthesis in bacteria Proc. Natl. Acad. Sci. U. S. A. 2001 98 10566–10571.
B. Miroux and J. E. Walker, Over-production of proteins in Escherichia coli: Mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels J. Mol. Biol. 1996 260 289–298.
K. Mukougawa, H. Kanamoto, T. Kobayashi, A. Yokota and T. Kohchi, Metabolic engineering to produce phytochromes with phytochromobilin, phycocyanobilin, or phycoerythrobilin chromophore in Escherichia coli FEBS Lett. 2006 580 1333–1338.
T. R. Berkelman and J. C. Lagarias, Visualization of bilin-linked peptides and proteins in polyacrylamide gels Anal. Biochem. 1986 156 194–201.
R. C. Edgar, MUSCLE: multiple sequence alignment with high accuracy and high throughput Nucleic Acids Res. 2004 32 1792–1797.
D. G. Higgins, J. D. Thompson and T. J. Gibson, Using CLUSTAL for multiple sequence alignments Methods Enzymol. 1996 266 383–402.
A. J. Fischer, N. C. Rockwell, A. Y. Jang, L. A. Ernst, A. S. Waggoner, Y. Duan, H. Lei and J. C. Lagarias, Multiple roles of a conserved GAF domain tyrosine residue in cyanobacterial and plant phytochromes Biochemistry 2005 44 15203–15215.
J. R. Wagner, J. Zhang, D. von Stetten, M. Gunther, D. H. Murgida, M. A. Mroginski, J. M. Walker, K. T. Forest, P. Hildebrandt and R. D. Vierstra, Mutational Analysis of Deinococcus radiodurans Bacteriophytochrome Reveals Key Amino Acids Necessary for the Photochromicity and Proton Exchange Cycle of Phytochromes J. Biol. Chem. 2008 283 12212–12226.
A. T. Ulijasz, G. Cornilescu, D. von Stetten, S. Kaminski, M. A. Mroginski, J. Zhang, D. Bhaya, P. Hildebrandt and R. D. Vierstra, Characterization of two thermostable cyanobacterial phytochromes reveals global movements in the chromophore-binding domain during photoconversion J. Biol. Chem. 2008 283 21251–21266.
N. C. Rockwell, D. Duanmu, S. S. Martin, C. Bachy, D. C. Price, D. Bhattacharya, A. Z. Worden and J. C. Lagarias, Eukaryotic algal phytochromes span the visible spectrum Proc. Natl. Acad. Sci. U. S. A. 2014 111 3871–3876.
Author information
Authors and Affiliations
Corresponding author
Additional information
Electronic supplementary information (ESI) available. See DOI: 10.1039/c4pp00336e
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1039/c4pp00336e