Browse > Article
http://dx.doi.org/10.14348/molcells.2020.0077

Color Sensing and Signal Transmission Diversity of Cyanobacterial Phytochromes and Cyanobacteriochromes  

Villafani, Yvette (Department of Biological Sciences, Chungnam National University)
Yang, Hee Wook (Department of Biological Sciences, Chungnam National University)
Park, Youn-Il (Department of Biological Sciences, Chungnam National University)
Abstract
To perceive fluctuations in light quality, quantity, and timing, higher plants have evolved diverse photoreceptors including UVR8 (a UV-B photoreceptor), cryptochromes, phototropins, and phytochromes (Phys). In contrast to plants, prokaryotic oxygen-evolving photosynthetic organisms, cyanobacteria, rely mostly on bilin-based photoreceptors, namely, cyanobacterial phytochromes (Cphs) and cyanobacteriochromes (CBCRs), which exhibit structural and functional differences compared with plant Phys. CBCRs comprise varying numbers of light sensing domains with diverse color-tuning mechanisms and signal transmission pathways, allowing cyanobacteria to respond to UV-A, visible, and far-red lights. Recent genomic surveys of filamentous cyanobacteria revealed novel CBCRs with broader chromophore-binding specificity and photocycle protochromicity. Furthermore, a novel Cph lineage has been identified that absorbs blue-violet/yellow-orange light. In this minireview, we briefly discuss the diversity in color sensing and signal transmission mechanisms of Cphs and CBCRs, along with their potential utility in the field of optogenetics.
Keywords
color sensing; cyanobacteria; cyanobacterial phytochromes; cyanobacteriochromes; signal transmission;
Citations & Related Records
Times Cited By KSCI : 2  (Citation Analysis)
연도 인용수 순위
1 Agostoni, M., Waters, C.M., and Montgomery, B.L. (2016). Regulation of biofilm formation and cellular buoyancy through modulating intracellular cyclic di-GMP levels in engineered cyanobacteria. Biotechnol. Bioeng. 113, 311-319.   DOI
2 Allen, R., Rittmann, B.E., and Curtiss, R. (2019). Axenic biofilm formation and aggregation by Synechocystis sp. strain PCC 6803 are induced by changes in nutrient concentration and require cell surface structures. Appl. Environ. Microbiol. 85, 1-33.
3 Bhaya, D. (2004). Light matters: phototaxis and signal transduction in unicellular cyanobacteria. Mol. Microbiol. 53, 745-754.   DOI
4 Rastogi, R.P., Sinha, R.P., Moh, S.H., Lee, T.K., Kottuparambil, S., Kim, Y.J., Rhee, J.S., Choi, E.M., Brown, M.T., Hader, D.P., et al. (2014). Ultraviolet radiation and cyanobacteria. J. Photochem. Photobiol. 141, 154-169.   DOI
5 Rockwell, N.C. and Lagarias, J.C. (2010). A brief history of phytochromes. Chemphyschem 11, 1172-1180.   DOI
6 Rockwell, N.C., Martin, S.S., Gulevich, A.G., and Lagarias, J.C. (2012). Phycoviolobilin formation and spectral tuning in the DXCF cyanobacteriochrome subfamily. Biochemistry 51, 1449-1463.   DOI
7 Blain-Hartung, M., Rockwell, N.C., Moreno, M.V., Martin, S.S., Gan, F., Bryant, D.A., and Lagarias, J.C. (2018). Cyanobacteriochrome-based photoswitchable adenylyl cyclases (cPACs) for broad spectrum light regulation of cAMP levels in cells. J. Biol. Chem. 293, 8473-8483.   DOI
8 Rockwell, N.C. and Lagarias, J.C. (2017). Phytochrome diversification in cyanobacteria and eukaryotic algae. Curr. Opin. Plant Biol. 37, 87-93.   DOI
9 Rockwell, N.C. and Lagarias, J.C. (2020). Phytochrome evolution in 3D: deletion, duplication, and diversification. New Phytol. 225, 2283-2300.   DOI
10 Rockwell, N.C., Martin, S.S., Feoktistova, K., and Lagarias, J.C. (2011). Diverse two-cysteine photocycles in phytochromes and cyanobacteriochromes. Proc. Natl. Acad. Sci. U. S. A. 108, 11854-11859.   DOI
11 Ramakrishnan, P. and Tabor, J.J. (2016). Repurposing Synechocystis PCC6803 UirS-UirR as a UV-violet/green photoreversible transcriptional regulatory tool in E. coli. ACS Synth. Biol. 5, 733-740.   DOI
12 Rockwell, N.C., Martin, S.S., Gulevich, A.G., and Lagarias, J.C. (2014). Conserved phenylalanine residues are required for blue-shifting of cyanobacteriochrome photoproducts. Biochemistry 53, 3118-3130.   DOI
13 Rockwell, N.C., Martin, S.S., and Lagarias, J.C. (2015). Identification of DXCF cyanobacteriochrome lineages with predictable photocycles. Photochem. Photobiol. Sci. 14, 929-941.   DOI
14 Rockwell, N.C., Martin, S.S., and Lagarias, J.C. (2016). Identification of cyanobacteriochromes detecting far-red light. Biochemistry 55, 3907-3919.   DOI
15 Chernov, K.G., Redchuk, T.A., Omelina, E.S., and Verkhusha, V.V. (2017). Near-infrared fluorescent proteins, biosensors, and optogenetic tools engineered from phytochromes. Chem. Rev. 117, 6423-6446.   DOI
16 Sato, T., Kikukawa, T., Miyoshi, R., Kajimoto, K., Yonekawa, C., Fujisawa, T., Unno, M., Eki, T., and Hirose, Y. (2019). Protochromic absorption changes in the two-cysteine photocycle of a blue/orange cyanobacteriochrome. J. Biol. Chem. 294, 18909-18922.   DOI
17 Buhrke, D., Battocchio, G., Wilkening, S., Blain-Hartung, M., Baumann, T., Schmitt, F.J., Friedrich, T., Mroginski, M.A., and Hildebrandt, P. (2020). Red, orange, green: light- and temperature-dependent color tuning in a cyanobacteriochrome. Biochemistry 59, 509-519.   DOI
18 Campbell, E.L., Hagen, K.D., Chen, R., Risser, D.D., Ferreira, D.P., and Meeks, J.C. (2015). Genetic analysis reveals the identity of the photoreceptor for phototaxis in hormogonium filaments of Nostoc punctiforme. J. Bacteriol. 197, 782-791.   DOI
19 Castillo-Hair, S.M., Baerman, E.A., Fujita, M., Igoshin, O.A., and Tabor, J.J. (2019). Optogenetic control of Bacillus subtilis gene expression. Nat. Commun. 10, 3099.   DOI
20 Chen, Y., Zhang, J., Luo, J., Tu, J.M., Zeng, X.L., Xie, J., Zhou, M., Zhao, J.Q., Scheer, H., and Zhao, K.H. (2012). Photophysical diversity of two novel cyanobacteriochromes with phycocyanobilin chromophores: photochemistry and dark reversion kinetics. FEBS J. 279, 40-54.   DOI
21 Song, J.Y., Lee, H.Y., Yang, H.W., Song, J.J., Lagarias, J.C., and Park, Y.I. (2020). Spectral and photochemical diversity of tandem cysteine cyanobacterial phytochromes. J. Biol. Chem. 295, 6754-6766.   DOI
22 Schwarzkopf, M., Yoo, Y.C., Huckelhoven, R., Park, Y.M., and Proels, R.K. (2014). Cyanobacterial phytochrome2 regulates heterotrophic metabolism and has a function in the heat and high-light stress response. Plant Physiol. 164, 2157-2166.   DOI
23 Sinha, R.P. and Hader, D.P. (2008). UV-protectants in cyanobacteria. Plant Sci. 174, 278-289.   DOI
24 Song, J.Y., Cho, H.S., Cho, J.I., Jeon, J.S., Lagarias, J.C., and Park, Y.I. (2011). Near-UV cyanobacteriochrome signaling system elicits negative phototaxis in the cyanobacterium Synechocystis sp. PCC 6803. Proc. Natl. Acad. Sci. U. S. A. 108, 10780-10785.   DOI
25 Tandar, S.T., Senoo, S., Toya, Y., and Shimizu, H. (2019). Optogenetic switch for controlling the central metabolic flux of Escherichia coli. Metab. Eng. 55, 68-75.   DOI
26 Wagner, J.R., Zhang, J., von Stetten, D., Gunther, M., Murgida, D.H., Mroginski, M.A., Walker, J.M., Forest, K.T., Hildebrandt, P., and Vierstra, R.D. (2008). Mutational analysis of Deinococcus radiodurans bacteriophytochrome reveals key amino acids necessary for the photochromicity and proton exchange cycle of phytochromes. J. Biol. Chem. 283, 12212-12226.   DOI
27 Sanfilippo, J.E., Garczarek, L., Partensky, F., and Kehoe, D.M. (2019). Chromatic acclimation in cyanobacteria: a diverse and widespread process for optimizing photosynthesis. Ann. Rev. Microbiol. 73, 407-433.   DOI
28 Cohen, S.E. and Golden, S.S. (2015). Circadian rhythms in cyanobacteria. Microbiol. Mol. Biol. Rev. 79, 373-385.   DOI
29 Cho, S.M., Jeoung, S.C., Song, J.Y., Kupriyanova, E.V., Pronina, N.A., Lee, B.W., Jo, S.W., Park, B.S., Choi, S.B., Song, J.J., et al. (2015). Genomic survey and biochemical analysis of recombinant candidate cyanobacteriochromes reveals enrichment for near UV/violet sensors in the halotolerant and alkaliphilic cyanobacterium Microcoleus IPPAS B353. J. Biol. Chem. 290, 28502-28514.   DOI
30 Cho, S.M., Jeoung, S.C., Song, J.Y., Song, J.J., and Park, Y.I. (2017). Hydrophobic residues near the bilin chromophore-binding pocket modulate spectral tuning of insert-Cys subfamily cyanobacteriochromes. Sci. Rep. 7, 1-12.   DOI
31 Xu, X., Port, A., Wiebeler, C., Zhao, K.H., Schapiro, I., and Gärtner, W. (2020). Structural elements regulating the photochromicity in a cyanobacteriochrome. Proc. Natl. Acad. Sci. U. S. A. 117, 2432-2440.   DOI
32 Wendt, K.E. and Pakrasi, H.B. (2019). Genomics approaches to deciphering natural transformation in cyanobacteria. Front. Microbiol. 10, 1259.   DOI
33 Wilde, A., Fiedler, B., and Borner, T. (2002). The cyanobacterial phytochrome Cph2 inhibits phototaxis towards blue light. Mol. Microbiol. 44, 981-988.   DOI
34 Wiltbank, L.B. and Kehoe, D.M. (2019). Diverse light responses of cyanobacteria mediated by phytochrome superfamily photoreceptors. Nat. Rev. Microbiol. 17, 37-50.   DOI
35 Yang, G., Cozad, M.A., Holland, D.A., Zhang, Y., Luesch, H., and Ding, Y. (2018a). Photosynthetic production of sunscreen shinorine using an engineered cyanobacterium. ACS Synth. Biol. 7, 664-671.   DOI
36 Yang, H.W., Song, J.Y., Cho, S.M., Kwon, H.C., Pan, C.H., and Park, Y.I. (2020). Genomic survey of salt acclimation-related genes in the halophilic cyanobacterium Euhalothece sp. Z-M001. Sci. Rep. 10, 676.   DOI
37 Yang, Y., Lam, V., Adomako, M., Simkovsky, R., Jakob, A., Rockwell, N.C., Cohen, S.E., Taton, A., Wang, J., Lagarias, J.C., et al. (2018b). Phototaxis in a wild isolate of the cyanobacterium Synechococcus elongatus. Proc. Natl. Acad. Sci. U. S. A. 115, E12378-E12387.   DOI
38 Yeh, K.C., Wu, S.H., Murphy, J.T., and Lagarias, J.C. (1997). A cyanobacterial phytochrome two-component light sensory system. Science 277, 1505-1508.   DOI
39 Yoshihara, S. and Ikeuchi, M. (2004). Phototactic motility in the unicellular cyanobacterium Synechocystis sp. PCC 6803. Photochem. Photobiol. Sci. 3, 512-518.   DOI
40 Damerval, T., Guglielmi, G., Houmard, J., and de Marsac, N.T. (2007). Hormogonium differentiation in the cyanobacterium Calothrix : a photoregulated developmental process. Plant Cell 3, 191-201.   DOI
41 Evans, K., Fordham-Skelton, A.P., Mistry, H., Reynolds, C.D., Lawless, A.M., and Papiz, M.Z. (2005). A bacteriophytochrome regulates the synthesis of LH4 complexes in Rhodopseudomonas palustris. Photosynth. Res. 85, 169-180.   DOI
42 Enomoto, G. and Ikeuchi, M. (2020). Blue-/green-light-responsive cyanobacteriochromes are cell shade sensors in red-light replete niches. iScience 23, 100936.   DOI
43 Enomoto, G., Ni-Ni-Win, Narikawa, R., and Ikeuchi, M. (2015). Three cyanobacteriochromes work together to form a light color-sensitive input system for c-di-GMP signaling of cell aggregation. Proc. Natl. Acad. Sci. U. S. A. 112, 8082-8087.   DOI
44 Enomoto, G., Nomura, R., Shimada, T., Win, N.N., Narikawa, R., and Ikeuchi, M. (2014). Cyanobacteriochrome SesA is a diguanylate cyclase that induces cell aggregation in Thermosynechococcus. J. Biol. Chem. 289, 24801-24809.   DOI
45 Fischer, A.J., Rockwell, N.C., Jang, A.Y., Ernst, L.A., Alan, S., Duan, Y., Lei, H., and Lagarias, J.C. (2005). Multiple roles of a conserved GAF domain tyrosine residue in cyanobacterial and plant phytochromes. Biochemistry 44, 15203-15215.   DOI
46 Fiedler, B., Broc, D., Schubert, H., Rediger, A., Börner, T., and Wilde, A. (2007). Involvement of cyanobacterial phytochromes in growth under different light qualitities and quantities. Photochem. Photobiol. 79, 551-555.   DOI
47 Franklin, K.A. and Quail, P.H. (2010). Phytochrome functions in Arabidopsis development. J. Exp. Bot. 61, 11-24.   DOI
48 Fujita, Y., Tsujimoto, R., and Aoki, R. (2015). Evolutionary aspects and regulation of tetrapyrrole biosynthesis in cyanobacteria under aerobic and anaerobic environments. Life 5, 1172-1203.   DOI
49 Fushimi, K., Miyazaki, T., Kuwasaki, Y., Nakajima, T., Yamamoto, T., Suzuki, K., Ueda, Y., Miyake, K., Takeda, Y., Choi, J.H., et al. (2019). Rational conversion of chromophore selectivity of cyanobacteriochromes to accept mammalian intrinsic biliverdin. Proc. Natl. Acad. Sci. U. S. A. 116, 8301-8309.   DOI
50 Yoshihara, S., Katayama, M., Geng, X., and Ikeuchi, M. (2004). Cyanobacterial phytochrome-like PixJ1 holoprotein dhows novel reversible photoconversion between blue- and green-absorbing forms. Plant Cell Physiol. 45, 1729-1737.   DOI
51 Fushimi, K., Nakajima, T., Aono, Y., Yamamoto, T., Win, N.N., Ikeuchi, M., Sato, M., and Narikawa, R. (2016). Photoconversion and fluorescence properties of a red/green-type cyanobacteriochrome AM1_C0023g2 that binds not only phycocyanobilin but also biliverdin. Front. Microbiol. 7, 588.   DOI
52 Fushimi, K. and Narikawa, R. (2019). Cyanobacteriochromes: photoreceptors covering the entire UV-to-visible spectrum. Curr. Opin. Struct. Biol. 57, 39-46.   DOI
53 He, Q., Tang, Q.Y., Sun, Y.F., Zhou, M., Gärtner, W., and Zhao, K.H. (2018). Chromophorylation of cyanobacteriochrome Slr1393 from Synechocystis sp. PCC 6803 is regulated by protein Slr2111 through allosteric interaction. J. Biol. Chem. 293, 17705-17715.   DOI
54 Hirose, Y., Narikawa, R., Katayama, M., and Ikeuchi, M. (2010). Cyanobacteriochrome CcaS regulates phycoerythrin accumulation in Nostoc punctiforme, a group II chromatic adapter. Proc. Natl. Acad. Sci. U. S. A. 107, 8854-8859.   DOI
55 Hirose, Y., Rockwell, N.C., Nishiyama, K., Narikawa, R., Ukaji, Y., Inomata, K., Lagarias, J.C., and Ikeuchi, M. (2013). Green/red cyanobacteriochromes regulate complementary chromatic acclimation via a protochromic photocycle. Proc. Natl. Acad. Sci. U. S. A. 110, 4974-4979.   DOI
56 Hirose, Y., Shimada, T., Narikawa, R., Katayama, M., and Ikeuchi, M. (2008). Cyanobacteriochrome CcaS is the green light receptor that induces the expression of phycobilisome linker protein. Proc. Natl. Acad. Sci. U. S. A. 105, 9528-9533.   DOI
57 Ishizuka, T., Narikawa, R., Kohchi, T., Katayama, M., and Ikeuchi, M. (2007). Cyanobacteriochrome TePixJ of Thermosynechococcus elongatus harbors phycoviolobilin as a chromophore. Plant Cell Physiol. 48, 1385-1390.   DOI
58 Hwang, D.Y., Park, S., Lee, S., Lee, S.S., Imaizumi, T., and Song, Y.H. (2019). GIGANTEA regulates the timing stabilization of CONSTANS by altering the interaction between FKF1 and ZEITLUPE. Mol. Cells 42, 693-701.   DOI
59 Ikeuchi, M. and Ishizuka, T. (2008). Cyanobacteriochromes: a new superfamily of tetrapyrrole-binding photoreceptors in cyanobacteria. Photochem. Photobiol. Sci. 7, 1159-1167.   DOI
60 Ishizuka, T., Kamiya, A., Suzuki, H., Narikawa, R., Noguchi, T., Kohchi, T., Inomata, K., and Ikeuchi, M. (2011). The cyanobacteriochrome, TePixJ, isomerizes its own chromophore by converting phycocyanobilin to phycoviolobilin. Biochemistry 50, 953-961.   DOI
61 Ishizuka, T., Shimada, T., Okajima, K., Yoshihara, S., Ochiai, Y., Katayama, M., and Ikeuchi, M. (2006). Characterization of cyanobacteriochrome TePixJ from a thermophilic cyanobacterium Thermosynechococcus elongatus strain BP-1. Plant Cell Physiol. 47, 1251-1261.   DOI
62 Khayatan, B., Meeks, J.C., and Risser, D.D. (2015). Evidence that a modified type IV pilus-like system powers gliding motility and polysaccharide secretion in filamentous cyanobacteria. Mol. Microbiol. 98, 1021-1036.   DOI
63 Klausen, C., Kaiser, F., Stüven, B., Hansen, J.N., and Wachten, D. (2019). Elucidating cyclic AMP signaling in subcellular domains with optogenetic tools and fluorescent biosensors. Biochem. Soc. Trans. 47, 1733-1747.   DOI
64 Lim, S., Yu, Q., Gottlieb, S.M., Chang, C.W., Rockwell, N.C., Martin, S.S., Madsen, D., Lagarias, J.C., and Ames, J.B. (2018). Correlating structural and photochemical heterogeneity in cyanobacteriochrome NpR6012g4. Proc. Natl. Acad. Sci. U. S. A. 115, 4387-4392.   DOI
65 Narikawa, R., Nakajima, T., Aono, Y., Fushimi, K., Enomoto, G., Itoh, S., Sato, M., and Ikeuchi, M. (2015). A biliverdin-binding cyanobacteriochrome from the chlorophyll d-bearing cyanobacterium Acaryochloris marina. Sci. Rep. 5, 1-10.
66 Maldener, I., Summers, M.L., and Sukenik, A. (2014). Cellular differentiation in filamentous cyanobacteria. In The Cell Biology of Cyanobacteria, E. Flores and A. Herrero, eds. (London, United Kingdom: Academic Press), pp. 263-291.
67 Marsac, N.T. (1994). Differentiation of hormogonia and relationships with other biological processes. In The Molecular Biology of Cyanobacteria, D.A. Bryant, ed. (Dordrecht, Netherlands: Kluwer Academic), pp. 825-842.
68 Milias-Argeitis, A., Rullan, M., Aoki, S.K., Buchmann, P., and Khammash, M. (2016). Automated optogenetic feedback control for precise and robust regulation of gene expression and cell growth. Nat. Commun. 7, 1-11.
69 Narikawa, R., Enomoto, G., Ni Ni, W., Fushimi, K., and Ikeuchi, M. (2014). A new type of dual-cys cyanobacteriochrome GAF domain found in cyanobacterium Acaryochloris marina, which has an unusual red/blue reversible photoconversion cycle. Biochemistry 53, 5051-5059.   DOI
70 Narikawa, R., Fukushima, Y., Ishizuka, T., Itoh, S., and Ikeuchi, M. (2008). A novel photoactive GAF domain of cyanobacteriochrome AnPixJ that shows reversible green/red photoconversion. J. Mol. Biol. 380, 844-855.   DOI
71 Oliinyk, O.S., Shemetov, A.A., Pletnev, S., Shcherbakova, D.M., and Verkhusha, V.V. (2019). Smallest near-infrared fluorescent protein evolved from cyanobacteriochrome as versatile tag for spectral multiplexing. Nat. Commun. 10, 279.   DOI
72 Ong, N.T., Olson, E.J., and Tabor, J.J. (2018). Engineering an E. coli nearinfrared light sensor. ACS Synth. Biol. 7, 240-248.   DOI