Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지
DOI QR코드

DOI QR Code

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)
  • Received : 2020.03.24
  • Accepted : 2020.04.28
  • Published : 2020.06.30
Download PDF
⟨ Previous Next ⟩

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

References

  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. https://doi.org/10.1002/bit.25712
  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. https://doi.org/10.1111/j.1365-2958.2004.04160.x
  4. 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. https://doi.org/10.1074/jbc.RA118.002258
  5. 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. https://doi.org/10.1021/acs.biochem.9b00931
  6. 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. https://doi.org/10.1128/JB.02374-14
  7. 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. https://doi.org/10.1038/s41467-019-10906-6
  8. 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. https://doi.org/10.1111/j.1742-4658.2011.08397.x
  9. 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. https://doi.org/10.1021/acs.chemrev.6b00700
  10. 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. https://doi.org/10.1074/jbc.M115.669150
  11. 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. https://doi.org/10.1038/s41598-016-0028-x
  12. Cohen, S.E. and Golden, S.S. (2015). Circadian rhythms in cyanobacteria. Microbiol. Mol. Biol. Rev. 79, 373-385. https://doi.org/10.1128/MMBR.00036-15
  13. 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. https://doi.org/10.1105/tpc.3.2.191
  14. Enomoto, G. and Ikeuchi, M. (2020). Blue-/green-light-responsive cyanobacteriochromes are cell shade sensors in red-light replete niches. iScience 23, 100936. https://doi.org/10.1016/j.isci.2020.100936
  15. 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. https://doi.org/10.1073/pnas.1504228112
  16. 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. https://doi.org/10.1074/jbc.M114.583674
  17. 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. https://doi.org/10.1007/s11120-005-1369-7
  18. 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. https://doi.org/10.1021/bi051633z
  19. 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. https://doi.org/10.1111/j.1751-1097.2004.tb01275.x
  20. Franklin, K.A. and Quail, P.H. (2010). Phytochrome functions in Arabidopsis development. J. Exp. Bot. 61, 11-24. https://doi.org/10.1093/jxb/erp304
  21. 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. https://doi.org/10.3390/life5021172
  22. 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. https://doi.org/10.1073/pnas.1818836116
  23. 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. https://doi.org/10.3389/fmicb.2016.00588
  24. Fushimi, K. and Narikawa, R. (2019). Cyanobacteriochromes: photoreceptors covering the entire UV-to-visible spectrum. Curr. Opin. Struct. Biol. 57, 39-46. https://doi.org/10.1016/j.sbi.2019.01.018
  25. 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. https://doi.org/10.1074/jbc.RA118.003830
  26. 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. https://doi.org/10.1073/pnas.1000177107
  27. 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. https://doi.org/10.1073/pnas.1302909110
  28. 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. https://doi.org/10.1073/pnas.0801826105
  29. 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. https://doi.org/10.14348/molcells.2019.0199
  30. Ikeuchi, M. and Ishizuka, T. (2008). Cyanobacteriochromes: a new superfamily of tetrapyrrole-binding photoreceptors in cyanobacteria. Photochem. Photobiol. Sci. 7, 1159-1167. https://doi.org/10.1039/b802660m
  31. 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. https://doi.org/10.1021/bi101626t
  32. 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. https://doi.org/10.1093/pcp/pcm106
  33. 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. https://doi.org/10.1093/pcp/pcj095
  34. 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. https://doi.org/10.1111/mmi.13205
  35. 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. https://doi.org/10.1042/BST20190246
  36. 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. https://doi.org/10.1073/pnas.1720682115
  37. 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.
  38. 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.
  39. 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.
  40. 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. https://doi.org/10.1021/bi500376b
  41. 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. https://doi.org/10.1016/j.jmb.2008.05.035
  42. 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.
  43. 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. https://doi.org/10.1038/s41467-018-08050-8
  44. Ong, N.T., Olson, E.J., and Tabor, J.J. (2018). Engineering an E. coli nearinfrared light sensor. ACS Synth. Biol. 7, 240-248. https://doi.org/10.1021/acssynbio.7b00289
  45. 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. https://doi.org/10.1021/acssynbio.6b00068
  46. 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. https://doi.org/10.1016/j.jphotobiol.2014.09.020
  47. Rockwell, N.C. and Lagarias, J.C. (2010). A brief history of phytochromes. Chemphyschem 11, 1172-1180. https://doi.org/10.1002/cphc.200900894
  48. Rockwell, N.C. and Lagarias, J.C. (2017). Phytochrome diversification in cyanobacteria and eukaryotic algae. Curr. Opin. Plant Biol. 37, 87-93. https://doi.org/10.1016/j.pbi.2017.04.003
  49. Rockwell, N.C. and Lagarias, J.C. (2020). Phytochrome evolution in 3D: deletion, duplication, and diversification. New Phytol. 225, 2283-2300. https://doi.org/10.1111/nph.16240
  50. 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. https://doi.org/10.1073/pnas.1107844108
  51. 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. https://doi.org/10.1021/bi201783j
  52. 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. https://doi.org/10.1021/bi500037a
  53. 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. https://doi.org/10.1039/C4PP00486H
  54. Rockwell, N.C., Martin, S.S., and Lagarias, J.C. (2016). Identification of cyanobacteriochromes detecting far-red light. Biochemistry 55, 3907-3919. https://doi.org/10.1021/acs.biochem.6b00299
  55. 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. https://doi.org/10.1146/annurev-micro-020518-115738
  56. 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. https://doi.org/10.1074/jbc.RA119.010384
  57. 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. https://doi.org/10.1104/pp.113.233270
  58. Sinha, R.P. and Hader, D.P. (2008). UV-protectants in cyanobacteria. Plant Sci. 174, 278-289. https://doi.org/10.1016/j.plantsci.2007.12.004
  59. 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. https://doi.org/10.1073/pnas.1104242108
  60. 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. https://doi.org/10.1074/jbc.RA120.012950
  61. 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. https://doi.org/10.1016/j.ymben.2019.06.002
  62. 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. https://doi.org/10.1074/jbc.M709355200
  63. Wendt, K.E. and Pakrasi, H.B. (2019). Genomics approaches to deciphering natural transformation in cyanobacteria. Front. Microbiol. 10, 1259. https://doi.org/10.3389/fmicb.2019.01259
  64. Wilde, A., Fiedler, B., and Borner, T. (2002). The cyanobacterial phytochrome Cph2 inhibits phototaxis towards blue light. Mol. Microbiol. 44, 981-988. https://doi.org/10.1046/j.1365-2958.2002.02923.x
  65. Wiltbank, L.B. and Kehoe, D.M. (2019). Diverse light responses of cyanobacteria mediated by phytochrome superfamily photoreceptors. Nat. Rev. Microbiol. 17, 37-50. https://doi.org/10.1038/s41579-018-0110-4
  66. 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. https://doi.org/10.1073/pnas.1910208117
  67. 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. https://doi.org/10.1021/acssynbio.7b00397
  68. 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. https://doi.org/10.1038/s41598-020-57546-1
  69. 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. https://doi.org/10.1073/pnas.1812871115
  70. 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. https://doi.org/10.1126/science.277.5331.1505
  71. Yoshihara, S. and Ikeuchi, M. (2004). Phototactic motility in the unicellular cyanobacterium Synechocystis sp. PCC 6803. Photochem. Photobiol. Sci. 3, 512-518. https://doi.org/10.1039/b402320j
  72. 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. https://doi.org/10.1093/pcp/pch214