A biliverdin-binding cyanobacteriochrome from the chlorophyll d-bearing cyanobacterium Acaryochloris marina

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Narikawa, Rei ^a,b,c   Nakajima, Takahiro ^b   Aono, Yuki ^b   Fushimi, Keiji ^a   Enomoto, Gen ^b   Ni Ni Win, ^b   Itoh, Shigeru ^d   Sato, Moritoshi ^b   Ikeuchi, Masahiko ^b,c  

^a SHIZUOKA UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BILIVERDIN; CHLOROPHYLL; CHLOROPHYLL D; PHYCOBILIN; PHYCOCYANIN; PHYCOCYANOBILIN; PHYCOVIOLOBILIN; PROTEIN BINDING; VISUAL PROTEINS AND PIGMENTS;

CHEMISTRY; CYANOBACTERIUM; LIGHT; METABOLISM;

BILIVERDINE; CHLOROPHYLL; CYANOBACTERIA; LIGHT; PHOTORECEPTORS, MICROBIAL; PHYCOBILINS; PHYCOCYANIN; PROTEIN BINDING;

EID: 84928712660     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep07950     Document Type: Article

References (57)

1. Narikawa, R., Enomoto, G., Ni Ni, W., Fushimi, K., Ikeuchi, M. 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:10.1021/bi500376b (2014).
2. Rockwell, N. C., Martin, S. S., Lagarias, J. C. Red/Green cyanobacteriochromes: sensors of color and power. Biochemistry 51, 9667-9677, doi:10.1021/bi3013565 (2012).
3. Rockwell, N. C., Martin, S. S., Lagarias, J. C. Mechanistic insight into the photosensory versatility of DXCF cyanobacteriochromes. Biochemistry 51, 3576-3585, doi:10.1021/bi300171s (2012).
4. Rockwell, N. C., Martin, S. S., Gulevich, A. G., Lagarias, J. C. Phycoviolobilin formation and spectral tuning in the DXCF cyanobacteriochrome subfamily. Biochemistry 51, 1449-1463, doi:10.1021/bi201783j (2012).
5. Narikawa, R. et al. Novel photosensory two-component system (PixA-NixBNixC) involved in the regulation of positive and negative phototaxis of cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol. 52, 2214-2224, doi:10.1093/pcp/pcr155 (2011).
6. Rockwell, N. C. et al. A second conserved GAF domain cysteine is required for the blue/green photoreversibility of cyanobacteriochrome Tlr0924 from Thermosynechococcus elongatus. Biochemistry 47, 7304-7316, doi:10.1021/bi800088t (2008).
7. Narikawa, R., Kohchi, T., Ikeuchi, M. Characterization of the photoactive GAF domain of the CikA homolog (SyCikA, Slr1969) of the cyanobacterium Synechocystis sp. PCC 6803. Photochem. Photobiol. Sci. 7, 1253-1259, doi:10.1039/b811214b (2008).
8. Narikawa, R., Fukushima, Y., Ishizuka, T., Itoh, S., Ikeuchi, M. A novel photoactive GAF domain of cyanobacteriochrome AnPixJ that shows reversible green/red photoconversion. J. Mol. Biol. 380, 844-855, doi:10.1016/j.jmb.2008.05.035 (2008).
9. Hirose, Y., Shimada, T., Narikawa, R., Katayama, M., Ikeuchi, M. 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 (2008).
10. Ishizuka, T. et al. Characterization of cyanobacteriochrome TePixJ from a thermophilic cyanobacterium Thermosynechococcus elongatus strain BP-1. Plant Cell Physiol. 47, 1251-1261 (2006).
11. Yoshihara, S., Katayama, M., Geng, X., Ikeuchi, M. Cyanobacterial phytochrome-like PixJ1 holoprotein shows novel reversible photoconversion between blue-and green-absorbing forms. Plant Cell Physiol. 45, 1729-1737 (2004).
12. Ma, Q. et al. A rising tide of blue-absorbing biliprotein photoreceptors: characterization of seven such bilin-binding GAF domains in Nostoc sp. PCC7120. FEBS J. 279, 4095-4108, doi:10.1111/febs.12003 (2012).
13. Savakis, P. et al. Light-induced alteration of c-di-GMP level controls motility of Synechocystis sp. PCC 6803. Mol. Microbiol. 85, 239-251, doi:10.1111/j.1365-2958.2012.08106.x (2012).
14. Song, J. Y. et al. 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:10.1073/pnas.1104242108 (2011).
15. Hirose, Y.,Narikawa, R., Katayama, M., Ikeuchi, M. Cyanobacteriochrome CcaS regulates phycoerythrin accumulation in Nostoc punctiforme, a group II chromatic adapter. Proc. Natl. Acad. Sci. U. S. A. 107, 8854-8859, doi:10.1073/pnas.1000177107 (2010).
16. Enomoto, G. et al. Cyanobacteriochrome SesA is a diguanylate cyclase that induces cell aggregation in Thermosynechococcus. J. Biol. Chem. 289, 24801-24809, doi:10.1074/jbc.M114.583674 (2014).
17. Rockwell, N. C.,Martin, S. S., Feoktistova, K.& Lagarias, J. C. Diverse two-cysteine photocycles in phytochromes and cyanobacteriochromes. Proc. Natl. Acad. Sci. U. S. A. 108, 11854-11859, doi:10.1073/pnas.1107844108 (2011).
18. Ishizuka, T. et al. The cyanobacteriochrome, TePixJ, isomerizes its own chromophore by converting phycocyanobilin to phycoviolobilin. Biochemistry 50, 953-961, doi:10.1021/bi101626t (2011).
19. Hirose, Y. et al. Green/red cyanobacteriochromes regulate complementary chromatic acclimation via a protochromic photocycle. Proc. Natl. Acad. Sci. U. S. A. 110, 4974-4979, doi:10.1073/pnas.1302909110 (2013).
20. Chen, Y. et al. Photophysical diversity of two novel cyanobacteriochromes with phycocyanobilin chromophores: photochemistry and dark reversion kinetics. FEBS J. 279, 40-54, doi:10.1111/j.1742-4658.2011.08397.x (2012).
21. Kim, P. W. et al. Second-chance forward isomerization dynamics of the red/green cyanobacteriochrome NpR6012g4 from Nostoc punctiforme. J. Am. Chem. Soc. 134, 130-133, doi:10.1021/ja209533x (2011).
22. Kim, P. W. et al. Femtosecond photodynamics of the red/green cyanobacteriochrome NpR6012g4 from Nostoc punctiforme. 1. Forward dynamics. Biochemistry 51, 608-618, doi:10.1021/bi201507k (2011).
23. Kim, P. W. et al. Femtosecond photodynamics of the red/green cyanobacteriochrome NpR6012g4 from Nostoc punctiforme. 2. reverse dynamics. Biochemistry 51, 619-630, doi:10.1021/bi2017365 (2011).
24. Fukushima, Y. et al. Photoconversion mechanism of a green/red photosensory cyanobacteriochrome AnPixJ: time-resolved optical spectroscopy and FTIR analysis of the AnPixJ-GAF2 domain. Biochemistry 50, 6328-6339, doi:10.1021/bi101799w (2011).
25. Narikawa, R. et al. Structures of cyanobacteriochromes from phototaxis regulators AnPixJ and TePixJ reveal general and specific photoconversion mechanism. Proc. Natl. Acad. Sci. U. S. A. 110, 918-923, doi:10.1073/pnas.1212098110 (2013).
26. Narikawa, R., Muraki, N., Shiba, T., Ikeuchi, M., Kurisu, G. Crystallization and preliminary X-ray studies of the chromophore-binding domain of cyanobacteriochrome AnPixJ from Anabaena sp. PCC 7120. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 65, 159-162, doi:10.1107/S1744309108044151 (2009).
27. Velazquez Escobar, F. et al. Photoconversion Mechanism of the Second GAF Domain of CyanobacteriochromeAnPixJ and the Cofactor Structure of Its Green-Absorbing State. Biochemistry 52, 4871-4880, doi:10.1021/bi400506a (2013).
28. Loughlin, P., Lin, Y., Chen, M. Chlorophyll d and Acaryochloris marina: current status. Photosynth. Res. 116, 277-293, doi:10.1007/s11120-013-9829-y (2013).
29. Tomo, T., Allakhverdiev, S. I., Mimuro, M. Constitution and energetics of photosystem I and photosystem II in the chlorophyll d-dominated cyanobacterium Acaryochloris marina. J. Photochem. Photobiol. B 104, 333-340, doi:10.1016/j.jphotobiol.2011.02.017 (2011).
30. Hu, Q. et al. A photosystem I reaction center driven by chlorophyll d in oxygenic photosynthesis. Proc. Natl. Acad. Sci. U. S. A. 95, 13319-13323 (1998).
31. Tomo, T. et al. Identification of the special pair of photosystem II in a chlorophyll d-dominated cyanobacterium. Proc. Natl. Acad. Sci. U. S. A. 104, 7283-7288, doi:10.1073/pnas.0701847104 (2007).
32. Chen, M., Bibby, T. S., Nield, J., Larkum, A., Barber, J. Iron deficiency induces a chlorophyll d-binding Pcb antenna system around Photosystem I in Acaryochloris marina. Biochim. Biophys. Acta 1708, 367-374, doi:10.1016/j.bbabio.2005.05.007 (2005).
33. Swingley, W. D. et al. Niche adaptation and genome expansion in the chlorophyll d-producing cyanobacterium Acaryochloris marina. Proc. Natl. Acad. Sci. U. S. A. 105, 2005-2010, doi:10.1073/pnas.0709772105 (2008).
34. Sato, M. Genetically encoded fluorescent biosensors for live cell imaging of lipid dynamics. Methods Mol. Biol. 1071, 73-81, doi:10.1007/978-1-62703-622-1-6 (2014).
35. Shcherbakova, D. M., Subach, O. M., Verkhusha, V. V. Red fluorescent proteins: advanced imaging applications and future design. Angew. Chem. Int. Ed. Engl. 51, 10724-10738, doi:10.1002/anie.201200408 (2012).
36. Auldridge, M. E., Forest, K. T. Bacterial phytochromes: more than meets the light. Crit. Rev. Biochem.Mol. Biol. 46, 67-88, doi:10.3109/10409238.2010.546389 (2011).
37. Ikeuchi, M., Ishizuka, T. Cyanobacteriochromes: a new superfamily of tetrapyrrole-binding photoreceptors in cyanobacteria. Photochem. Photobiol. Sci. 7, 1159-1167, doi:10.1039/b802660m (2008).
38. Lamparter, T., Michael, N., Mittmann, F., Esteban, B. Phytochrome from Agrobacterium tumefaciens has unusual spectral properties and reveals an Nterminal chromophore attachment site. Proc. Natl. Acad. Sci. U. S. A. 99, 11628-11633 (2002).
39. Yang, X., Kuk, J.,Moffat, K. Conformational differences between the Pfr and Pr states in Pseudomonas aeruginosa bacteriophytochrome. Proc. Natl. Acad. Sci. U. S. A. 106, 15639-15644, doi:10.1073/pnas.0902178106 (2009).
40. Wagner, J. R., Brunzelle, J. S., Forest, K. T., Vierstra, R. D. A light-sensing knot revealed by the structure of the chromophore-binding domain of phytochrome. Nature 438, 325-331 (2005).
41. Essen, L. O., Mailliet, J., Hughes, J. The structure of a complete phytochrome sensory module in the Pr ground state. Proc. Natl. Acad. Sci. U. S. A. 105, 14709-14714, doi:10.1073/pnas.0806477105 (2008).
42. Kiss, E., Kos, P. B., Chen, M.& Vass, I.A unique regulation of the expression of the psbA, psbD, and psbE genes, encoding the D1, D2 and cytochrome b559 subunits of the Photosystem II complex in the chlorophyll d containing cyanobacterium Acaryochloris marina. Biochim. Biophys. Acta 1817, 1083-1094, doi:10.1016/j.bbabio.2012.04.010 (2012).
43. Duxbury, Z., Schliep, M., Ritchie, R. J., Larkum, A. W., Chen, M. Chromatic photoacclimation extends utilisable photosynthetically active radiation in the chlorophyll d-containing cyanobacterium, Acaryochloris marina. Photosynth. Res. 101, 69-75, doi:10.1007/s11120-009-9466-7 (2009).
44. Moglich, A., Moffat, K. Engineered photoreceptors as novel optogenetic tools. Photochem. Photobiol. Sci. 9, 1286-1300, doi:10.1039/c0pp00167h (2010).
45. Stepanenko, O. V., Stepanenko, O. V., Kuznetsova, I. M., Verkhusha, V. V., Turoverov, K. K. Beta-barrel scaffold of fluorescent proteins: folding, stability and role in chromophore formation. Int. Rev. Cell Mol. Biol. 302, 221-278, doi:10.1016/b978-0-12-407699-0.00004-2 (2013).
46. Filonov, G. S. et al. Bright and stable near-infrared fluorescent protein for in vivo imaging. Nat. Biotechnol. 29, 757-761, doi:10.1038/nbt.1918 (2011).
47. Shu, X. et al. Mammalian expression of infrared fluorescent proteins engineered from a bacterial phytochrome. Science 324, 804-807, doi:10.1126/science.1168683 (2009).
48. Leung, D. W., Otomo, C., Chory, J., Rosen, M. K. Genetically encoded photoswitching of actin assembly through the Cdc42-WASP-Arp2/3 complex pathway. Proc. Natl. Acad. Sci. U. S. A. 105, 12797-12802, doi:10.1073/pnas.0801232105 (2008).
49. Filonov, G. S., Verkhusha, V. V. A near-infrared BiFC reporter for in vivo imaging of protein-protein interactions. Chem. Biol. 20, 1078-1086, doi:10.1016/j.chembiol.2013.06.009 (2013).
50. Yu, D. et al. An improved monomeric infrared fluorescent protein for neuronal and tumour brain imaging. Nat. Commun. 5, 3626, doi:10.1038/ncomms4626 (2014).
51. Chozinski, T. J., Gagnon, L. A., Vaughan, J. C. Twinkle, twinkle little star: Photoswitchable fluorophores for super-resolution imaging. FEBS Lett. 588, 3603-3612, doi:10.1016/j.febslet.2014.06.043 (2014).
52. Sineshchekov, V. Photobiophysics and photobiochemistry of the heterogenous phytochrome system. Biochim. Biophys. Acta 1228, 125-164 (1995).
53. Schultz, J., Milpetz, F., Bork, P., Ponting, C. P. SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. U. S. A. 95, 5857-5864 (1998).
54. Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., Higgins, D. G. The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882 (1997).
55. Huson, D. H. et al. Dendroscope: An interactive viewer for large phylogenetic trees. BMC Bioinformatics 8, 460, doi:10.1186/1471-2105-8-460 (2007).
56. Mukougawa, K., Kanamoto, H., Kobayashi, T., Yokota, A., Kohchi, T. Metabolic engineering to produce phytochromes with phytochromobilin, phycocyanobilin, www.nature.com/scientificreports or phycoerythrobilin chromophore in Escherichia coli. FEBS Lett. 580, 1333-1338 (2006).
57. Berkelman, T. R., Lagarias, J. C. Visualization of bilin-linked peptides and proteins in polyacrylamide gels. Anal. Biochem. 156, 194-201 (1986).