Cyanobacterial phytochrome-like PixJ1 holoprotein shows novel reversible photoconversion between blue- and green-absorbing forms

Plant and Cell Physiology

Volumn 45, Issue 12, 2004, Pages 1729-1737

  Yoshihara, Shizue ^a,b   Katayama, Mitsunori ^a   Geng, Xiaoxing ^a   Ikeuchi, Masahiko ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b Osaka Prefecture University   (Japan)

Author keywords

Cyanobacterium; Motility; Photoreceptor; Phototaxis; Phytochrome; Signal transduction

Indexed keywords

CYANOBACTERIA; SYNECHOCYSTIS; SYNECHOCYSTIS SP.; SYNECHOCYSTIS SP. PCC 6803;

EID: 12444323680     PISSN: 00320781     EISSN: None     Source Type: Journal    
DOI: 10.1093/pcp/pch214     Document Type: Article

References (53)

1. Aravind, L. and Ponting, C.P. (1997) The GAF domain: an evolutionary link between diverse phototransducing proteins. Trends Biochem. Sci. 22: 458-459.
2. Berkelman, T.R. and Lagarias, J.C. (1986) Visualization of bilin-linked peptides and proteins in polyacrylamide gels. Anal. Biochem. 156: 194-201.
3. Bhaya, D., Bianco, N.R., Bryant, D. and Grossman, A. (2000) Type IV pilus biogenesis and motility in the cyanobacterium Synechocystis sp. PCC6803. Mol. Microbiol. 37: 941-951.
4. Bhaya, D., Watanabe, N., Ogawa, T. and Grossman, A.R. (1999) The role of an alternative sigma factor in motility and pilus formation in the cyanobacterium Synechocystis sp. strain PCC6803. Proc. Natl Acad. Sci. USA 96: 3188-3193.
5. Bhoo, S.H., Davis, S.J., Walker, J., Karniol, B. and Vierstra, R.D. (2001) Bacteriophytochromes are photochromic histidine kinases using a biliverdin chromophore. Nature 414: 776-779.
6. Bourret, R.B. and Stock, A.M. (2002) Molecular information processing: lessons from bacterial chemotaxis. J. Biol. Chem. 277: 9625-9628.
7. Choi, J.S., Chung, Y.H., Moon, Y.J., Kim, C., Watanabe, M., Song, P.S., Joe, C.O., Bogorad, L. and Park, Y.M. (1999) Photomovement of the gliding cyanobacterium Synechocystis sp. PCC 6803. Photochem. Photobiol. 70: 95-102.
8. Cornejo, J., Willows, R.D. and Beale, S.I. (1998) Phytobilin biosynthesis: cloning and expression of a gene encoding soluble ferredoxin-dependent heme oxygenase from Synechocystis sp. PCC 6803. Plant J. 15: 99-107.
9. Davis, S.J., Vener, A.V. and Vierstra, R.D. (1999) Bacteriophytochromes: phytochrome-like photoreceptors from nonphotosynthetic eubacteria. Science 286: 2517-2520.
10. Dolganov, N. and Grossman, A.R. (1999) A polypeptide with similarity to phycocyanin alpha-subunit phycocyanobilin lyase involved in degradation of phycobilisomes. J. Bacteriol. 181: 610-617.
11. Frankenberg, N., Mukougawa, K., Kohchi, T. and Lagarias, J.C. (2001) Functional genomic analysis of the HY2 family of ferredoxin-dependent bilin reductases from oxygenic photosynthetic organisms. Plant Cell 13: 965-978.
12. Galperin, M.Y., Nikolskaya, A.N. and Koonin, E.V. (2001) Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol. Lett. 203: 11-21.
13. Gambetta, G.A. and Lagarias, J.C. (2001) Genetic engineering of phytochrome biosynthesis in bacteria. Proc. Natl Acad. Sci. USA 98: 10566-10571.
14. Giraud, E., Fardoux, J., Fourrier, N., Hannibal, L., Genty, B., Bouyer, P., Dreyfus, B. and Vermeglio, A. (2002) Bacteriophytochrome controls photosystem synthesis in anoxygenic bacteria. Nature 417: 202-205.
15. Hihara, Y. and Ikeuchi, M. (1997) Mutation in a novel gene required for photomixotrophic growth leads to enhanced photoautotrophic growth of Synechocystis sp. PCC 6803. Photosynth. Res. 53: 129-139.
16. Hughes, J., Lamparter, T., Mittmann, F., Hartmann, E., Gärtner, W., Wilde, A. and Börner, T. (1997) A prokaryotic phytochrome. Nature 386: 663.
17. Hübschmann, T., Börner, T., Hartmann, E. and Lamparter, T. (2001) Characterization of the Cph1 holo-phytochrome from Synechocystis sp. PCC 6803. Eur. J. Biochem. 268: 2055-2063.
18. Jorissen, H.J., Quest, B., Remberg, A., Coursin, T., Braslavsky, S.E., Schaffner, K., Tandeau de Marsac, N. and Gartner, W. (2002) Two independent, light-sensing two-component systems in a filamentous cyanobacterium. Eur. J. Biochem. 269: 2662-2671.
19. Kaneko, T., Nakamura, Y., Wolk, C.P., Kuritz, T., Sasamoto, S., Watanabe, A., Iriguchi, M., Ishikawa, A., Kawashima, K., Kimura, T., Kishida, Y., Kohara, M., Matsumoto, M., Matsuno, A., Muraki, A., Nakazaki, N., Shimpo, S., Sugimoto, M., Takazawa, M., Yamada, M., Yasuda, M. and Tabata, S. (2001) Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res. 8: 205-213, 227-253.
20. Kaneko, T., Sato, S., Kotani, H., Tanaka, A., Asamizu, E., Nakamura, Y., Miyajima, N., Hirosawa, M., Sugiura, M., Sasamoto, S., Kimura, T., Hosouchi, T., Matsuno, A., Muraki, A., Nakazaki, N., Naruo, K., Okumura, S., Shimpo, S., Takeuchi, C., Wada, T., Watanabe, A., Yamada, M., Yasuda, M. and Tabata, S. (1996) Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 3: 109-136.
21. Karniol, B. and Vierstra, R.D. (2003) The pair of bacteriophytochromes from Agrobacterium tumefaciens are histidine kinases with opposing photobiological properties. Proc. Natl Acad. Sci. USA 100: 2807-2812.
22. Kehoe, D.M. and Grossman, A.R. (1996) Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science 273: 1409-1412.
23. Kondou, Y., Nakazawa, M., Higashi, S., Watanabe, M. and Manabe, K. (2001) Equal-quantum action spectra indicate fluence-rate-selective action of multiple photoreceptors for photomovement of the thermophilic cyanobacterium Synechococcus elongatus. Photochem. Photobiol. 73: 90-95.
24. Lamparter, T., Carrascal, M., Michael, N., Martinez, E., Rottwinkel, G. and Abian, J. (2004) The biliverdin chromophore binds covalently to a conserved cysteine residue in the N-terminus of Agrobacterium phytochrome Agp1. Biochemistry 43: 3659-3669.
25. Lamparter, T., Esteban, B. and Hughes, J. (2001) Phytochrome Cph1 from the cyanobacterium Synechocystis PCC6803. Purification, assembly, and quaternary structure. Eur. J. Biochem. 268: 4720-4730.
26. Lamparter, T., Michael, N., Mittmann, F. and Esteban, B. (2002) Phytochrome from Agrobacterium tumefaciens has unusual spectral properties and reveals an N-terminal chromophore attachment site. Proc. Natl Acad. Sci. USA 99: 11628-11633.
27. Landgraf, F.T., Forreiter, C., Hurtado Pico, A., Lamparter, T. and Hughes, J. (2001) Recombinant holophytochrome in Escherichia coli. FEBS Lett. 508: 459-462.
28. Li, L. and Lagarias, J.C. (1992) Phytochrome assembly. Defining chromophore structural requirements for covalent attachment and photoreversibility. J. Biol. Chem. 267: 19204-19210.
29. McAllister-Lucas, L.M., Haik, T.L., Colbran, J.L., Sonnenburg, W.K., Seger, D., Turko, I.V., Beavo, J.A., Francis, S.H. and Corbin, J.D. (1995) An essential aspartic acid at each of two allosteric cGMP-binding sites of a cGMP-specific phosphodiesterase. J Biol. Chem. 270: 30671-30679.
30. Mutsuda, M., Michel, K.P., Zhang, X., Montgomery, B.L. and Golden, S.S. (2003) Biochemical properties of CikA, an unusual phytochrome-like histidine protein kinase that resets the circadian clock in Synechococcus elongatus PCC 7942. J. Biol. Chem. 278: 19102-19110.
31. Nakamura, Y., Kaneko, T., Sato, S., Ikeuchi, M., Katoh, H., Sasamoto, S., Watanabe, A., Iriguchi, M., Kawashima, K., Kimura, T., Kishida, Y., Kiyokawa, C., Kohara, M., Matsumoto, M., Matsuno, A., Nakazaki, N., Shimpo, S., Sugimoto, M., Takeuchi, C., Yamada, M. and Tabata, S. (2002) Complete genome structure of the thermophilic cyanobacterium Thermosynechococcus elongatus BP-1. DNA Res. 9: 123-130.
32. Ng, W.O., Grossman, A.R. and Bhaya, D. (2003) Multiple light inputs control phototaxis in Synechocystis sp. strain PCC6803. J. Bacteriol. 185: 1599-1607.
33. Ng, W.O., Zentella, R., Wang, Y., Taylor, J.S. and Pakrasi, H.B. (2000) phrA, the major photoreactivating factor in the cyanobacterium Synechocystis sp. strain PCC 6803 codes for a cyclobutane-pyrimidine-dimer-specific DNA photolyase. Arch. Microbiol. 173: 412-417.
34. Ohmori, M., Ikeuchi, M., Sato, N., Wolk, P., Kaneko, T., Ogawa, T., Kanehisa, M., Goto, S., Kawashima, S., Okamoto, S., Yoshimura, H., Katoh, H., Fujisawa, T., Ehira, S., Kamei, A., Yoshihara, S., Narikawa, R. and Tabata, S. (2001) Characterization of genes encoding multi-domain proteins in the genome of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res. 8: 271-284.
35. Okamoto, S. and Ohmori, M. (2002) The cyanobacterial PilT protein responsible for cell motility and transformation hydrolyzes ATP. Plant Cell Physiol. 43:1127-1136.
36. Okamoto, S. and Ohmori, M. (2003) Distribution of chromophore-binding GAF domains in genome sequence. In Genome Infomatics. Edited by Lathrop, R., Nakai, K., Miyano, S., Takagi, T. and Kanehisa, M. pp. 442-443. Universal Academy Press, Tokyo.
37. Park, C.M., Kimn, J.I., Yang, S.S., Kang, J.G., Kang, J.H., Shim, J.Y., Chung, Y.H., Park, Y.M. and Song, P.S. (2000) A second photochromic bacteriophytochrome from Synechocystis sp. PCC 6803: spectral analysis and down-regulation by light. Biochemistry 39: 10840-10847.
38. Quail, P.H. (2002) Phytochrome photosensory signalling networks. Nat. Rev. Mol. Cell. Biol. 3: 85-93.
39. Quest, B. and Gartner, W. (2004) Chromophore selectivity in bacterial phytochromes: dissecting the process of chromophore attachment. Eur. J. Biochem. 271: 1117-1126.
40. Schluchter, W.M. and Glazer, A.N. (1997) Characterization of cyanobacterial biliverdin reductase. Conversion of biliverdin to bilirubin is important for normal phycobiliprotein biosynthesis. J. Biol. Chem. 272: 13562-13569.
41. Schmitz, O., Katayama, M., Williams, S.B., Kondo, T. and Golden, S.S. (2000) CikA, a bacteriophytochrome that resets the cyanobacterial circadian clock. Science 289: 765-768.
42. Sidler, W.A. (1994) Phycobilisome and phycobiliprotein structures. In The Molecular Biology of Cyanobacteria. Edited by Bryant, D.A. pp. 139-216. Kluwer Academic Publishers, Dordrecht, The Netherlands.
43. Stanier, R.Y., Kunisawa, R., Mandel, M. and Cohen-Bazire, G. (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bacteriol. Rev. 35: 171-205.
44. Storf, M., Parbel, A., Meyer, M., Strohmann, B., Scheer, H., Deng, M.G., Zheng, M., Zhou, M. and Zhao, K.H. (2001) Chromophore attachment to biliproteins: specificity of PecE/PecF, a lyase-isomerase for the photoactive 3(1)-cys-alpha 84-phycoviolobilin chromophore of phycoerythrocyanin. Biochemistry 40: 12444-12456.
45. Terauchi, K., Montgomery, B.L., Grossman, A.R., Lagarias, J.C. and Kehoe, D.M. (2004) RcaE is a complementary chromatic adaptation photoreceptor required for green and red light responsiveness. Mol. Microbiol. 51: 567-577.
46. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. and Higgins, D.G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25: 4876-4882.
47. Wilde, A., Churin, Y., Schubert, H. and Börner, T. (1997) Disruption of a Synechocystis sp. PCC 6803 gene with partial similarity to phytochrome genes alters growth under changing light qualities. FEBS Lett. 406: 89-92.
48. Yoshihara, S., Geng, X. and Ikeuchi, M. (2002) pilG gene cluster and split pilL genes involved in pilus biogenesis, motility and genetic transformation in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol. 43: 513-521.
49. Yoshihara, S., Geng, X., Okamoto, S., Yura, K., Murata, T., Go, M., Ohmori, M. and Ikeuchi, M. (2001) Mutational analysis of genes involved in pilus structure, motility and transformation competency in the unicellular motile cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol. 42: 63-73.
50. Yoshihara, S., Suzuki, F., Fujita, H., Geng, X.X. and Ikeuchi, M. (2000) Novel putative photoreceptor and regulatory genes required for the positive phototactic movement of the unicellular motile cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol. 41: 1299-1304.
51. Zhao, K.H., Haessner, R., Cmiel, E. and Scheer, H. (1995) Type I reversible photochemistry of phycoerythrocyanin involves Z/E-isomerization of a-84 phycoviolobilin chromophore. Biochim. Biophys. Acta 1228: 235-243.
52. Zhao, K.H. and Scheer, H. (1995) Type I and type II reversible photochemistry of phycoerythrocyanin a-subunit from Mastigocladus laminosus both involve Z, E isomerization of phycoviolobilin chromophore and are controlled by sulfhydryls in apoprotein. Biochim. Biophys. Acta 1228: 244-253.
53. Zhao, K.H., Wu, D., Wang, L., Zhou, M., Storf, M., Bubenzer, C., Strohmann, B. and Scheer, H. (2002) Characterization of phycoviolobilin phycoerythrocyanin-alpha 84-cystein-lyase-(isomerizing) from Mastigocladus laminosus. Eur. J. Biochem. 269: 4542-4550.