Sensing the light: Photoreceptive systems and signal transduction in cyanobacteria

Molecular Microbiology

Volumn 64, Issue 1, 2007, Pages 16-27

  Montgomery, Beronda L ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYPTOCHROME; PHYCOBILIPROTEIN; PHYTOCHROME; RHODOPSIN;

BLUE LIGHT; CYANOBACTERIUM; NONHUMAN; PHOTOMORPHOGENESIS; PHOTORECEPTOR; PHOTOSYNTHESIS; PHOTOTROPHIC BACTERIUM; PRIORITY JOURNAL; SHORT SURVEY; SIGNAL TRANSDUCTION; ULTRAVIOLET RADIATION;

CYANOBACTERIA; GENE EXPRESSION REGULATION, BACTERIAL; LIGHT; MORPHOGENESIS; PHOTORECEPTORS, MICROBIAL; PHOTOSYNTHESIS; PHYTOCHROME; SIGNAL TRANSDUCTION;

CYANOBACTERIA; PROKARYOTA;

EID: 33947245585     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2007.05622.x     Document Type: Short Survey

References (80)

1. Alvey, R.M., Li, L., Balabas, B.E., Seib, L., Stowe-Evans, E.L., and Kehoe, D.M. (2005) Signal transduction pathways regulating chromatic adaptation. In Light Sensing in Plants. Wada, M., Shimazaki, K., and Iino, M. (eds). Tokyo: Springer-Verlag, pp. 299-306.
2. Aravind, L., and Ponting, C.P. (1997) The GAF domain: an evolutionary link between diverse phototransducing proteins. Trends Biochem Sci 22: 458-459.
3. Ashby, M.K., and Houmard, J. (2006) Cyanobacterial two-component proteins: structure, diversity, distribution, and evolution. Microbiol Mol Biol Rev 70: 472-509.
4. Baca, M., Borgstahl, G.E., Boissinot, M., Burke, P.M., Williams, D.R., Slater, K.A., and Getzoff, E.D. (1994) Complete chemical structure of photoactive yellow protein: novel thioester-linked 4-hydroxycinnamyl chromophore and photocycle chemistry. Biochemistry 33: 14369-14377.
5. Bebout, B.M., and Garcia-Pichel, F. (1995) UV B-induced vertical migrations of cyanobacteria in a microbial mat. Appl Environ Microbiol 61: 4215-4222.
6. Bourret, R.B., and Stock, A.M. (2002) Molecular information processing: lessons from bacterial chemotaxis. J Biol Chem 277: 9625-9628.
7. Brudler, R., Hitomi, K., Daiyasu, H., Toh, H., Kucho, K., Ishiura, M., et al. (2003) Identification of a new cryptochrome class. Structure, function, and evolution. Mol Cell 11: 59-67.
8. Burja, A.M., Dhamwichukorn, S., and Wright, P.C. (2003) Cyanobacterial postgenomic research and systems biology. Trends Biotechnol 21: 504-511.
9. Campbell, D., Eriksson, M.-J., Oquist, G., Gustafsson, P., and Clarke, A.K. (1998) The cyanobacterium Synechococcus resists UV-B by exchanging photosystem II reaction-center D1 proteins. Proc Natl Acad Sci USA 95: 364-369.
10. Crosson, S., Rajagopal, S., and Moffat, K. (2003) The LOV domain family: photoresponsive signaling modules coupled to diverse output domains. Biochemistry 42: 2-10.
11. Everroad, C., Six, C., Partensky, F., Thomas, J.-C., Holtzendorff, J., and Wood, A.M. (2006) Biochemical bases of type IV chromatic adaptation in marine Synechococcus spp. J Bacteriol 188: 3345-3356.
12. Fiedler, B., Broc, D., Schubert, H., Rediger, A., Börner, T., and Wilde, A. (2004) Involvement of cyanobacterial phytochromes in growth under different light qualities and quantities. Photochem Photobiol 79: 551-555.
13. Fiedler, B., Borner, T., and Wilde, A. (2005) Phototaxis in the cyanobacterium Synechocystis sp. PCC 6803: role of different photoreceptors. Photochem Photobiol 81: 1481-1488.
14. Fischer, A.J., and Lagarias, J.C. (2004) Harnessing phytochrome's glowing potential. Proc Natl Acad Sci USA 101: 17334-17339.
15. Fischer, A.J., Rockwell, N.C., Jang, A.Y., Ernst, L.A., Waggoner, A.S., Duan, Y., et al. (2005) Multiple roles of a conserved GAF domain tyrosine residue in cyanobacterial and plant phytochromes. Biochemistry 44: 15203-15215.
16. Galperin, M.Y. (2006) Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J Bacteriol 188: 4169-4182.
17. Gill, R.T., Katsoulakis, E., Schmitt, W., Taroncher-Oldenburg, G., Misra, J., and Stephanopoulos, G. (2002) Genome-wide dynamic transcriptional profiling of the light-to-dark transition in Synechocystis sp. strain PCC 6803. J Bacteriol 184: 3671-3681.
18. Giraud, E., Fardoux, J., Fourrier, N., Hannibal, L., Genty, B., Bouyer, P., et al. (2002) Bacteriophytochrome controls photosystem synthesis in anoxygenic bacteria. Nature 417: 202.
19. Gomelsky, M., and Klug, G. (2002) BLUF: a novel FAD-binding domain involved in sensory transduction in microorganisms. Trends Biochem Sci 27: 497-500.
20. Hitomi, K., Okamoto, K., Daiyasu, H., Miyashita, H., Iwai, S., Toh, H., et al. (2000) Bacterial cryptochrome and photolyase: characterization of two photolyase-like genes of Synechocystis sp. PCC6803. Nucleic Acids Res 28: 2353-2362.
21. van der Horst, M.A., and Hellingwerf, K.J. (2004) Photoreceptor proteins, 'star actors of modern times': a review of the functional dynamics in the structure of representative members of six different photoreceptor families. Acc Chem Res 37: 13-20.
22. Hübschmann, T., Jorissen, H.J., Börner, T., Gärtner, W., and Tandeau de Marsac, N. (2001) Phosphorylation of proteins in the light-dependent signalling pathway of a filamentous cyanobacterium. Eur J Biochem 268: 3383-3389.
23. Hübschmann, T., Yamamoto, H., Gieler, T., Murata, N., and Börner, T. (2005) Red and far-red light alter the transcript profile in the cyanobacterium Synechocystis sp. PCC 6803: impact of cyanobacterial phytochromes. FEBS Lett 579: 1613-1618.
24. Hughes, J., Lamparter, T., Mittmann, F., Hartmann, E., Gartner, W., Wilde, A., and Borner, T. (1997) A prokaryotic phytochrome. Nature 386: 663.
25. 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.
26. Jung, K.-H., Trivedi, V.D., and Spudich, J.L. (2003) Demonstration of a sensory rhodopsin in eubacteria. Mol Microbiol 47: 1513-1522.
27. Kehoe, D.M., and Grossman, A.R. (1996) Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science 273: 1409-1412.
28. Kehoe, D.M., and Grossman, A.R. (1997) New classes of mutants in complementary chromatic adaptation provide evidence for a novel four-step phosphorelay system. J Bacteriol 179: 3914-3921.
29. Kehoe, D.M., and Gutu, A. (2006) Responding to color: the regulation of complementary chromatic adaptation. Annu Rev Plant Biol 57: 127-150.
30. Kita, A., Okajima, K., Morimoto, Y., Ikeuchi, M., and Miki, K. (2005) Structure of a cyanobacterial BLUF protein, Tll0078, containing a novel FAD-binding blue light sensor domain. J Mol Biol 349: 1-9.
31. Lamparter, T. (2004) Evolution of cyanobacterial and plant phytochromes. FEBS Lett 573: 1-5.
32. Losi, A., Polverini, E., Quest, B., and Gärtner, W. (2002) First evidence for phototropin-related blue-light receptors in prokaryotes. Biophys J 82: 2627-2634.
33. Mascher, T., Helmann, J.D., and Unden, G. (2006) Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol Mol Biol Rev 70: 910-938.
34. Masuda, S., and Ono, T.-A. (2004) Biochemical characterization of the major adenylyl cyclase, Cya1, in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett 577: 255.
35. Masuda, S., Hasegawa, K., Ishii, A., and Ono, T.A. (2004) Light-induced structural changes in a putative blue-light receptor with a novel FAD binding fold sensor of blue-light using FAD (BLUF); Slr1694 of Synechocystis sp. PCC6803. Biochemistry 43: 5304-5313.
36. Montgomery, B.L., and Lagarias, J.C. (2002) Phytochrome ancestry: sensors of bilins and light. Trends Plant Sci 7: 357-366.
37. Montgomery, B.L., Casey, E.S., Grossman, A.R., and Kehoe, D.M. (2004) AplA, a member of a new class of phycobiliproteins lacking a traditional role in photosynthetic light harvesting. J Bacteriol 186: 7420-7428.
38. Moon, Y.J., Park, Y.M., Chung, Y.H., and Choi, J.S. (2004) Calcium is involved in photomovement of cyanobacterium Synechocystis sp. PCC 6803. Photochem Photobiol 79: 114-119.
39. Mullineaux, C.W. (2001) How do cyanobacteria sense and respond to light? Mol Microbiol 41: 965-971.
40. Narikawa, R., Okamoto, S., Ikeuchi, M., and Ohmori, M. (2004) Molecular evolution of PAS domain-containing proteins of filamentous cyanobacteria through domain shuffling and domain duplication. DNA Res 11: 69-81.
41. Narikawa, R., Zikihara, K., Okajima, K., Ochiai, Y., Katayama, M., Shichida, Y., et al. (2006) Three putative photosensory LOV domains with distinct biochemical properties from the filamentous cyanobacterium Anabaena sp. PCC 7120. Photochem Photobiol 82: 1627-1633.
42. Ng, W.O., and Pakrasi, H.B. (2001) DNA photolyase homologs are the major UV resistance factors in the cyanobacterium Synechocystis sp. PCC 6803. Mol Gen Genet 264: 924-930.
43. 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.
44. Ohmori, M., Ikeuchi, M., Sato, N., Wolk, P., Kaneko, T., Ogawa, T., et al. (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.
45. Ohmori, M., Terauchi, K., Okamoto, S., and Watanabe, M. (2002) Regulation of cAMP-mediated photosignaling by a phytochrome in the cyanobacterium Anabaena cylindrica. Photochem Photobiol 75: 675-679.
46. Okajima, K., Yoshihara, S., Fukushima, Y., Geng, X., Katayama, M., Higashi, S., et al. (2005) Biochemical and functional characterization of BLUF-type flavin-binding proteins of two species of cyanobacteria. J Biochem (Tokyo) 137: 741-750.
47. Okajima, K., Fukushima, Y., Suzuki, H., Kita, A., Ochiai, Y., Katayama, M., et al. (2006) Fate determination of the flavin photoreceptions in the cyanobacterial blue light receptor TePixD (Tll0078). J Mol Biol 363: 10-18.
48. Okamoto, S., and Ohmori, M. (2003) Distribution of chromophore-binding GAF domains in genome sequence. Genome Inform 14: 442-443.
49. Okamoto, S., Kasahara, M., Kamiya, A., Nakahira, Y., and Ohmori, M. (2004) A phytochrome-like protein AphC triggers the cAMP signaling induced by far-red light in the cyanobacterium Anabaena sp. strain PCC7120. Photochem Photobiol 80: 429-433.
50. Padan, E., Zilberstein, D., and Schuldiner, S. (1981) pH homeostasis in bacteria. Biochim Biophys Acta 650: 151-166.
51. Palenik, B. (2001) Chromatic adaptation in marine Synechococcus strains. Appl Environ Microbiol 67: 991-994.
52. Pandey, R., Chauhan, S., Singhal, G.S., and Kale, R.K. (2000) Spectral light quality affects protein profile of Synechococcus sp. PCC 7942: a comparative 2-dimensional gel electrophoresis (2-DGE) analysis. Curr Microbiol 40: 297-301.
53. Park, C.M., Kim, J.I., Yang, S.S., Kang, J.G., Kang, J.H., Shim, J.Y., et al. (2000) A second photochromic bacteriophytochrome from Synechocystis sp. PCC 6803: spectral analysis and down-regulation by light. Biochemistry 39: 10840-10847.
54. Portwich, A., and Garcia-Pichel, F. (2000) A novel prokaryotic UVB photoreceptor in the cyanobacterium Chlorogloeopsis PCC 6912. Photochem Photobiol 71: 493-498.
55. Rockwell, N.C., and Lagarias, J.C. (2006) The structure of phytochrome: a picture is worth a thousand spectra. Plant Cell 18: 4-14.
56. Romling, U., Gomelsky, M., and Galperin, M.Y. (2005) C-di-GMP: the dawning of a novel bacterial signalling system. Mol Microbiol 57: 629-639.
57. Ryan, R.P., Fouhy, Y., Lucey, J.F., and Dow, J.M. (2006) Cyclic di-GMP signaling in bacteria: recent advances and new puzzles. J Bacteriol 188: 8327-8334.
58. 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.
59. Shi, L., Yoon, S.R., Bezerra, A.G., Jr, Jung, K.H., and Brown, L.S. (2006) Cytoplasmic shuttling of protons in Anabaena sensory rhodopsin: implications for a signaling mechanism. J Mol Biol 358: 686-700.
60. Sineshchekov, O.A., Trivedi, V.D., Sasaki, J., and Spudich, J.L. (2005) Photochromicity of Anabaena sensory rhodopsin, an atypical microbial receptor with a cis-retinal light-adapted form. J Biol Chem 280: 14663-14668.
61. Spudich, J.L. (2006) The multitalented microbial sensory rhodopsins. Trends Microbiol 14: 480-487.
62. Steglich, C., Frankenberg-Dinkel, N., Penno, S., and Hess, W.R. (2005) A green light-absorbing phycoerythrin is present in the high-light-adapted marine cyanobacterium Prochlorococcus sp. MED4. Environ Microbiol 7: 1611-1618.
63. Stock, A.M., Robinson, V.L., and Goudreau, P.N. (2000) Two-component signal transduction. Annu Rev Biochem 69: 183-215.
64. Stowe-Evans, E.L., and Kehoe, D.M. (2004) Signal transduction during light-quality acclimation in cyanobacteria: a model system for understanding phytochrome-response pathways in prokaryotes. Photochem Photobiol Sci 3: 495-502.
65. Stowe-Evans, E.L., Ford, J., and Kehoe, D.M. (2004) Genomic DNA microarray analysis: identification of new genes regulated by light color in the cyanobacterium Fremyella diplosiphon. J Bacteriol 186: 4338-4349.
66. Strauss, H.M., Schmieder, P., and Hughes, J. (2005) Light-dependent dimerisation in the N-terminal sensory module of cyanobacterial phytochrome 1. FEBS Lett 579: 3970-3974.
67. Tarutina, M., Ryjenkov, D.A., and Gomelsky, M. (2006) An unorthodox bacteriophytochrome from Rhodobacter sphaeroides involved in turnover of the second messenger c-di-GMP. J Biol Chem 281: 34751-34758.
68. Taylor, B.L., and Zhulin, I.B. (1999) PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 63: 479-506.
69. 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.
70. Vogeley, L., Sineshchekov, O.A., Trivedi, V.D., Sasaki, J., Spudich, J.L., and Luecke, H. (2004) Anabaena sensory rhodopsin: a photochromic color sensor at 2.0 Å. Science 306: 1390-1393.
71. Wagner, J.R., Brunzelle, J.S., Forest, K.T., and Vierstra, R.D. (2005) A light-sensing knot revealed by the structure of the chromophore-binding domain of phytochrome. Nature 438: 325-331.
72. West, A.H., and Stock, A.M. (2001) Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci 26: 369.
73. Wilde, A., Churin, Y., Schubert, H., and Borner, 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.
74. Wilde, A., Fiedler, B., and Borner, T. (2002) The cyanobacterial phytochrome Cph2 inhibits phototaxis towards blue light. Mol Microbiol 44: 981-988.
75. 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.
76. 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.
77. Yoshihara, S., Katayama, M., Geng, X., and Ikeuchi, M. (2004) Cyanobacterial phytochrome-like PixJ1 holoprotein shows novel reversible photoconversion between blue- and green-absorbing forms. Plant Cell Physiol 45: 1729-1737.
78. Yoshihara, S., Shimada, T., Matsuoka, D., Zikihara, K., Kohchi, T., and Tokutomi, S. (2006) Reconstitution of blue-green reversible photoconversion of a cyanobacterial photoreceptor, PixJ1, in phycocyanobilin-producing Escherichia coli. Biochemistry 45: 3775-3784.
79. Yuan, H., Anderson, S., Masuda, S., Dragnea, V., Moffat, K., and Bauer, C. (2006) Crystal structures of the Synechocystis photoreceptor Slr1694 reveal distinct structural states related to signaling. Biochemistry 45: 12687-12694.
80. Zhang, C.C., Jang, J., Sakr, S., and Wang, L. (2005) Protein phosphorylation on Ser, Thr and Tyr residues in cyanobacteria. J Mol Microbiol Biotechnol 9: 154-166.