Abstract
Phototaxis, positive (movement toward the light source) or negative (from the light source) mediates the adaptation of cyanobacteria to varying wave lengths and illumination intensity. The transcription regulator PrqR of the family TetR is known as a repressor of the prqRA operon controlling resistance to the oxidative stress inducer methyl viologen in the cyanobacterium Synechocystis sp. PCC 6803. However, it was shown in this work that mutation prqRL17Q affecting the DNA-binding domain of the PrqR protein, which causes derepression of the prqRA operon and enhances cell resistance to methyl viologen, additionally determines negative phototaxis induced with white light and red light of low intensity. The inactivation of gene prqA did not affect cell motility in mutant PqR carrying mutation prqRL17Q and in the wild-type strain characterized by positive phototaxis appearing in response to the light of low intensity. Moreover, a mutant with deletion prqR did not differ from the wild-type strain with respect to phototaxis type suggesting that the specificity of the regulator protein was changed in cells carrying prqRL17Q mutation. Note that changes in transcription of pilA genes that control biogenesis of pili providing for cell motility were not detected in mutant PqR, and, in agreement with data of atomic force microscopy, the type of pili formation is identical in prqR mutants and the wild-type strain. Meanwhile, mutant PqR manifested a decrease in transcription of gene taxD1 encoding the photoreceptor of red light that is required for the positive phototaxis of cyanobacteria. These data imply that mutation prqRL17Q changes the specificity of the PrqR repressor protein and thereby affects the regulation of phototaxis at the level of photoperception and signal transduction in cells.
References
Asada, K. Production and Action of Active Oxygen Species in Photosynthetic Tissues, Causes of Photooxidative Stress and Amelioration of Defense Systems in Plants, Foyer, C.H. and Millineaux, P.M., Eds., Boca Raton: CRC, 1994, pp. 77–104.
Kagawa, T. and Wada, M., Chloroplast-Avoidance Response Induced by High-Fluence Blue Light in Prothallial Cells of the Fern Adiantum capillusveneris as Analyzed by Microbeam Irradiation, Plant Physiol., 1999, vol. 119, pp. 917–923.
Castenholz, R.W. and Garcia-Pichel, F., Cyanobacterial Responses to UV-Radiation, The Ecology of Cyanobacteria, Whitton, B.A. and Potts, M., Eds., Boston: Kluwer, 2000, pp. 591–611.
Ng, W.-O., Grossman, A.R., and Bhaya, D., Multiple Light Inputs Control Phototaxis in Synechocystis sp. Strain PCC 6803, J. Bacteriol., 2003, vol. 185, pp. 1599–1607.
Mulo, P., Laakso, S., Maenpaa, P., and Aro, E., Stepwise Photoinhibition of Photosystem II: Studies with Synechocystis Species PCC 6803 Mutants with a Modified D-E Loop of the Reaction Center Polypeptide D1, Plant Physiol., 1998, vol. 117, pp. 483–490.
Mattick, J., Whitchurch, C., and Alm, R., The Molecular Genetics of Type-4 Fimbriae in Pseudomonas aeruginosa: A Review, Gene, 1996, vol. 179, pp. 147–155.
Bhaya, D., Watanabe, N., Ogawa, T., and Grossman, A.R., The Role of an Alternative Sigma Factor in Motility and Pilus Formation in the Cyanobacterium Synechocystis sp. Strain PCC 6803, Proc. Natl Acad. Sci. USA, 1999, vol. 96, pp. 3188–3193.
Bhaya, D., Bianco, N., Bryant, D., and Grossman, A.R., Type IV Pilus Biogenesis and Motility in the Cyanobacterium Synechocystis sp. PCC 6803, Mol. Microbiol., 2000, vol. 37, pp. 941–951.
Chung, Y., Cho, M., Moon, Y., et al., Ctr1, a Gene Involved in a Signal Transduction Pathway of the Gliding Motility in the Cyanobacterium Synechocystis sp. PCC 6803, FEBS Lett., 2001, vol. 492, pp. 33–38.
Bhaya, D., Takahashi, A., and Grossman, A.R., Light Regulation of Type IV Pilus-Dependent Motility by Chemosensor-Like Elements in Synechocystis PCC 6803, Proc. Natl Acad. Sci. USA, 2001, vol. 98, pp. 7540–7545.
Bhaya, D., Takahashi, A., Shahi, P., and Grossman, A.R., Novel Motility Mutants of Synechocystis Strain PCC 6803 Generated by in vitro Transposon Mutagenesis, J. Bacteriol., 2001, vol. 183, pp. 6140–6143.
Kamei, A., Yoshihara, S., Yuasa, T., et al., Biochemical and Functional Characterization of a Eukaryotic-Type Protein Kinase, spkB, in the Cyanobacterium, Synechocystis sp. PCC 6803, Curr. Microbiol., 2003, vol. 46, pp. 296–301.
Panichkin, V., Arakawa-Kobayashi, S., Kanaseki, T., et al., Serine/Threonine Protein Kinase SpkA in Synechocystis sp. PCC 6803 Is a Regulator of Expression of Three Putative pilA Operons, Formation of Thick Pili, and Cell Motility, J. Bacteriol., 2006, vol. 188, pp. 7696–7699.
Yoshihara, S., Suzuki, F., Fujita, H., et al., Novel Putative Photoreceptor and Regulatory Genes Required for the Positive Phototactic Movement of the Unicellular Motile Cyanobacterium Synechocystis sp. PCC 6803, Plant Cell Physiol., 2000, vol. 41, pp. 1299–1304.
Fiedler, B., Borner, T., and Wilde, A., Phototaxis in the Cyanobacterium Synechocystis sp. PCC 6803: Role of Different Photoreceptors, Photochem. Photobiol., 2005, vol. 81, pp. 1481–1488.
Okajima, K., Yoshihara, S., Fukushima, Y., et al., Biochemical and Functional Characterization of BLUF-Type Flavin-Binding Proteins of Two Species of Cyanobacteria, J. Biochem. (Tokyo, Jpn.), 2005, vol. 137, pp. 741–750.
Sambrook, J., Fritsch, E.F., and Maniatis, T., Molecular Cloning: A Laboratory Manual, 2nd Ed., New York: Cold Spring Harbor Lab., 1989.
Rippka, R., Deruelles, D.E., Waterbury, J.B., et al., Generic Assignments, Strain Histories and Properties of Pure Cultures of Cyanobacteria, J. Gen. Microbiol., 1979, vol. 111, pp. 1–61.
Nefedova, L.N., Fantin, Yu.S., Zinchenko, V.V., and Babykin, M.M., The prqA and mvrA Genes Encoding Proteins Controlling Methyl Viologen Resistance of Cyanobacterium Synechocystis sp. PCC 6803, Russ. J. Genet., 2003, vol. 39, no. 3, pp. 264–268.
Lichtenthaler, H.K., Chlorophylls and Carotenoids: Pigments of Photosynthetic Biomembranes, Methods Enzymol., 1987, vol. 148, pp. 350–382.
Babykin, M.M., Sidoruk, K.V., Zinchenko, V.V., et al., On the Involvement of the Regulatory Gene prqR in the Development of Resistance to Methyl Viologen in Cyanobacterium Synechocystis sp PCC 6803, Russ. J. Genet., 2003, vol. 39, no. 1, pp. 18–24.
Cyanobase Website. http://www.kazusa.or.jp/cyano/Synechocystis
Dubrovin, E.V., Kirik, I.A., Babykin, M.M., and Yaminsky, I.V., Atomic Force Microscopy Study of Pili in the Cyanobacterium Synechocystis sp. PCC 6803, From Cells to Proteins: Imaging Nature Across Dimensions, Evangelista, V., Barsanti, L., Passarelli, V., and Gualtieri, P., Eds., NATO Security through Science Series, Sub-Series B: Physics and Biophysics, 2005, vol. 3, pp. 405–414.
Ramos, J.L., Martinez-Bueno, M., Molina-Henares, A.J., et al., The TetR Family of Transcriptional Repressors, Microbiol. Mol. Biol. Rev., 2005, vol. 69, pp. 326–356.
Kirik, I.A., Zinchenko, V.V., Shestakov, S.V., and Babykin, M.M., In Cis and in Trans Autorepression of the prqR Gene in Cyanobacterium Synechocystis sp. RCC 6803, Mol. Biol., (Moscow), 2003, vol. 37, no. 6, pp. 880–887.
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Original Russian Text © I.A. Kirik, L.N. Nefedova, Yu.S. Fantin, M.M. Babykin, 2008, published in Genetika, 2008, Vol. 44, No. 4, pp. 474–482.
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Kirik, I.A., Nefedova, L.N., Fantin, Y.S. et al. Inversion of phototaxis in cells of Synechocystis sp. PCC 6803 determined by a mutation in the regulatory gene prqR . Russ J Genet 44, 405–412 (2008). https://doi.org/10.1134/S1022795408040042
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DOI: https://doi.org/10.1134/S1022795408040042