574
Views
21
CrossRef citations to date
0
Altmetric
Review Article

Signal transduction pathways in Synechocystis sp. PCC 6803 and biotechnological implications under abiotic stress

, , , , , , , & show all
Pages 269-280 | Received 11 Apr 2013, Accepted 24 Aug 2013, Published online: 01 Oct 2013

References

  • Barford D. (1996). Molecular mechanisms of the protein serine/threonine phosphatases. Trends Biochem Sci, 21, 407–12
  • Bhaya D, Takahashi A, Grossman AR. (2001). Light regulation of type IV pilus-dependent motility by chemosensor-like elements in Synechocystis PCC 6803. Proc Natl Acad Sci USA, 98, 7540–5
  • Cadoret JC, Rousseau B, Perewoska I, et al. (2005). Cyclic nucleotides, the photosynthetic apparatus and response to a UV-B stress in the Cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem, 280, 33935–44
  • Chang C, Kwok SF, Bleecker AB, Meyerowitz EM. (1993). Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science, 262, 539–44
  • Duplessis MR, Karol KG, Adman ET, et al. (2007). Chloroplast His-to-Asp signal transduction: a potential mechanism for plastid gene regulation in Heterosigma akashiwo (Raphidophyceae). BMC Evol Biol, 7, 70
  • Durocher D, Jackson SP. (2002). The FHA domain. FEBS Lett, 513, 58–66
  • Fiedler B, Broc D, Schubert H, et al. (2004). Involvement of cyanobacterial phytochromes in growth under different light qualities and quantities. Photochem Photobiol, 79, 551–5
  • Galkin AN, Mikheeva LE, Shestakov SV. (2003). Insertional inactivation of genes encoding eukaryotic type serine/threonine protein kinases in cyanobacterium Synechocystis sp. PCC 6803. Mikrobiologiia, 72, 64–9
  • Habib K, Kumar S, Manikar N, et al. (2011). Biochemical effect of carbaryl on oxidative stress, antioxidant enzymes and osmolytes of cyanobacterium Calothrix brevissima. Bull Environ Contam Toxicol, 87, 615–20
  • Han G, Zhang CC. (2001). On the origin of Ser/Thr kinases in a prokaryote. FEMS Microbiol Lett, 200, 79–84
  • Hanks SK, Hunter T. (1995). Protein kinases 6. The eukaryotic protein kinase superfamily: kinasE. (catalytic) domain structure and classification. FASEB J, 9, 576–96
  • He, Q, Dolganov N, Bjorkman O, Grossman AR. (2001). The high light-inducible polypeptides in Synechocystis PCC 6803. Expression and function in high light. J Biol Chem, 276, 306–14
  • He YY, Klisch M, Hader DP. (2002). Adaptation of cyanobacteria to UV-B stress correlated with oxidative stress and oxidative damage. Photochem Photobiol, 76, 188–96
  • Hihara Y, Sonoike K, Kanehisa M, Ikeuchi M. (2003). DNA microarray analysis of redox-responsive genes in the genome of the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol, 185, 1719–25
  • Hirani TA, Suzuki I, Murata N, et al. (2001). Characterization of a two-component signal transduction system involved in the induction of alkaline phosphatase under phosphate-limiting conditions in Synechocystis sp. PCC 6803. Plant Mol Biol, 45, 133–44
  • Houot L, Floutier M, Marteyn B, et al. (2007). Cadmium triggers an integrated reprogramming of the metabolism of Synechocystis PCC 6803, under the control of the Slr1738 regulator. BMC Genomics, 8, 78--97
  • Hsiao HY, He, Q, Van Waasbergen LG, Grossman AR. (2004). Control of photosynthetic and high-light-responsive genes by the histidine kinase DspA: negative and positive regulation and interactions between signal transduction pathways. J Bacteriol, 186, 3882–8
  • Huang L, McCluskey MP, Ni H, LaRossa RA. (2002). Global gene expression profiles of the cyanobacterium Synechocystis sp. strain PCC 6803 in response to irradiation with UV-B and white light. J Bacteriol, 184, 6845–58
  • Hubschmann T, Yamamoto H, Gieler T, et al. (2005). Red and far-red light alter the transcript profile in the cyanobacterium Synechocystis sp. PCC 6803: impact of cyanobacterial phytochromes. FEBS Lett, 579, 1613–18
  • Imamura S, Asayama M. (2009). Sigma factors for cyanobacterial transcription. Gene Regulation Syst Biol, 3, 65–87
  • Inaba M, Suzuki I, Szalontai B, et al. (2003). Gene-engineered rigidification of membrane lipids enhances the cold inducibility of gene expression in Synechocystis. J Biol Chem, 278, 12191–8
  • Ito H, Mutsuda M, Murayama Y, et al. (2009). Cyanobacterial daily life with Kai-based circadian and diurnal genome-wide transcriptional control in Synechococcus elongatus. Proc Natl Acad Sci USA, 106, 14168–73
  • Ivleva NB, Gao T, LiWang AC, Golden SS. (2006). Quinone sensing by the circadian input kinase of the cyanobacterial circadian clock. Proc Natl Acad Sci USA, 103, 17468–73
  • Jung K, Veen M, Altendorf K. (2000). K+ and ionic strength directly influence the autophosphorylation activity of the putative turgor sensor KdpD of Escherichia coli. J Biol Chem, 275, 40142–7
  • Juntarajumnong W, Hirani TA, Simpson JM, et al. (2007). Phosphate sensing in Synechocystis sp. PCC 6803: SphU and the SphS-SphR two-component regulatory system. Arch Microbiol, 188, 389–402
  • Kamei A, Yoshihara S, Yuasa T, et al. (2003). Biochemical and functional characterization of a eukaryotic-type protein kinase, SpkB, in the cyanobacterium, Synechocystis sp. PCC 6803. Curr Microbiol, 46, 296–301
  • Kamei A, Yuasa T, Geng X, Ikeuchi M. (2002). Biochemical examination of the potential eukaryotic-type protein kinase genes in the complete genome of the unicellular cyanobacterium Synechocystis sp. PCC 6803. DNA Res, 9, 71–8
  • Kamei A, Yuasa T, Orikawa K, et al. (2001). A eukaryotic-type protein kinase, SpkA, is required for normal motility of the unicellular Cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol, 183, 1505–10
  • Kaneko T, Nakamura Y, Sasamoto S, et al. (2003). Structural analysis of four large plasmids harboring in a unicellular cyanobacterium, Synechocystis sp. PCC 6803. DNA Res, 10, 221–8
  • Kaneko T, Sato S, Kotani H, et al. (1996a). Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res, 3, 109–36
  • Kaneko T, Sato S, Kotani H, et al. (1996b). Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. (supplement). DNA Res, 3, 185–209
  • Kanesaki Y, Suzuki I, Allakhverdiev SI, et al. (2002). Salt stress and hyperosmotic stress regulate the expression of different sets of genes in Synechocystis sp PCC 6803. Biochem Biophys Res Commun, 290, 339–48
  • Kanesaki Y, Yamamoto H, Paithoonrangsarid K, et al. (2007). Histidine kinases play important roles in the perception and signal transduction of hydrogen peroxide in the cyanobacterium, Synechocystis sp. PCC 6803. Plant J, 49, 313–24
  • Kappell AD, van Waasbergen LG. (2007). The response regulator RpaB binds the high light regulatory 1 sequence upstream of the high-light-inducible hliB gene from the cyanobacterium Synechocystis PCC 6803. Arch Microbiol, 187, 337–42
  • Kato T, Sato S, Nakamura Y, et al. (2003). Structural analysis of a Lotus japonicus genome. V. Sequence features and mapping of sixty-four TAC clones which cover the 6.4 mb regions of the genome. DNA Res, 10, 277–85
  • Kennelly PJ. (2003). Archaeal protein kinases and protein phosphatases: insights from genomics and biochemistry. Biochem J, 370, 373–89
  • Kim YH, Park YM, Kim SJ, et al. (2004). The role of Slr1443 in pilus biogenesis in Synechocystis sp. PCC 6803: involvement in post-translational modification of pilins. Biochem Biophys Res Commun, 315, 179–86
  • Kobayashi M, Ishizuka T, Katayama M, et al. (2004). Response to oxidative stress involves a novel peroxiredoxin gene in the unicellular cyanobacterium Synechocystis sp PCC 6803. Plant Cell Physiol, 45, 290–9
  • Kurian D, Jansen T, Maenpaa P. (2006). Proteomic analysis of heterotrophy in Synechocystis sp. PCC 6803. Proteomics, 6, 1483–94
  • Latifi A, Ruiz M, Zhang CC. (2009). Oxidative stress in cyanobacteria. FEMS Microbiol Rev, 33, 258–78
  • Lemeille S, Geiselmann J, Latifi A. (2005). Crosstalk regulation among group 2-sigma factors in Synechocystis PCC 6803. BMC Microbiol, 5, 18
  • Li H, Sherman LA. (2000). A redox-responsive regulator of photosynthesis gene expression in the cyanobacterium Synechocystis sp. Strain PCC 6803. J Bacteriol, 182, 4268–77
  • Li H, Singh AK, McIntyre LM, Sherman LA. (2004). Differential gene expression in response to hydrogen peroxide and the putative PerR regulon of Synechocystis sp strain PCC 6803. J Bacteriol, 186, 3331–45
  • Li RH, Ben Potters M, Shi L, Kennelly PJ. (2005). The protein phosphatases of Synechocystis sp strain PCC 6803: Open reading frames sll1033 and sll1387 encode enzymes that exhibit both protein-serine and protein-tyrosine phosphatase activity in vitro. J Bacteriol, 187, 5877–84
  • Liang C, Zhang X, Chi X, et al. (2011). Serine/threonine protein kinase SpkG is a candidate for high salt resistance in the unicellular cyanobacterium Synechocystis sp. PCC 6803. PLoS One, 6, e18718
  • Lindahl M, Florencio FJ. (2003). Thioredoxin-linked processes in cyanobacteria are as numerous as in chloroplasts, but targets are different. Proc Natl Acad Sci USA, 100, 16107–12
  • Lopez-Maury L, Garcia-Dominguez M, Florencio FJ, Reyes JC. (2002). A two-component signal transduction system involved in nickel sensing in the cyanobacterium Synechocystis sp. PCC 6803. Mol Bacteriol, 43, 247–56
  • Los DA, Murata N. (2002). Sensing and response to low temperature in cyanobacteria. Amsterdam: Elsevier
  • Los DA, Murata N. (2004). Membrane fluidity and its roles in the perception of environmental signals. Biochim Biophys Acta, 1666, 142–57
  • Los DA, Zorina A, Sinetova M, et al. (2010). Stress sensors and signal transducers in cyanobacteria. Sensors. (Basel), 10, 2386–415
  • Mackey SR, Choi JS, Kitayama Y, et al. (2008). Proteins found in a CikA interaction assay link the circadian clock, metabolism, cell division in Synechococcus elongatus. J Bacteriol, 190, 3738–46
  • Maeda T, Wurgler-Murphy SM, Saito H. (1994). A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature, 369, 242–5
  • Manickavelu A, Nadarajan N, Ganesh SK, et al. (2006). Organogenesis induction in rice callus by cyanobacterial extracellular product. Afr J Biotechnol, 5, 437–9
  • Mansilla MC, de Mendoza D. (2005). The Bacillus subtilis desaturase: a model to understand phospholipid modification and temperature sensing. Arch Microbiol, 183, 229–35
  • Marin K, Suzuki I, Yamaguchi K, et al. (2003). Identification of histidine kinases that act as sensors in the perception of salt stress in Synechocystis sp. PCC 6803. Proc Natl Acad Sci USA, 100, 9061–6
  • Matsuda N, Uozumi N. (2006). Ktr-mediated potassium transport, a major pathway for potassium uptake, is coupled to a proton gradient across the membrane in Synechocystis sp. PCC 6803. Biosci Biotechnol Biochem, 70, 273–5
  • Mikami K, Kanesaki Y, Suzuki I, Murata N. (2002). The histidine kinase Hik33 perceives osmotic stress and cold stress in Synechocystis sp PCC 6803. Mol Bacteriol, 46, 905–15
  • Mizuno T, Kaneko T, Tabata S. (1996). Compilation of all genes encoding bacterial two-component signal transducers in the genome of the cyanobacterium, Synechocystis sp. strain PCC 6803. DNA Res, 3, 407–14
  • Montgomery BL, Lagarias JC. (2002). Phytochrome ancestry: sensors of bilins and light. Trends Plant Sci, 7, 357–66
  • Morrison SS, Mullineaux CW, Ashby MK. (2005). The influence of acetyl phosphate on DspA signalling in the Cyanobacterium Synechocystis sp. PCC 6803. BMC Microbiol, 5, 47
  • Murata N, Los DA. (2006). Histidine kinase Hik33 is an important participant in cold-signal transduction in cyanobacteria. Physiol Plantarum, 126, 17–27
  • Murata N, Suzuki I. (2006). Exploitation of genomic sequences in a systematic analysis to access how cyanobacteria sense environmental stress. J Exp Bot, 57, 235–47
  • Nodop A, Suzuki I, Barsch A, et al. (2006). Physiological and molecular characterization of a Synechocystis sp. PCC 6803 mutant lacking histidine kinase Slr1759 and response regulator Slr1760. Z Naturforsch C, 61, 865–78
  • Novikova GV, Moshkov IE, Los DA. (2007). Protein sensors and transducers of cold, hyperosmotic and salt stresses in cyanobacteria and plants. Mol BioL, (Mosk), 41, 478–90
  • Ogawa T, Bao DH, Katoh H, et al. (2002). A two-component signal transduction pathway regulates manganese homeostasis in Synechocystis 6803, a photosynthetic organism. J Biol Chem, 277, 28981–6
  • Ohkawa H, Price GD, Badger MR, Ogawa T. (2000b). Mutation of ndh genes leads to inhibition of CO2 uptake rather than uptake in Synechocystis sp. strain PCC 6803. J Bacteriol, 182, 2591–6
  • Osanai T, Kanesaki Y, Nakano T, et al. (2005). Positive regulation of sugar catabolic pathways in the cyanobacterium Synechocystis sp. PCC 6803 by the group 2 sigma factor sigE. J Biol Chem, 280, 30653–9
  • Paithoonrangsarid K, Shoumskaya MA, Kanesaki Y, et al. (2004). Five histidine kinases perceive osmotic stress and regulate distinct sets of genes in Synechocystis. J Biol Chem, 279, 53078–86
  • Panichkin VB, Kobayashi AS, Kanaseki T, et al. (2006). Serine/threonine protein kinase SpkA in Synechocystis sp. strain PCC 6803 is a regulator of expression of three putative pilA operons, formation of thick pili, cell motility. J Bacteriol, 188, 7696–9
  • Perez-Perez ME, Florencio FJ, Lindahl M. (2006). Selecting thioredoxins for disulphide proteomics: target proteomes of three thioredoxins from the cyanobacterium Synechocystis sp. PCC 6803. Proteomics, 6, S186–95
  • Puthiyaveetil S, Allen JF. (2009). Chloroplast two-component systems: evolution of the link between photosynthesis and gene expression. Proc. R. Soc. B, doi:10.1098.
  • Sakamoto T, Murata N. (2002). Regulation of the desaturation of fatty acids and its role in tolerance to cold and salt stress. Curr Opin Microbiol, 5, 208–10
  • Sarwat M, Ahmad P, Nabi G, Hu X. (2013). Ca2+ signals: the versatile decoders of environmental cues. Crit Rev Biotechnol, 33, 97–109
  • Shao HB, Chu LY, Shao MA, et al. (2008). Higher plant antioxidants and redox signaling under environmental stresses. Comptes Rendus Biologies, 331, 433–41
  • Shi L, Potts M, Kennelly PJ. (1998). The serine, threonine, and/or tyrosine-specific protein kinases and protein phosphatases of prokaryotic organisms: a family portrait. FEMS Microbiol Rev, 22, 229–53
  • Shoumskaya MA, Paithoonrangsarid K, Kanesaki Y, et al. (2005). Identical Hik-Rre systems are involved in perception and transduction of salt signals and hyperosmotic signals but regulate the expression of individual genes to different extents in Synechocystis. J Biol Chem, 280, 21531–8
  • Singh AK, Elvitigala T, Bhattacharyya-Pakrasi M, et al. (2008). Integration of carbon and nitrogen metabolism with energy production is crucial to light acclimation in the cyanobacterium Synechocystis. Plant Physiol, 148, 467–78
  • Singh AK, Li H, Sherman LA. (2004). Microarray analysis and redox control of gene expression in the cyanobacterium Synechocystis sp. PCC 6803. Physiol Plant, 120, 27–35
  • Singh AK, Sherman LA. (2005). Pleiotropic effect of a histidine kinase on carbohydrate metabolism in Synechocystis sp. strain PCC 6803 and its requirement for heterotrophic growth. J Bacteriol, 187, 2368–76
  • Skjanes K, Rebours C, Lindblad P. (2013). Potential for green microalgae to produce hydrogen, pharmaceuticals and other high value products in a combined process. Crit Rev Biotechnol, 33, 172–215
  • Stork T, Michel KP, Pistorius EK, Dietz KJ. (2005). Bioinformatic analysis of the genomes of the cyanobacteria Synechocystis sp. PCC 6803 and Synechococcus elongatus PCC 7942 for the presence of peroxiredoxins and their transcript regulation under stress. J Exp Bot, 56, 3193–206
  • Suzuki I, Kanesaki Y, Hayashi H, et al. (2005). The histidine kinase Hik34 is involved in thermotolerance by regulating the expression of heat shock genes in synechocystis. Plant Physiol, 138, 1409–21
  • Suzuki I, Kanesaki Y, Mikami K, et al. (2001). Cold-regulated genes under control of the cold sensor Hik33 in Synechocystis. Mol Bacteriol, 40, 235–44
  • Suzuki I, Los DA, Kanesaki Y, et al. (2000a). The pathway for perception and transduction of low-temperature signals in Synechocystis. EMBO J, 19, 1327–34
  • Suzuki I, Los DA, Murata N. (2000b). Perception and transduction of low-temperature signals to induce desaturation of fatty acids. Biochem Soc Trans, 28, 628–30
  • Suzuki S, Ferjani A, Suzuki I, Murata N. (2004). The SphS-SphR two component system is the exclusive sensor for the induction of gene expression in response to phosphate limitation in synechocystis. J Biol Chem, 279, 13234–40
  • Trautmann D, Voss B, Wilde A, et al. (2012). Microevolution in cyanobacteria: re-sequencing a motile substrain of Synechocystis sp. PCC 6803. DNA Res
  • Tu CJ, Shrager J, Burnap RL, et al. (2004). Consequences of a deletion in dspA on transcript accumulation in Synechocystis sp. strain PCC 6803. J Bacteriol, 186, 3889–902
  • van Waasbergen LG, Dolganov N, Grossman AR. (2002). nblS, a gene involved in controlling photosynthesis-related gene expression during high light and nutrient stress in Synechococcus elongatus PCC 7942. J Bacteriol, 184, 2481–90
  • Verhamme DT, Arents JC, Postma PW, et al. (2002). Investigation of in vivo cross-talk between key two-component systems of Escherichia coli. Microbiology, 148, 69–78
  • Vinnemeier J, Kunert A, Hagemann M. (1998). Transcriptional analysis of the isiAB operon in salt-stressed cells of the cyanobacterium Synechocystis sp. PCC 6803. FEMS Microbiol Lett, 169, 323–30
  • Walderhaug MO, Polarek JW, Voelkner P, et al. (1992). KdpD and KdpE, proteins that control expression of the kdpABC operon, are members of the two-component sensor-effector class of regulators. J Bacteriol, 174, 2152–9
  • Wang HL, Postier BL, Burnap RL. (2004). Alterations in global patterns of gene expression in Synechocystis sp. PCC 6803 in response to inorganic carbon limitation and the inactivation of ndhR, a LysR family regulator. J Biol Chem, 279, 5739–51
  • Wang L, Sun YP, Chen WL, et al. (2002). Genomic analysis of protein kinases, protein phosphatases and two-component regulatory systems of the cyanobacterium Anabaena sp. strain PCC 7120. FEMS Microbiol Lett, 217, 155–65
  • West AH, Stock AM. (2001). Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci, 26, 369–76
  • Wilde A, Fiedler B, Borner T. (2002). The cyanobacterial phytochrome Cph2 inhibits phototaxis towards blue light. Mol Bacteriol, 44, 981–8
  • Xue-Xuan X, Hong-Bo S, Yuan-Yuan M, et al. (2010). Biotechnological implications from abscisic acid (ABA) roles in cold stress and leaf senescence as an important signal for improving plant sustainable survival under abiotic-stressed conditions. Crit Rev Biotech, 30, 222–30
  • Yamaguchi K, Suzuki I, Yamamoto H, et al. (2002). A two-component Mn2+-sensing system negatively regulates expression of the mntCAB operon in Synechocystis. Plant Cell, 14, 2901–13
  • Yang MK, Qiao ZX, Zhang WY, et al. (2013).Global phosphoproteomic analysis reveals diverse functions of Serine/Threonine/Tyrosine phosphorylation in the model cyanobacterium Synechococcus sp. strain PCC 7002. J Proteome Res, DOI: 10.1021/pr4000043
  • Yao D, Kieselbach T, Komenda J, et al. (2007). Localization of the small CAB-like proteins in photosystem II. J Biol Chem, 282, 267–76
  • Yeremenko N, Jeanjean R, Prommeenate P, et al. (2005). Open reading frame ssr2016 is required for antimycin A-sensitive photosystem I-driven cyclic electron flow in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol, 46, 1433–6
  • Yoshihara S, Suzuki, F, Fujita H, et al. (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, 1299–304
  • Yoshimura T, Imamura S, Tanaka K, et al. (2007). Cooperation of group 2 sigma factors, SigD and SigE for light-induced transcription in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett, 581, 1495–500
  • Zabulon G, Richaud C, Guidi-Rontani C, Thomas JC. (2007). NblA gene expression in Synechocystis PCC 6803 strains lacking DspA. (Hik33) and a NblR-like protein. Curr Microbiol, 54, 36–41
  • Zhang CC, Gonzalez L, Phalip V. (1998b). Survey, analysis and genetic organization of genes encoding eukaryotic-like signaling proteins on a cyanobacterial genome. Nucleic Acids Res, 26, 3619–25
  • Zhang X, Zhao, F, Guan X, et al. (2007). Genome-wide survey of putative serine/threonine protein kinases in cyanobacteria. BMC Genomics, 8, 395
  • Zhang XW. (2008). Comparative genomes analysis of cyanobacterial signal transduction systems and functional validation of their important genes. In: Marine biology. Qingdao: Institute of Oceanology, Chinese Academy of Sciences, 1--87
  • Zorina A, Stepanchenko N, Novikova GV, et al. (2011). Eukaryotic-like Ser/Thr protein kinases SpkC/F/K were involved in phosphorylation of GroES in the cyanobacterium Synechocystis. DNA Res, 18, 137–51

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.