Advertisement

Sensors and Signal Transducers of Environmental Stress in Cyanobacteria

  • Yu Kanesaki
  • Dmitry. A. Los
  • Iwane Suzuki
  • Norio Murata
Chapter

Summary

The perception of environmental stress and the subsequent transduction of stress signals are primary events in the acclimation of all organisms to changes in their environment. Many of the molecular sensors and transducers of environmental stress cannot be identified by traditional and conventional methods. Based on genomic information, a systematic approach has been applied to the solution of this problem in cyanobacteria, involving mutagenesis of potential sensors and signal transducers in combination with DNA microarray analyses for the genome-wide expression of genes. Almost all of the histidine kinases (Hiks) and response regulators (Rres) have been successfully inactivated by targeted mutagenesis in the unicellular cyanobacterium Synechocystis sp. PCC 6803. Screening of mutant libraries by genome-wide DNA microarray analysis under various stress and non-stress conditions has allowed identification of the Hiks and Rres that perceive and transduce signals of environmental stress. In this chapter, we summarize recent progress in the identification of regulatory two-component systems. In addition, we discuss the potential roles of Spks, DNA supercoiling, sigma factors and transcription factors in the regulation of the responses of cyanobacterial cells to various types of stress.

Keywords

DNA microarray environment histidine kinase response regulator sensor signal perception signal transduction stress 

Abbreviations:

cph -

gene for cyanobacterial phytochrome;

crt -

gene for carotenoid metabolism; phytoene desaturase;

etr -

gene for ethylene-receptor;

fab -

gene for fatty-acid biosynthesis;

feo -

gene for ferrous iron transport;

FTIR-

Fourier-transform infrared spectrometry;

Fus -

gene for fusion;

glo -

gene for glyoxylase (lactoylglutathione lyase);

htp -

gene for heat-tolerance protein;

Hik-

histidine kinase;

hli-

gene for high light-inducible protein;

kdp -

gene for high-affinity potassium transporter;

nbl -

gene for phycobilisome degradation protein;

ndh -

gene for NADH dehydrogenase;

pgr -

gene for plant growth regulator;

pho -

gene for low affinity to ortho-phosphate;

rbp -

gene for RNA binding protein;

Rre-

response regulator;

sig -

RNA polymerase sigma factor;

sph -

gene for Synechocystis phosphate sensor/regulator;

Spk-

serine/threonine protein kinase;

Tyr-

tyrosine protein kinases

Notes

Acknowledgements

This work has been supported by the Cooperative Research Program of the National Institute for Basic Biology, Japan, by a Sasagawa Scientific Research Grant from the Japan Science Society to Y.K., a grant from the Russian Foundation for Basic Research (no. 09-04-01074) and a grant from the “Molecular and Cell Biology Program” of the Russian Academy of Sciences to D.A.L.

References

  1. Adamcik J, Viglasky V, Valle F, Antalik M, Podhradsky D, Dietler G (2002) Effect of bacteria growth temperature on the distribution of supercoiled DNA and its thermal stability. Electrophoresis 23:3300-3309PubMedCrossRefGoogle Scholar
  2. Aguilar PS, Hernandez-Arriaga AM, Cybulski LE, Erazo AC, de Mendoza D (2001) Molecular basis of thermosensing: a two-component signal transduction thermometer in Bacillus subtilis. EMBO J 20:1681-1691PubMedCrossRefGoogle Scholar
  3. Allakhverdiev SI, Nishiyama Y, Miyairi S, Yamamoto H, Inagaki N, Kanesaki Y, Murata N (2002) Salt stress inhibits the repair of photodamaged Photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis. Plant Physiol 130:1443-1453PubMedCrossRefGoogle Scholar
  4. Aoyama T, Takanami M (1988) Supercoiling response of E. coli promoters with different spacer lengths. Biochim Biophys Acta 949:311-317PubMedCrossRefGoogle Scholar
  5. Aravind L, Anantharaman V, Iyer LM (2003) Evolutionary connections between bacterial and eukaryotic signaling systems: a genomic perspective. Curr Opin Microbiol 6:490-497PubMedCrossRefGoogle Scholar
  6. Bartsevich VV, Pakrasi HB (1995) Molecular identification of an ABC transporter complex for manganese: analysis of a cyanobacterial mutant strain impaired in the photosynthetic oxygen evolution process. EMBO J 14:1845-1853PubMedGoogle Scholar
  7. Bartsevich VV, Pakrasi HB (1996) Manganese transport in the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 271:26057-26061PubMedCrossRefGoogle Scholar
  8. Bartsevich VV, Shestakov SV (1995) The dspA gene product of the cyanobacterium Synechocystis sp. strain PCC 6803 influences sensitivity to chemically different growth inhibitors and has amino acid similarity to histidine protein kinases. Microbiology 141:2915-2920PubMedCrossRefGoogle Scholar
  9. Cheung KJ, Badarinarayana V, Selinger DW, Janse D, Church GM (2003) A microarray-based antibiotic screen identifies a regulatory role for supercoiling in the osmotic stress response of Escherichia coli. Genome Res 13206-215PubMedCrossRefGoogle Scholar
  10. Conter A, Menchon C, Gutierrez C (1997) Role of DNA supercoiling and rpoS sigma factor in the osmotic and growth phase-dependent induction of the gene osmE of Escherichia coli K12. J Mol Biol 273:75-83PubMedCrossRefGoogle Scholar
  11. Dorman CJ (1996) Flexible response: DNA supercoiling, transcription and bacterial adaptation to environmental stress. Trends Microbiol 4:214-216PubMedCrossRefGoogle Scholar
  12. Duplessis MR, Karol KG, Adman ET, Choi LY, Jacobs MA, Cattolico RA (2007) Chloroplast His-to-Asp signal transduction: a potential mechanism for plastid gene regulation in Heterosigma akashiwo (Raphidophyceae). BMC Evol Biol 7:70. http://www.biomedcentral.com/1471-2148/7/70 (May 3, 2007)
  13. Elhai J, Wolk CP (1988) Conjugal transfer of DNA into cyanobacteria. Methods Enzymol 167:747-765PubMedCrossRefGoogle Scholar
  14. Fiedler B, Broc D, Schubert H, Rediger A, Boerner T, Wilde A (2004) Involvement of cyanobacterial phytochromes in growth under different light qualities and quantities. Photochem Photobiol 79:551-555PubMedCrossRefGoogle Scholar
  15. Franco RJ, Drlica K (1989) Gyrase inhibitors can increase gyrA expression and DNA supercoiling. J Bacteriol 171:6573-6579PubMedGoogle Scholar
  16. Galkin AN, Mikheeva LE, Shestakov SV (2003) Insertional inactivation of genes encoding eukaryotic-type serine/threonine protein kinases in the cyanobacterium Synechocystis sp. PCC 6803. Mikrobiologiia 72:64-69PubMedGoogle Scholar
  17. Gellert M, O’Dea MH, Itoh T, Tomizawa J (1976) Novobiocin and coumermycin inhibit DNA supercoiling catalyzed by DNA gyrase. Proc Natl Acad Sci USA 73:4474-4478PubMedCrossRefGoogle Scholar
  18. Gilmour D, Gellert M (1961) The binding of p-chloromercuribenzoate by myosin. Arch Biochem Biophys 93:605-616PubMedCrossRefGoogle Scholar
  19. Glatz A, Vass I, Los DA, Vigh L (1999) The Synechocystis model of stress: from molecular chaperons to membranes. Plant Physiol Biochem 37:1-12CrossRefGoogle Scholar
  20. Graeme-Cook KA, May G, Bremer E, Higgins CF (1989) Osmotic regulation of porin expression: a role for DNA supercoiling. Mol Microbiol 3:1287-1294PubMedCrossRefGoogle Scholar
  21. Grau R, Gardiol D, Glikin GC, de Mendoza D (1994) DNA supercoiling and thermal regulation of unsaturated fatty acid synthesis in Bacillus subtilis. Mol Microbiol 11:933-941PubMedCrossRefGoogle Scholar
  22. Haselkorn R (1991) Genetic systems in cyanobacteria. Methods Enzymol 204:418-430PubMedCrossRefGoogle Scholar
  23. Hecker M, Schumann W, Volker U (1996) Heat-shock and general stress response in Bacillus subtilis. Mol Microbiol 19:417-428PubMedCrossRefGoogle Scholar
  24. Higgins CF, Dorman CJ, Stirling DA, Waddell L, Booth IR, May G, Bremer E (1988) A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. typhimurium and E. coli. Cell 52:569-584PubMedCrossRefGoogle Scholar
  25. Hirani TA, Suzuki I, Murata N, Hayashi H, Eaton-Rye JJ (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 45:133-144PubMedCrossRefGoogle Scholar
  26. 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 186:3882-3888PubMedCrossRefGoogle Scholar
  27. Hübschmann T, Yamamoto H, Gieler T, Murata N, 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 579:1613-1618PubMedCrossRefGoogle Scholar
  28. Hughes J, Lamparter T, Mittmann F, Hartmann E, Gartner W, Wilde A, Boerner T (1997) A prokaryotic phytochrome. Nature 386:663PubMedCrossRefGoogle Scholar
  29. Hulko M, Berndt F, Gruber M, Linder JU, Truffault V, Schultz A, Martin J, Schultz JE, Lupas AN, Coles M (2006) The HAMP domain structure implies helix rotation in transmembrane signaling. Cell 126:929-940PubMedCrossRefGoogle Scholar
  30. Inaba M, Suzuki I, Szalontai B, Kanesaki Y, Los DA, Hayashi H, Murata N (2003) Gene-engineered rigidification of membrane lipids enhances the cold inducibility of gene expression in Synechocystis. J Biol Chem 278:12191-12198PubMedCrossRefGoogle Scholar
  31. Iwasaki H, Williams SB, Kitayama Y, Ishiura M, Golden SS, Kondo T (2000) A kaiC-interacting sensory histidine kinase, SasA, necessary to sustain robust circadian oscillation in cyanobacteria. Cell 101:223-233PubMedCrossRefGoogle Scholar
  32. Jorissen HJ, Quest B, Remberg A, Coursin T, Braslavsky SE, Schaffner K, Tandeau de Marsac N, Gartner W (2002) Two independent, light-sensing, two-component systems in a filamentous cyanobacterium. Eur J Biochem 269:2662-2671PubMedCrossRefGoogle Scholar
  33. 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 275:40142-40147PubMedCrossRefGoogle Scholar
  34. Juntarajumnong W, Hirani TA, Simpson JM, Incharoensakdi A, Eaton-Rye JJ (2007) Phosphate sensing in Synechocystis sp. PCC 6803: SphU and the SphS-SphR two-component regulatory system. Arch Microbiol 188:389-402PubMedCrossRefGoogle Scholar
  35. Kamei A, Yuasa T, Orikawa K, Geng XX, Ikeuchi M (2001) A eukaryotic-type protein kinase, SpkA, is required for normal motility of the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 183:1505-1510PubMedCrossRefGoogle Scholar
  36. Kamei A, Yoshihara S, Yuasa T, Geng X, Ikeuchi M (2003) Biochemical and functional characterization of a eukaryotic-type protein kinase, SpkB, in the cyanobacterium Synechocystis sp. PCC 6803. Curr Microbiol 46:296-301PubMedCrossRefGoogle Scholar
  37. 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, 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 3:185-209PubMedCrossRefGoogle Scholar
  38. Kaneko T, Nakamura Y, Sasamoto S, Watanabe A, Kohara M, Matsumoto M, Shimpo S, Yamada M, Tabata S (2003) Structural analysis of four large plasmids harboring in a unicellular cyanobacterium, Synechocystis sp. PCC 6803. DNA Res 10:221-228PubMedCrossRefGoogle Scholar
  39. Kanesaki Y, Suzuki I, Allakhverdiev SI, Mikami K, Murata N (2002) Salt stress and hyperosmotic stress regulate the expression of different sets of genes in Synechocystis sp. PCC 6803. Biochem Biophys Res Commun 290:339-348PubMedCrossRefGoogle Scholar
  40. Kanesaki Y, Yamamoto H, Paithoonrangsarid K, Shoumskaya M, Suzuki I, Hayashi H, Murata N (2007) Histidine kinases play important roles in the perception and signal transduction of H2O2 in the cyanobacterium Synechocystis. Plant J 49:313-324PubMedCrossRefGoogle Scholar
  41. 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 187:337-342PubMedCrossRefGoogle Scholar
  42. Kehoe DM, Grossman AR (1994) Complementary chromatic adaptation: photoperception to gene regulation. Semin Cell Biol 5:303-313PubMedCrossRefGoogle Scholar
  43. Kehoe DM, Grossman AR (1996) Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science 273:1409-1412PubMedCrossRefGoogle Scholar
  44. Koretke KK, Lupas AN, Warren PV, Rosenberg M, Brown JR (2000) Evolution of two-component signal transduction. Mol Biol Evol 17:1956-1970PubMedCrossRefGoogle Scholar
  45. Leonard CJ, Aravind L, Koonin EV (1998) Novel families of putative protein kinases in bacteria and archaea: evolution of the “eukaryotic” protein kinase superfamily. Genome Res 8:1038-1047PubMedGoogle Scholar
  46. Li H, Sherman LA (2000) A redox-responsive regulator of photosynthesis gene expression in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 182:4268-4277PubMedCrossRefGoogle Scholar
  47. 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 Microbiol 43:247-256PubMedCrossRefGoogle Scholar
  48. López-Maury L, Florencio FJ, Reyes JC (2003) Arsenic sensing and resistance system in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 185:5363-5371PubMedCrossRefGoogle Scholar
  49. Los DA (2004) The effect of low-temperature-induced DNA supercoiling on the expression of the desaturase genes in Synechocystis. Cell Mol Biol 50:605-612PubMedGoogle Scholar
  50. Los DA, Murata N (1999) Responses to cold shock in cyanobacteria. J Mol Microbiol Biotechnol 1:221-230PubMedGoogle Scholar
  51. Los DA, Murata N (2000) Regulation of enzymatic activity and gene expression by membrane fluidity. Science’s Signal Transduction Knowledge Environment 62: PE1. http://www.stke.org/cgi/content/full/OC_sigtrans;2000/62/pe1
  52. Los DA, Murata N (2002) Sensing and response to low temperature in cyanobacteria. In: Storey KB, Storey JM (eds) Cell and molecular responses to stress, sensing, signaling and cell adaptation, vol 3. Elsevier, Amsterdam, pp 139-153CrossRefGoogle Scholar
  53. Los DA, Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. Biochim Biophys Acta 1666:142-157PubMedCrossRefGoogle Scholar
  54. Marin K, Suzuki I, Yamaguchi K, Ribbeck K, Yamamoto H, Kanesaki Y, Hagemann M, Murata N (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 100:9061-9066PubMedCrossRefGoogle Scholar
  55. Mikami K, Murata N (2003) Membrane fluidity and the perception of environmental signals in cyanobacteria and plants. Prog Lipid Res 42:527-543PubMedCrossRefGoogle Scholar
  56. 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 Microbiol 46:905-915PubMedCrossRefGoogle Scholar
  57. 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 3:407-414PubMedCrossRefGoogle Scholar
  58. Murata N, Los DA (2006) Histidine kinase Hik33 is an important participant in cold signal transduction in cyanobacteria. Physiol Plant 126:17-27CrossRefGoogle Scholar
  59. Murata N, Suzuki I (2006) Exploitation of genomic sequences in a systematic analysis to access how cyanobacteria sense environmental stress. J Exp Bot 57:235-247PubMedCrossRefGoogle Scholar
  60. Murata N, Wada H (1995) Acyl-lipid desaturases, their importance in the tolerance and acclimatization to cold of cyanobacteria. Biochem J 308:1-8PubMedGoogle Scholar
  61. Nakamoto H, Suzuki M, Kojima K (2003) Targeted inactivation of the hrcA repressor gene in cyanobacteria. FEBS Lett 549:57-62PubMedCrossRefGoogle Scholar
  62. Ogawa T, Bao DH, Katoh H, Shibata M, Pakrasi HB, Bhattacharyya-Pakrasi M (2002) A two-component signal transduction pathway regulates manganese homeostasis in Synechocystis 6803, a photosynthetic organism. J Biol Chem 277:28981-28986PubMedCrossRefGoogle Scholar
  63. Okamoto S, Ikeuchi M, Ohmori M (1999) Experimental analysis of recently transposed insertion sequences in the cyanobacterium Synechocystis sp. PCC 6803. DNA Res 6:265-273PubMedCrossRefGoogle Scholar
  64. Osanai T, Kanesaki Y, Nakano T, Takahashi H, Asayama M, Shirai M, Kanehisa M, Suzuki I, Murata N, Tanaka K (2005) Positive regulation of sugar catabolic pathways in the cyanobacterium Synechocystis sp. PCC 6803 by the group 2 sigma factor sigE. J Biol Chem 280:30653-30659PubMedCrossRefGoogle Scholar
  65. Paithoonrangsarid K, Shoumskaya MA, Kanesaki Y, Satoh S, Tabata S, Los DA, Zinchenko VV, Hayashi H, Tanticharoen M, Suzuki I, Murata N (2004) Five histidine kinases perceive osmotic stress and regulate distinct sets of genes in Synechocystis. J Biol Chem 279:53078-53086PubMedCrossRefGoogle Scholar
  66. Panichkin VB, Arakawa-Kobayashi S, Kanaseki T, Suzuki I, Los DA, Shestakov SV, Murata N (2006) 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 188:7696-7699PubMedCrossRefGoogle Scholar
  67. Schmitz O, Katayama M, Williams SB, Kondo T, Golden SS (2000) CikA, a bacterio-phytochrome, that resets the cyanobacterial circadian clock. Science 289:765-768PubMedCrossRefGoogle Scholar
  68. 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 22:229-253PubMedCrossRefGoogle Scholar
  69. Shoumskaya MA, Paithoonrangsarid K, Kanesaki Y, Los DA, Zinchenko VV, Tanticharoen M, Suzuki I, Murata N (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 80:21531-21538CrossRefGoogle Scholar
  70. Sineshchekov V, Hughes J, Hartmann E, Lamparter T (1998) Fluorescence and photochemistry of recombinant phytochrome from the cyanobacterium Synechocystis. Photochem Photobiol 67:263-267PubMedCrossRefGoogle Scholar
  71. Sineshchekov OA, Trivedi VD, Sasaki J, Spudich JL (2005) Photochromicity of Anabaena sensory rhodopsin, an atypical microbial receptor with a cis-retinal light-adapted form. J Biol Chem 280:14663-14668PubMedCrossRefGoogle Scholar
  72. Stock AM, Robinson VL, Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69:183-215PubMedCrossRefGoogle Scholar
  73. Suzuki I, Los DA, Kanesaki Y, Mikami K, Murata N (2000) The pathway for perception and transduction of low-temperature signals in Synechocystis. EMBO J 19:1327-1334PubMedCrossRefGoogle Scholar
  74. Suzuki I, Kanesaki Y, Mikami K, Kanehisa M, Murata N (2001) Cold-regulated genes under control of the cold sensor Hik33 in Synechocystis. Mol Microbiol 40:235-244PubMedCrossRefGoogle Scholar
  75. 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 279:13234-13240PubMedCrossRefGoogle Scholar
  76. Suzuki I, Kanesaki Y, Hayashi H, Hall JJ, Simon WJ, Slabas AR, Murata N (2005) The histidine kinase Hik34 is involved in thermotolerance by regulating the expression of heat-shock genes in Synechocystis. Plant Physiol 138:1409-1421PubMedCrossRefGoogle Scholar
  77. Szalontai B, Nishiyama Y, Gombos Z, Murata N (2000) Membrane dynamics as seen by Fourier Transform Infrared Spectroscopy in a cyanobacterium, Synechocystis PCC 6803: The effects of lipid unsaturation and the protein-to-lipid ratio. Biochim Biophys Acta 1509:409-419PubMedCrossRefGoogle Scholar
  78. Takai N, Nakajima M, Oyama T, Kito R, Sugita C, Sugita M, Kondo T, Iwasaki H (2006) A KaiC-associating SasA-RpaA two-component regulatory system as a major circadian timing mediator in cyanobacteria. Proc Natl Acad Sci USA 103:12109-12114PubMedCrossRefGoogle Scholar
  79. Tao W, Malone CL, Ault AD, Deschenes RJ, Fassler JS (2002) A cytoplasmic coiled-coil domain is required for histidine kinase activity of the yeast osmosensor SLN1. Mol Microbiol 43:459-473PubMedCrossRefGoogle Scholar
  80. Tasaka Y, Gombos Z, Nishiyama Y, Mohanty P, Ohba T, Ohki K, Murata N (1996) Targeted mutagenesis of acyl-lipid desaturases in Synechocystis: Evidence for the important roles of polyunsaturated membrane lipids in growth, respiration and photosynthesis. EMBO J 15:6416-6425PubMedGoogle Scholar
  81. Taylor BL, Zhulin IB (1999) PAS domains: internal sensors of oxygen, redox potential and light. Microbiol Mol Biol Rev 63:479-506PubMedGoogle Scholar
  82. Tu CJ, Shrager J, Burnap RL, Postier BL, Grossman AR (2004) Consequences of a deletion in dspA on transcript accumulation in Synechocystis sp. strain PCC 6803. J Bacteriol 186:3889-3902PubMedCrossRefGoogle Scholar
  83. 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 184:2481-2490PubMedCrossRefGoogle Scholar
  84. Vermaas WF (1998) Gene modifications and mutation mapping to study the function of photosystem II. Methods Enzymol 297:293-310PubMedCrossRefGoogle Scholar
  85. Vogeley L, Sineshchekov OA, Trivedi VD, Sasaki J, Spudich JL, Luecke H (2004) Anabaena sensory rhodopsin: a photochromic color sensor at 2.0 A. Science 306:1390-1393PubMedCrossRefGoogle Scholar
  86. Walderhaug MO, Polarek JW, Voelkner P, Daniel JM, Hesse JE, Altendorf K, Epstein W (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 174:2152-2159PubMedGoogle Scholar
  87. Wang HL, Postier BL, Burnap RL (2004a) 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 279:5739-5751PubMedCrossRefGoogle Scholar
  88. Wang JC, Lynch AS (1993) Transcription and DNA supercoiling. Curr Opin Genet Dev 3:764-768PubMedCrossRefGoogle Scholar
  89. Wang T, Shen G, Balasubramanian R, McIntosh L, Bryant DA, Golbeck JH (2004b) The sufR gene (sll0088 in Synechocystis sp. strain PCC 6803) functions as a repressor of the sufBCDS operon in iron-sulfur cluster biogenesis in cyanobacteria. J Bacteriol 186:956-967PubMedCrossRefGoogle Scholar
  90. Weinstein-Fischer D, Elgrably-Weiss M, Altuvia S (2000) Escherichia coli response to hydrogen peroxide: a role for DNA supercoiling, topoisomerase I and Fis. Mol Microbiol 35:1413-1420PubMedCrossRefGoogle Scholar
  91. Widmann C, Gibson S, Jarpe MB, Johnson GL (1999) Mitogen activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol Rev 79:143-180PubMedGoogle Scholar
  92. Wilde A, Churin Y, Schubert H, Boerner T (1997) Disruption of a Synechocystis sp. PCC 6803 gene with partial similarity to phytochrome genes alters growth under changing light qualities. FEBS Lett 406:89-92PubMedCrossRefGoogle Scholar
  93. Williams JGK (1988) Construction of specific mutations in Photosystem II photosynthetic reaction center by genetic engineering methods in Synechocystis PCC6803. Methods Enzymol 167:766-778CrossRefGoogle Scholar
  94. Williams SB, Stewart V (1999) Functional similarities among two-component sensors and methyl-accepting chemotaxis proteins suggest a role for linker region amphipathic helices in transmembrane signal transduction. Mol Microbiol 33:1093-1102PubMedCrossRefGoogle Scholar
  95. Yamaguchi K, Suzuki I, Yamamoto H, Lyukevich A, Bodrova I, Los DA, Piven I, Zinchenko V, Kanehisa M, Murata N (2002) A two-component Mn2+-sensing system negatively regulates expression of the mntCAB operon in Synechocystis. Plant Cell 14:2901-2913PubMedCrossRefGoogle Scholar
  96. Yeh KC, Wu SH, Murphy JT, Lagarias JC (1997) A cyanobacterial phytochrome two-component light-sensory system. Science 277:1505-1508PubMedCrossRefGoogle Scholar
  97. Zabulon G, Richaud C, Guidi-Rontani C, Thomas JC (2007) NblA gene expression in Synechocystis PCC 6803 strains lacking DspA (Hik33) and an NblR-like protein. Curr Microbiol 54:36-41PubMedCrossRefGoogle Scholar
  98. Zhang CC, Gonzalez L, Phalip V (1998) Survey, analysis and genetic organization of genes encoding eukaryotic-like signaling proteins on a cyanobacterial genome. Nucleic Acids Res 26:3619-3625PubMedCrossRefGoogle Scholar
  99. Zhang CC, Jang J, Sakr S, Wang L (2005) Protein phosphorylation on Ser, Thr and Tyr residues in cyanobacteria. J Mol Microbiol Biotechnol 9:154-166PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Yu Kanesaki
    • 1
  • Dmitry. A. Los
    • 2
  • Iwane Suzuki
    • 3
  • Norio Murata
    • 4
  1. 1.Bio-Resource Genome Analysis CenterTokyo University of AgricultureSetagaya-kuJapan
  2. 2.Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia
  3. 3.Graduate School of Life and Environmental SciencesUniversity of TsukubaTennodaiJapan
  4. 4.National Institute for Basic BiologyMyodaijiJapan

Personalised recommendations