Cyanobacterial salt stress acclimation: Genetic manipulation and regulation

Stress Biology of Cyanobacteria: Molecular Mechanisms to Cellular Responses

Volumn , Issue , 2013, Pages 189-202

  Pade, Nadin ^a   Hagemann, Martin ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84922025973     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1201/b13853     Document Type: Chapter

References (90)

1. Galinski, E.A. and Trüper, H.G., Microbial behaviour in salt-stressed ecosystems, FEMS Microbiol. Rev., 15, 95, 1994.
2. Hagemann, M., Molecular biology of cyanobacterial salt acclimation, FEMS Microbiol. Rev., 35, 87, 2011.
3. Oren, A., The genera Haloanaerobium, Halobacteroides and Sporohalobacter, in The Prokaryotes. A Handbook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Applications, Balows, A., Trüper, H.G., Dworkin, M., Harder, W., and Schleifer, K.-H., Eds., Springer-Verlag, New York, 1992, p. 1893.
4. Oren, A. and Mana, L., Amino acid composition of bulk protein and salt relationships of selected enzymes of Salinibacter ruber, an extremely halophilic bacterium, Extremophiles, 6, 217, 2002.
5. Oren, A., Bioenergetic aspects of halophilism, Microbiol. Mol. Biol. Rev., 63, 334, 1999.
6. Brown, A.D., Microbial water stress, Bacteriol. Rev., 40, 803, 1976.
7. Poolman, B. and Glaasker, E., Regulation of compatible solute accumulation in bacteria, Mol. Microbiol., 29, 397, 1998.
8. Reed, R.H. et al., Organic solute accumulation in osmotically stressed cyanobacteria, FEMS Microbiol. Lett., 39, 51, 1986.
9. Klähn, S. et al., Glucosylglycerate: A secondary compatible solute common to marine cyanobacteria from nitrogen-poor environments, Environ. Microbiol., 12, 83, 2010.
10. Fulda, S. et al., Analysis of stress responses in the cyanobacterial strains Synechococcus sp. PCC 7942, Synechocystis sp. PCC 6803, and Synechococcus sp. PCC 7418: Osmolyte accumulation and stress pro¬teins synthesis, J. Plant Physiol., 154, 240, 1999.
11. MacKay, M.A., Norton, R., and Borowitzka, L.J., Organic osmoregulatory solutes in cyanobacteria, J. Gen. Microbiol., 130, 2177, 1984.
12. Singh, A.K. et al., Evidence for a role of l-proline as a salinity protectant in the cyanobacterium Nostoc muscorum, Plant Cell Environ., 19, 490, 1996.
13. Hagemann, M. and Marin, K., Salt-induced sucrose accumulation is mediated by sucrose-phosphate-synthase in cyanobacteria, J. Plant Physiol., 155, 424, 1999.
14. Curatti, L. et al., Sucrose-phosphatesynthase from Synechocystis sp. Strain PCC 6803: Identification of the spsA gene and characterization of the enzyme expressed in Escherichia coli, J. Bacteriol., 180, 6776, 1998.
15. Porchia, A.C., Curatti, L., and Salerno, G.L., Sucrose metabolism in cyanobacteria: Sucrose synthase from Anabaena sp. strain PCC 7119 is remarkably different from the plant enzymes with respect to sub¬strate affinity and amino-terminal sequence, Planta, 210, 234, 1999.
16. Hagemann, M. et al., The stpA gene form Synechocystis sp. strain PCC 6803 encodes the glucosylglyc¬erol-phosphate phosphatase involved in cyanobacterial osmotic response to salt shock, J. Bacteriol., 179, 1727, 1997.
17. Marin, K. et al., The ggpS gene from Synechocystis sp. strain PCC 6803 encoding glucosyl-glycerol-phosphate synthase is involved in osmolyte synthesis, J. Bacteriol., 180, 4843, 1998.
18. Engelbrecht, F., Marin, K., and Hagemann, M., Expression of the ggpS gene, involved in osmolyte syn¬thesis in the marine cyanobacterium Synechococcus sp. strain PCC 7002, revealed regulatory differ¬ences between this strain and the freshwater strain Synechocystis sp. strain PCC 6803, Appl. Environ. Microbiol., 65, 4822, 1999.
19. Higo, A. et al., The role of a gene cluster for trehalose metabolism in dehydration tolerance of the fila¬mentous cyanobacterium Anabaena sp. PCC 7120, Microbiology, 152, 979, 2006.
20. Sakamoto, T. et al., Accumulation of trehalose in response to desiccation and salt stress in the terrestrial cyanobacterium Nostoc commune, Phycol. Res., 57, 66, 2009.
21. Wang, H.L., Postier, B.L., and Burnap, R.L., Polymerase chain reaction-based mutageneses identify key transporters belonging to multigene families involved in Na+ and pH homeostasis of Synechocystis sp. PCC 6803, Mol. Microbiol., 44, 1493, 2002.
22. Elanskaya, I.V. et al., Functional analysis of the Na+/H+ antiporter encoding genes of the cyanobacterium Synechocystis PCC 6803, Biochemistry (Moscow), 67432, 2002.
23. Billini, M., Stamatakis, K., and Sophianopoulou, V., Two members of a network of putative Na+/H+ anti¬porters are involved in salt and pH tolerance of the freshwater cyanobacterium Synechococcus elongates, J. Bacteriol., 190, 6318, 2008.
24. Blanco-Rivero, A. et al., mrpA, a gene with roles in resistance to Na+ and adaptation to alkaline pH in the cyanobacterium Anabaena sp. PCC 7120, Microbiology, 151, 1671, 2005.
25. Fukaya, F. et al., An Mrp-like cluster in the halotolerant cyanobacterium Aphanothece halophytica func¬tions as a Na+/H+ antiporter, Appl. Environ. Microbiol., 75, 6626, 2009.
26. Sutherland, D. et al., Osmotic regulation of transcription: Induction of the proU betaine transport system is dependent on accumulation of intracellular potassium, J. Bacteriol., 168, 805, 1986.
27. Booth, I.R. and Higgins, C.F., Enteric bacteria and osmotic stress: Intracellular potassium glutamate as a secondary signal of osmotic stress, FEMS Microbiol. Rev., 75, 239, 1990.
28. Shibata, M. et al., Genes essential to sodium-dependent bicarbonate transport in cyanobacteria: Function and phylogenetic analysis, J. Biol. Chem., 277, 18658, 2002.
29. Berry, S. et al., Potassium uptake in the unicellular cyanobacterium Synechocystis sp. strain PCC 6803 mainly depends on a Ktr-like system encoded by slr1509 (ntpJ), FEBS Lett., 548, 53, 2003.
30. Ballal, A., Basu, B., and Apte, S.K., The Kdp-ATPase system and its regulation, J. Biosci., 32, 559, 2007.
31. Katoh, H., Asthana, R.K., and Ohmori, M., Gene expression in the cyanobacterium Anabaena sp. PCC7120 under desiccation, Microb. Ecol., 47, 164, 2004.
32. Jeanjean, R. et al., Mutants of the cyanobacterium Synechocystis PCC 6803 impaired in respiration and unable to tolerate high salt concentrations, FEMS Microbiol. Lett., 68, 125, 1990.
33. Hagemann, M. and Zuther, E., Selection and characterization of mutants of the cyanobacterium Synechocystis sp. PCC 6803 unable to tolerate high salt concentrations, Arch. Microbiol., 158, 429, 1992.
34. Karandashova, I. et al., Identification of genes essential for growth at high salt concentrations using salt-sensitive mutants of the cyanobacterium Synechocystis sp. PCC 6803, Curr. Microbiol., 44, 184, 2002.
35. Zuther, E., Schubert, H., and Hagemann, M., Mutation of a gene encoding a putative glycoprotease leads to reduced salt tolerance, altered pigmentation, and cyanophycin accumulation in the cyanobacterium Synechocystis sp. strain PCC 6803, J. Bacteriol., 180, 1715, 1998.
36. Asadulghani et al., Comparative analysis of the hspA mutant and wild-type Synechocystis sp. strain PCC 6803 under salt stress: Evaluation of the role of hspA in salt-stress management, Arch. Microbiol., 182, 487, 2004.
37. Nakamura, T. et al., A cyanobacterial non-coding RNA, Yfr1, is required for growth under multiple stress conditions, Plant Cell Physiol., 48, 1309, 2007.
38. Kanesaki, Y. et al., Salt stress and hyperosmotic stress regulate the expression of different sets of genes in Synechocystis sp. PCC 6803, Biochem. Biophys. Res. Commun., 290, 339, 2007.
39. Marin, K. et al., Identification of histidine kinases that act as sensors in the perception of salt stress in Synechocystis sp. PCC 6803, Proc. Natl. Acad. Sci. U.S.A., 100, 9061, 2003.
40. Marin, K. et al., Gene expression profiling reflects physiological processes in salt acclimation of Synechocystis sp. strain PCC 6803, Plant Physiol., 136, 3290, 2004.
41. Fulda, S. et al., Proteomics of Synechocystis sp. strain PCC 6803. Identification of periplasmic proteins in cells, grown at low and high salt concentrations, Eur. J. Biochem., 267, 5900, 2000.
42. Fulda, S. et al., Proteome analysis of salt stress response in the cyanobacterium Synechocystis sp. strain PCC 6803, Proteomics, 6, 2733, 2006.
43. Ludwig, M. and Bryant, D.A., Transcription profiling of the model cyanobacterium Synechococcus sp. strain PCC 7002 by Next-Gen (SOLiD™) sequencing of cDNA, Front. Microbiol., 2, e41, 2011.
44. Hagemann, M. et al., unpublished data.
45. Waditee, R. et al., Overexpression of a Na+/H+ antiporter confers salt tolerance on a freshwater cyanobac¬terium, making it capable of growth in sea water, Proc. Natl. Acad. Sci. U.S.A., 99, 4109, 2002.
46. Waditee, R. et al., Genes for direct methylation of glycine provide high levels of glycinebetaine and abi¬otic-stress tolerance in Synechococcus and Arabidopsis, Proc. Natl. Acad. Sci. U.S.A., 102, 1318, 2005.
47. Deshnium, P. et al., Transformation of Synechococcus with a gene for choline oxidase enhances tolerance to salt stress, Plant Mol. Biol., 29, 897, 1995.
48. Nomura, M. et al., Synechococcus sp. PCC 7942 transformed with Escherichia coli bet genes produces glycine betaine from choline and acquires resistance to salt stress, Plant Physiol., 107, 703, 1995.
49. Soontharapirakkul, K. et al., Halotolerant cyanobacterium Aphanothece halophytica contains an Na+-dependent F1F0-ATPsynthase with a potential role in salt-stress tolerance, J. Biol. Chem., 286, 10169, 2011.
50. Klähn, S. et al., Expression of the ggpPS gene for glucosylglycerol biosynthesis from Azotobacter vine¬landii improves the salt tolerance of Arabidopsis thaliana, J. Exp. Bot., 60, 1679, 2009.
51. Reed, R.H. et al., Multiphasic osmotic adjustment in a euryhaline cyanobacterium, FEMS Microbiol. Lett., 28, 225, 1985.
52. Matsuda, N. et al., Na+-dependent K+ uptake Ktr system from the cyanobacterium Synechocystis sp. PCC 6803 and its role in the early phases of cell adaptation to hyperosmotic shock, J. Biol. Chem., 279, 54952, 2004.
53. Blumwald, E., Mehlhorn, R.J., and Packer, L., Studies of osmoregulation in salt adaptation of cyanobac¬teria with ESR spin-probe techniques, Proc. Natl. Acad. Sci. U.S.A., 80, 2599, 1983.
54. Hagemann, M., Fulda, S., and Schubert, H., DNA, RNA, and protein synthesis in the cyanobacterium Synechocystis sp. PCC 6803 adapted to different salt concentrations, Curr. Microbiol., 28, 201, 1994.
55. Miller, D.M. et al., Ion metabolism in a halophilic blue green alga Aphanothece halophytica, Arch. Microbiol., 111, 145, 1976.
56. Reed, R.H. and Stewart, W.D.P., Osmotic adjustment and organic solute accumulation in unicellular cyanobacteria from freshwater and marine habitats, Mar. Biol., 88, 1, 1985.
57. Stock, A.M., Robinson, V.L., and Goudreau, P.N., Two-component signal transduction, Annu. Rev. Biochem., 69, 183, 2000.
58. Aguilar, P.S. et al., Molecular basis of thermosensing: A two-component signal transduction thermometer in Bacillus subtilis, EMBO J., 20, 1681, 2001.
59. Wood, J.M., Osmosensing by bacteria: Signals and membrane-based sensors, Microbiol. Mol. Biol. Rev., 63, 230, 1999.
60. Suzuki, I. et al., The pathway for perception and transduction of low-temperature signals in Synechocystis, EMBO J., 19, 1327, 2000.
61. Shoumskaya, M.A. et al., 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, 2005.
62. Murata, N. and Suzuki, I., Exploitation of genomic sequences in a systematic analysis to access how cyanobacteria sense environmental stress, J. Exp. Bot., 57, 235, 2006.
63. Los, D.A. et al., Stress responses in Synechocystis: Regulated genes and regulatory systems, in The Cyanobacteria-Molecular Biology, Genomics and Evolution, Herrero, A. and Flores E., Eds., Caister Academic Press., Norfolk, U.K., 2008, p. 117.
64. Mikami, K. et al., The histidine kinase Hik33 perceives osmotic stress and cold stress in Synechocystis sp. PCC 6803, Mol. Microbiol., 46, 905, 2002.
65. Los, D.A. et al., Stress sensors and signal transducers in cyanobacteria, Sensors, 10, 2386, 2010.
66. Sakayori, T., Shiraiwa, Y., and Suzuki, I., A Synechocystis homolog of SipA protein, Ssl3451, enhances the activity of the histidine kinase Hik33, Plant Cell Physiol., 50, 1439, 2009.
67. Imamura, S. and Asayama, M., Sigma factors for cyanobacterial transcription, Gene Regul. Syst. Biol., 2009, 65, 2009.
68. Gruber, T.M. and Gross, C.A., Multiple sigma subunits and the partitioning of bacterial transcription space, Annu. Rev. Microbiol., 57, 441, 2003.
69. Hecker, M., Pané-Farré, J., and Völker, U., SigB-dependent general stress response in Bacillus subtilis and related Gram-positive bacteria, Annu. Rev. Microbiol., 61, 215, 2007.
70. Hengge-Aronis, R., Back to log phase: Sigma S as a global regulator in the osmotic control of gene expression in Escherichia coli, Mol. Microbiol., 21, 887, 1996.
71. Kanesaki, Y. et al., Histidine kinases play important roles in the perception and signal transduction of hydrogen peroxide in the cyanobacterium, Synechocystis sp. PCC6803, Plant J., 49, 313, 2007.
72. Pollari, M. et al., Characterization of single and double in activation strains reveals new physiological roles for group 2 sigma factors in the cyanobacterium Synechocystis sp. PCC6803, Plant Physiol., 147, 1994, 2008.
73. Huckauf, J. et al., Stress responses of Synechocystis sp. strain PCC 6803 mutants impaired in genes encoding putative alternative sigma factors, Microbiology, 146, 2877, 2000.
74. Marin, K. et al., Salt-dependent expression of glucosylglycerol-phosphate synthase, involved in osmolyte synthesis in the cyanobacterium Synechocystis sp. strain PCC 6803, J. Bacteriol., 184, 2870, 2002.
75. Imamura, S. et al., Purification, characterization, and gene expression of all sigma factors of RNA poly¬merase in a cyanobacterium, J. Mol. Biol., 325, 857, 2003.
76. Mitschke, J. et al., An experimentally anchored map of transcriptional start sites in the model cyanobac¬terium Synechocystis sp. PCC 6803, Proc. Natl. Acad. Sci. U.S.A., 108, 2124, 2011.
77. Vinnemeier, J. and Hagemann, M., Identification of salt-regulated genes in the genome of the cyanobac¬terium Synechocystis sp. strain PCC 6803 by subtractive RNA hybridization, Arch. Microbiol., 172, 377, 1999.
78. Klähn, S. et al., The gene ssl3076 encodes a protein mediating the salt-induced expression of ggpS for the biosynthesis of the compatible solute glucosylglycerol in Synechocystis sp. strain PCC 6803, J. Bacteriol., 192, 4403, 2010.
79. Georg, J. et al., Evidence for a major role of antisense RNAs in cyanobacterial gene regulation, Mol. Syst. Biol., 5, 305, 2009.
80. Blumwald, E., Mehlhorn, R.J., and Packer, L., Ionic osmoregulation during salt adaptation of the cyano¬bacterium Synechococcus 6311, Plant Physiol., 73, 377, 1983.
81. Shapiguzov, A. et al., Osmotic shrinkage of cells of Synechocystis sp. PCC 6803 by water efflux via aquaporins regulates osmostress-inducible gene expression, Microbiology, 151, 447, 2005.
82. Hagemann, M. et al., Biochemical characterization of glucosylglycerol-phosphate synthase of Synechocystis sp. strain PCC 6803: Comparison of crude, purified, and recombinant enzymes, Curr. Microbiol., 43, 278, 2002.
83. Novak, J.F., Stirnberg, M., and Marin, K., A novel mechanism of osmosensing: Salt dependent protein-DNA interaction in the cyanobacterium Synechocystis sp. PCC 6803, J. Biol. Chem., 286, 3235, 2011.
84. Gralla, J.D. and Vargas, D.R. Potassium glutamate as transcriptional inhibitor during bacterial osmoregu¬lation, EMBO J., 25, 1515, 2005.
85. Wang, J.C. and Lynch, A.S., Transcription and DNA supercoiling, Curr. Opin. Genet. Dev., 3, 764, 1993.
86. Higgins, C.F. et al., A physiological role for DNA supercoiling in the osmotic regulation of gene expres¬sion in S. typhimurium and E. coli, Cell, 52, 569, 1988.
87. Dorman, C.J., DNA supercoiling and bacterial gene expression, Sci. Prog., 89, 151, 2006.
88. Prakash, J.S. et al., DNA supercoiling regulates the stress inducible expression of genes in the cyanobac¬terium Synechocystis, Mol. Biosyst., 5, 1904, 2009.
89. Maxwell, A., DNA gyrase as a drug target, Biochem. Soc. Trans., 27, 48, 1999.
90. Lewis, R.J., Tsai, F.T.F., and Wigley, D.B., Molecular mechanisms of drug inhibition of DNA gyrase, Bioassays, 18, 661, 1996.