Salt acclimation of cyanobacteria and their application in biotechnology

Life

Volumn 5, Issue 1, 2015, Pages 25-49

  Pade, Nadin ^a   Hagemann, Martin ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

Compatible solute; Genome mining; Ion export; Regulation; Salt sensing

Indexed keywords

CYANOBACTERIA;

EID: 84922024536     PISSN: None     EISSN: 20751729     Source Type: Journal    
DOI: 10.3390/life5010025     Document Type: Review

References (137)

1. Tandeau de Marsac, N.T.; Houmard, J. Adaptation of cyanobacteria to environmental stimuli: New steps toward molecular mechanisms. FEMS Microbiol. Rev. 1993, 104, 119-190.
2. Oren, A. Salts and brines. In The Ecology of Cyanobacteria; Whitton, B.A., Potts, M., Eds.; Kluwer Academic Publishers: Dordrecht, the Netherlands, 2000; pp. 281-306.
3. Ladas, N.P.; Papageorigou, G.C. Cell turgor: A critical factor for the proliferation of cyanobacteria at unfavorable salinity. Photosynth Res. 2000, 65, 155-164.
4. Galinski, E.A.; Trüper, H.G. Microbial behaviour in salt-stressed ecosystems. FEMS Microbiol. Rev. 1994, 15, 95-108.
5. Hagemann, M. Molecular biology of cyanobacterial salt acclimation. FEMS Microbiol. Rev. 2011, 35, 87-123.
6. 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., Schleifer, K.-H., Eds.; Springer: New York, NY, USA, 1993; pp. 1983-1900.
7. Oren, A.; Mana, L. Amino acid composition of bulk protein and salt relationships of selected enzymes of Salinibacter ruber, an extremely halophilic bacterium. Extremophiles 2002, 6, 217-223.
8. Oren, A. Bioenergetic aspects of halophilism. Microbiol. Mol. Biol. Rev. 1999, 63, 334-348.
9. Müller, V.; Oren, A. Metabolism of chloride in halophilic prokaryotes. Extremophiles 2003, 7, 261-266.
10. Brown, A.D. Microbial water stress. Bacteriol. Rev. 1976, 40, 803-846.
11. Bremer, E.; Krämer, R. Coping with osmotic challenges: osmoregulation through accumulation and release of compatible solute in bacteria. In Bacterial Stress Responses; Hengge-Aronis, R., Ed.; ASM Press: Washington, DC, USA, 2000; pp. 79-96.
12. Wood, J. Bacterial osmoregulation: a paradigm for the study of cellular homeostasis. Annu. Rev. Microbiol. 2011, 65, 215-238.
13. Krämer, R. Bacterial stimulus perception and signal transduction: Response to osmotic stress. Chem. Rec. 2010, 10, 217-229.
14. Kempf, B.; Bremer, E. Uptake and synthsis of compatible solutes as microbial stress response to high-osmolality environment. Arch. Microbiol. 1998, 170, 319-330.
15. Potts, M. Desiccation tolerance of prokaryotes. Microbiol. Rev. 1994, 58, 755-805.
16. Klähn, S.; Hagemann, M. Compatible solute biosynthesis in cyanobacteria. Environ. Microbiol. 2011, 13, 551-562.
17. Hagemann, M. Genomics of salt acclimation: synthesis of compatible solutes among cyanobacteria. In Genomics of Cyanobacteria; Chauvat, F., Cassier-Chauvat, C., Eds.; Academic Press: Waltham, MA, USA, 2013; Volum 65, pp. 27-55.
18. Pade, N.; Hagemann, M. Cyanobacterial salt stress acclimation: genetic manipulation and regulation. In Stress Biology of Cyanobacteria: Molecular Mechanisms to Cellular Responses; Srivastava, A.K.; Rai, A.N.; Neilan, B.A., Eds.; CRC Press: London, UK, 2013; pp 189-202.
19. Arakawa, T.; Timasheff, S.N. The stabilization of proteins by osmolytes. Biophys. J. 1985, 47, 411-414.
20. Wood, J.M. Osmosensing by bacteria: Signals and membrane-based sensors. Micobiol. Mol. Biol. Rev. 1999, 63, 230-262.
21. Poolman, B.; Glaasker, E. Regulation of compatible solute accumulation in bacteria. Mol. Microbiol. 1998, 29, 397-407.
22. Reed, R.H.; Borowitzka, L.J.; Mackay, M.A.; Chudek, J.A.; Foster, R.; Warr, S.R.C.; Moore, D.J.; Stewart, W.D.P. Organic solute accumulation in osmotically stressed cyanobacteria. FEMS Microbiol. Lett. 1986, 39, 51-56.
23. Mackay, M.A.; Norton, R.S.; Borowitzka, L.J. Organic osmoregulatory solutes in cyanobacteria. J. Gen. Microbiol. 1984, 130, 2177-2191.
24. Singh, A.K.; Chakarvathy, D.; Singh, T.P.K.; Singh, H.N. Evidence for a role for L-proline as a salinity protectant in the cyanobacterium Nostoc muscorum. Plant Cell Environ. 1996, 19, 490-494.
25. Fulda, S.; Huckauf, J.; Schoor, A.; Hagemann, M. 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 proteins synthesis. J. Plant Physiol. 1999, 154, 240-249.
26. Klähn, S.; Steglich, C.; Hess, W.R.; Hagemann, M. Glucosylglycerate: A secondary compatible solute common to marine cyanobacteria from nitrogen-poor environments. Environ. Microbiol. 2010, 12, 83-94.
27. Shih, P.M.; Wu, D.; Latifi, A.; Axen, S.D.; Fewer, D.P.; Talla, E.; Calteau, A.; Cai, F.; Tandeau de Marsac, N.; Rippka, R.; et al. Improving the coverage of the cyanobacterial phylum using diversity-driven genome sequencing. Proc. Natl. Acad. Sci. USA 2013, 110, 1053-1058.
28. 2-fixing taxon Crocosphaera watsonii. ISME J 2009, 3, 618-631.
29. Pade, N.; Compaore, J.; Klähn, S.; Stal, L.J.; Hagemann, M. The marine cyanobacterium Crocosphaera watsonii WH8501 synthesizes the compatible solute trehalose by a laterally acquired OtsAB fusion protein. Environ. Microbiol. 2012, 14, 1261-1271.
30. Bergman, B.; Sandh, G.; Lin, S.; Larsson, J.; Carpenter, E.J. Trichodesmium-a widespread marine cyanobacterium with unusual nitrogen fixation properties. FEMS Microbiol. Rev. 2013, 37, 286-302.
31. Salerno, G.L.; Porchia, A.C.; Vargas, W.A.; Abdian, P.L. Fructose-containing oligosaccharides: Novel compatible solutes in Anabaena cells exposed to salt stress. Plant Sci. 2004, 167, 1003-1008.
32. Fischer, D.; Geyer, A.; Loos, E. Occurrence of glucosylsucrose [α-D-glucopyranosyl-(1→2)-α-D-glucopyranosyl-(1→2)-β-D-fructofuranoside] and glucosylated homologues in cyanobacteria: Structural properties, cellular contents and possible function as thermoprotectants. FEBS J. 2006, 273, 137-149.
33. Goh, F.; Barrow, K.D.; Burns, B.P.; Neilan, B.A. Identification and regulation of novel compatible solutes from hypersaline stromatolite-associated cyanobacteria. Arch. Microbiol. 2010, 192, 1031-1038.
34. Borges, N.; Ramos, A.; Raven, N.D.H.; Sharp, R.J.; Santos, H. Comparative study of the thermostabilizing properties of mannosylglycerate and other compatible solutes on model enzymes. Extremophiles 2002, 6, 209-216.
35. Hincha, D.K.; Hagemann, M. Stabilization of model membranes during drying by compatible solutes involved in the stress tolerance of plants and microorganisms. Biochem. J. 2004, 383, 277-283.
36. Kandror, O.; DeLeon, A.; Goldberg, A.L. Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. Proc. Natl. Acad. Sci. USA 2002, 99, 9727-9732.
37. Jang, I.C.; Oh, S.J.; Seo, J.S.; Choi, W.B.; Song, S.I.; Kim, C.H.; Kim, Y.S.; Seo, H.S.; Choi, Y.D.; Nahm, B.H.; et al. Expression of a bifunctional fusion of the Escherichia coli genes for trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase in transgenic rice plants increases trehalose accumulation and abiotic stress tolerance without stunting growth. Plant Physiol. 2003, 131, 516-524.
38. Diamant, S.; Rosenthal, D.; Azem, A.; Eliahu, N.; Ben-Zvi, A.P.; Goloubinoff, P. Dicarboxylic amino acids and glycine-betaine regulate chaperone-mediated protein-disaggregation under stress. Mol. Microbiol. 2003, 49, 401-410.
39. Sawangwan, T.; Goedl, C.; Nidetzky, B. Glucosylglycerol and glucosylglycerate as enzyme stabilizers. Biotechnol. J. 2010, 5, 187-191.
40. Luley-Goedel, C.; Nidetzky, B. Glycosides as compatible solutes: biosynthesis and applications. Nat. Prod. Rep. 2011, 28, 875-896.
41. Hagemann, M.; Erdmann, N. Activation and pathway of glucosylglycerol biosynthesis in the cyanobacterium Synechocystis sp. PCC 6803. Microbiology 1994, 140, 1427-1431.
42. Hagemann, M.; Schoor, A.; Jeanjean, R.; Zuther, E.; Joset, F. The stpA gene form Synechocystis sp. strain PCC 6803 encodes the glucosylglycerol-phosphate phosphatase involved in cyanobacterial osmotic response to salt shock. J. Bacteriol. 1997, 179, 1727-1733.
43. Marin, K.; Zuther, E.; Kerstan, T.; Kunert, A.; Hagemann, M. The ggpS gene from Synechocystis sp. strain PCC 6803 encoding glucosylglycerol-phosphate synthase is involved in osmolyte synthesis. J. Bacteriol. 1998, 180, 4843-4849.
44. Porchia, A.C.; Salerno, G.L. Sucrose biosynthesis in a prokaryotic organism: Presence of two sucrose-phosphate synthases in Anabaena with remarkable differences compared with the plant enzymes. Proc. Natl. Acad. Sci. USA 1996, 93, 13600-13604.
45. Higo, A.; Katoh, H.; Ohmori, K.; Ikeuchi, M.; Ohmori, M. The role of a gene cluster for trehalose metabolism in dehydration tolerance of the filamentous cyanobacterium Anabaena sp. PCC 7120. Microbiology 2006, 152, 979-987.
46. Waditee, R.; Tanaka, Y.; Aoki, K.; Hibino, T.; Jikuya, H.; Takabe, T.; Takabe, T. Isolation and functional characterization of N-methyltransferase that catalyze betaine synthesis from glycine in a halotolerant photosynthetic organism Aphanothece halophytica. J. Biol. Chem. 2003, 278, 4932-4942.
47. Martínez-Noël, G.M.; Cumino, A.C.; Kolman M.A.; Salerno, G.L. First evidence of sucrose biosynthesis by single cyanobacterial bimodular proteins. FEBS Lett. 2013, 587, 1669-1674.
48. Kolman, M.A.; Torres, L.L.; Martin, M.L.; Salerno, G.L. Sucrose synthase in unicellular cyanobacteria and its relationship with salt and hypoxic stress. Planta 2011, 235, 955-964.
49. Azua-Bustos, A.; Zúñiga, J.; Arenas-Fajardo, C.; Orellana, M.; Salas, L.; Rafael, V. Gloeocapsopsis AAB1, an extremely desiccation-tolerant cyanobacterium isolated from the Atacama Desert. Extremophiles 2014, 18, 61-74.
50. Yoshikawa, T.; Ikeda, Y.; Sakata, T.; Maeda, H. Cloning and analysis of the ggpS gene from Cyanobacteria Arthrospira spp. involved in the synthesis of an osmolyte glucosylglycerol. Biocontrol. Sci. 2011, 16, 55-61.
51. Kothari, A.; Vaughn, M.; Garcia-Pichel, F. Comparative genomic analyses of the cyanobacterium, Lyngbya aestuarii BL J, a powerful hydrogen producer. Front. Microbiol. 2013, 4, doi:10.3389/ fmicb.2013.00363.
52. Mao, X.; Olman, V.; Stuart, R.; Paulsen, I.T.; Palenik, B.; Xu, Y. Computational prediction of the osmoregulation network in Synechococcus sp. WH8102. BMC Genomics 2010, 11, doi:10.1186/1471-2164-11-291.
53. Csonka, L.N.; Hanson, A.D. Prokaryotic osmoregulation: genetics and physiology. Annu. Rev. Microbiol. 1991, 45, 569-606.
54. Ziegler, C.; Bremer, E.; Krämer, R. The BCCT family of carriers: from physiology to crystal structure. Mol. Microbiol. 2010, 78, 13-34.
55. Pittelkow, M.; Bremer, E. Cellular adjustment of Bacillus subtilis and other bacilli to fluctuating salinities. In Halophiles and Hypersaline Environments: Current Research and Future Trends, Ventosa, A., Ohren, A., Ma, Y., Eds.; Springer: Berlin, Germany, 2011; pp. 275-302.
56. Lucht, J.M.; Bremer, E. Adaptation of Escherichia coli to high osmolarity environments: Osmoregulation of the high-affinity glycine betaine transport system ProU. FEMS Microbiol. Rev. 1995, 14, 3-20.
57. Moore, D.J.; Reed, R.H.; Stewart, W.D.P. A glycine betaine transport system in Aphanothece halophytica and other glycine betaine-synthesizing cyanobacteria. Arch. Microbiol. 1987, 147, 399-405.
58. Laloknam, S.; Tanaka, K.; Buaboocha, T.; Waditee, R.; Incharoensakdi, A.; Hibino, T.; Tanaka, Y.; Takabe, T. Halotolerant cyanobacterium Aphanothece halophytica contains a betaine transporter active at alkaline pH and high salinity. Appl. Environ. Microbiol. 2006, 72, 6018-6026.
59. Mikkat, S.; Hagemann, M.; Schoor, A. Active transport of glucosylglycerol is involved in salt adaptation of the cyanobacterium Synechocystis sp. PCC 6803. Arch. Microbiol. 1996, 142, 1725-1732.
60. Mikkat, S.; Effmert, U.; Hagemann, M. Uptake and use of the osmoprotective compounds trehalose, glucosylglycerol, and sucrose by the cyanobacterium Synechocystis sp. PCC6803. Arch. Microbiol. 1997, 167, 112-118.
61. Hagemann, M.; Richter, S.; Mikkat, S. The ggtA gene encodes a subunit of the transport system for the osmoprotective compound glucosylglycerol in Synechocystis sp. strain PCC 6803. J. Bacteriol. 1997, 179, 714-720.
62. Mikkat, S.; Hagemann, M. Molecular analysis of the ggtBCD gene cluster of Synechocystis sp. Strain PCC6803 encoding subunits of an ABC transporter for osmoprotective compounds. Arch. Microbiol 2000, 174, 273-282.
63. Kopf, M.; Klähn, S.; Pade, N.; Weingärtner, C.; Hagemann, M.; Voß, B.; Hess, W.R. Comparative genome analysis of the closely related Synechocystis strains PCC 6714 and PCC 6803. DNA Res. 2014, 21, 255-266.
64. Ferjani, A.; Mustardy, L.; Sulpice, R.; Marin, K.; Suzuki, I.; Hagemann, M.; Murata, N. Glucosylglycerol, a compatible solute, sustains cell division under salt stress. Plant Physiol. 2003, 131, 1628-1637.
65. Horn, C.; Jenewein, S.; Sohn-Bösser, L.; Bremer, E.; Schmitt, L. Biochemical and structural analysis of the Bacillus subtilis ABC transporter OpuA and its isolated subunits. J. Mol. Microbiol. Biotechnol. 2005, 10, 76-91.
66. Ducat, D.C.; Avelar-Rivas, J.A.; Way, J.C.; Silver, P.A. Rerouting carbon flux to enhance photosynthetic productivity. Appl. Environ. Microbiol. 2012, 78, 2660-2668.
67. Roder, A.; Hoffmann, E.; Hagemann, M.; Berg, G. Synthesis of the compatible solutes glucosylglycerol and trehalose by salt-stressed cells of Stenotrophomonas strains. FEMS Microbiol. Lett. 2005, 243, 219-226.
68. Alavi, P.; Starcher, M.R.; Zachow, C.; Müller, H.; Berg, G. Root-microbe systems: The effect and mode of interaction of stress protecting agent (SPA) Stenotrophomonas rhizophila DSM14405T. Front. Plant Sci. 2013, 4, doi:10.3389/fpls.2013.00141.
69. Reed, R.H.; Warr, S.R.C.; Richardson, D.L.; Moore, D.J.; Stewart, W.D.P. Multiphasic osmotic adjustment in a euryhaline cyanobacterium. FEMS Microbiol. Lett. 1985, 28, 225-229.
70. Marin, K.; Kanesaki, Y.; Los, D.A.; Murata, N.; Suzuki, I.; Hagemann, M. Gene expression profiling reflects physiological processes in salt acclimation of Synechocystis sp. Strain PCC 6803. Plant Physiol. 2004, 136, 3290-3300.
71. Blumwald, E.; Mehlhorn, R.J.; Packer, L. Studies of osmoregulation in salt adaptation of cyanobacteria with ESR spin-probe techniques. Proc. Natl. Acad. Sci. USA 1983, 80, 2599-2602.
72. Shapiguzov, A.; Lyukevich, A.A.; Allakhverdiev, S.I.; Sergeyenko, T.V.; Suzuki, I.; Murata, N.; Los, D.A. Osmotic shrinkage of cells of Synechocystis sp. PCC 6803 by water efflux via aquaporins regulates osmostress-inducible gene expression. Microbiology 2005, 151, 447-455.
73. + 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. 2004, 279, 54952-54962.
74. Nanatani, K.; Shijuku, T.; Takano, Y.; Zulkifli, L.; Yamazaki, T.; Tominaga, A.; Souma, S.; Onai, K.; Morishita, M.; Ishiura, M.; et al. Comparative analysis of kdp and ktr mutants reveals distinct doles of the potassium transporters in the model cyanobacterium Synechocystis sp. PCC 6803. J. Bacteriol. 2014, doi:10.1128/JB.02276-14.
75. Schubert, H.; Fulda, S.; Hagemann, M. Effects of adaptation to different salt concentrations on photosynthesis and pigmentation of the cyanobacterium Synechocystis sp. PCC 6803. J. Plant Physiol. 1993, 142, 291-295.
76. Hagemann, M.; Fulda, S.; Schubert, H. DNA, RNA and protein synthesis in the cyanobacterium Synechocystis sp. PCC 6803 adapted to different salt concentrations. Curr. Microbiol. 1994, 28, 201-207.
77. + antiporter encoding genes of the cyanobacterium Synechocystis PCC 6803. Biochemistry (Moscow) 2002, 67, 432-440.
78. + and pH homeostasis of Synechocystis sp. PCC 6803. Mol. Microbiol. 2002, 44, 1493-1506.
79. + antiporter Nhas3 from the thylakoid membrane of Synechocystis sp. PCC 6803. J. Biol. Chem. 2009, 284, 16513-16521.
80. + and adaptation to alkaline pH in the cyanobacterium Anabaena sp. PCC7120. Microbiology 2005, 151, 1671-1682.
81. + antiporter. Appl. Environ. Microbiol. 2009, 75, 6626-6629.
82. +-dependent F1F0-ATP synthase with a potential role in salt-stress tolerance. J. Biol. Chem. 2011, 286, 10169-10176.
83. + antiporter from a cyanobacterium. Biochemistry 2011, 50, 788-794.
84. Berry, S.; Esper, B.; Karandashova, I.; Teuber, M.; Elanskaya, I.; Rögner, M.; Hagemann, M. Potassium uptake in the unicellular cyanobacterium Synechocystis sp. strain PCC 6803 mainly depends on a Ktr-like system encoded by slr1509 (ntpJ). FEBS Lett. 2003, 548, 53-58.
85. Ballal, A.; Basu, B.; Apte, S.K. The Kdp-ATPase system and its regulation. J. Biosci. 2007, 32, 559-568.
86. Katoh, H.; Asthana, R.K.; Ohmori, M. Gene expression in the cyanobacterium Anabaena sp. PCC7120 under desiccation. Microb. Ecol. 2004, 47, 164-174.
87. Kanesaki, Y.; Suzuki, I.; Allakhverdiev, S.I.; Mikami, K.; Murata, N. Salt stress and hyperosmotic stress regulate the expression of different sets of genes in Synechocystis sp. PCC 6803. Biochem. Biophys. Res. Commun. 2002, 290, 339-348.
88. Marin, K.; Suzuki, I.; Yamaguchi, K.; Ribbeck, K.; Yamamoto, H.; Kanesaki, Y.; Hagemann, M.; Murata, N. Identification of histidine kinases that act as sensors in the perception of salt stress in Synechocystis sp. PCC 6803. Proc. Natl. Acad. Sci. USA 2003, 100, 9061-9066.
89. Mitschke, J.; Georg, J.; Scholz, I.; Sharma, C.M.; Dienst, D.; Bantscheff, J.; Voss, B.; Steglich, C.; Wilde, A.; Vogel, J.; Hess, W.R. An experimentally anchored map of transcriptional start sites in the model cyanobacterium Synechocystis sp. PCC6803. Proc. Natl Acad Sci USA 2011, 108, 2124-2129.
90. Ludwig, M.; Bryant, D.A. Synechococcus sp. strain PCC 7002 transcriptome: acclimation to temperature, salinity, oxidative stress, and mixotrophic growth conditions. Front. Microbiol. 2012, 3, doi:10.3389/fmicb.2012.00354.
91. Schubert, H.; Hagemann, M. Salt effect on 77 K fluorescence and photosynthesis in the cyanobacterium Synechocystis spec. PCC 6803. FEMS Microbiol. Lett. 1990, 71, 169-172.
92. Qiao, J.; Huang, S.; Te, R.; Wang, J.; Chen, L.; Zhang, W. Integrated proteomic and transcriptomic analysis reveals novel genes and regulatory mechanisms involved in salt stress responses in Synechocystis sp. PCC 6803. Appl. Microbiol. Biotechnol. 2013, 97, 8253-8264.
93. Billis, K.; Billini, M.; Tripp, H.J.; Kyrpides, N.C.; Mavromatis, K. Comparative transcriptomics between Synechococcus PCC 7942 and Synechocystis PCC 6803 provide insights into mechanisms of stress acclimation. PLoS One 2014, 9, e109738.
94. Fulda, S.; Huang, F.; Nilsson, F.; Hagemann, M.; Norling, B. Proteomics of Synechocystis sp. strain PCC 6803 identification of periplasmic proteins in cells grown at low and high salt concentrations. Eur. J. Biochem. 2000, 267, 5900-5907.
95. Huang, F.; Fulda, S.; Hagemann, M.; Norling, B. Proteomic screening of salt-stress-induced changes in plasma membranes of Synechocystis sp. strain PCC 6803. Proteomics 2006, 6, 910-920.
96. Fulda, S.; Mikkat, S.; Huang, F.; Huckauf, J.; Marin, K.; Norling, B.; Hagemann, M. Proteome analysis of salt stress response in the cyanobacterium Synechocystis sp. strain PCC 6803. Proteomics 2006, 6, 2733-2745.
97. Wang, H.; Yang, Y.; Chen, W.; Ding, L.; Li, P.; Zhao, X.; Wang, X.; Li, A.; Bao, Q. Identification of differentially expressed proteins of Arthrospira (Spirulina) platensis-YZ under salt-stress conditions by proteomics and qRT-PCR analysis. Proteome Sci. 2013, 11, doi:10.1186/1477-5956-11-6.
98. Qiao, J.; Shao, M.; Chen, L.; Wang, J.; Wu, G.; Tian, X.; Liu, J.; Huang, S.; Zhang, W. Systematic characterization of hypothetical proteins in Synechocystis sp. PCC 6803 reveals proteins functionally relevant to stress responses. Gene 2013, 512, 6-15.
99. Rai, S.; Agrawal, C.; Shrivastava, A.K.; Singh, P.K.; Rai, L.C. Comparative proteomics unveils cross species variations in Anabaena under salt stress. J. Proteomics 2014, 98, 254-270.
100. Rai, S.; Singh, S.; Shrivastava, A.K.; Rai, L.C. Salt and UV-B induced changes in Anabaena PCC 7120: Physiological, proteomic and bioinformatic perspectives. Photosynth. Res. 2013, 118, 105-114.
101. Poolman, B.; Spitzer, J.J.; Wood, J.M. Bacterial osmosensing: roles of membrane structure and electrostatics in lipid-protein and protein-protein interactions. Biochim. Biophys. Acta 2004, 1666, 88-104.
102. Novak, J.F.; Stirnberg, M.; Roenneke, B.; Marin, K. A novel mechanism of osmosensing, a salt-dependent protein-nucleic acid interaction in the cyanobacterium Synechocystis species PCC 6803. J. Biol Chem 2011, 286, 3235-3241.
103. Marin, K.; Huckauf, J.; Fulda, S.; Hagemann, M. Salt-dependent expression of glucosylglycerol-phosphate synthase, involved in osmolyte synthesis in the cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol. 2002, 184, 2870-2877.
104. Klähn, S.; Höhne, A.; Simon, E.; Hagemann, M. 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. 2010, 192, 4403-4412.
105. Gralla, J.D.; Vargas, D.R. Potassium glutamate as a transcriptional inhibitor during bacterial osmoregulation. EMBO J. 2006, 25, 1515-1521.
106. Nikkinen, H.L.; Hakkila, K.; Gunnelius, L.; Huokko, T.; Pollari, M.; Tyystjärvi, T. The SigB σ factor regulates multiple salt acclimation responses of the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol. 2012, 158, 514-523.
107. Pollari, M.; Gunnelius, L.; Tuominen, I.; Ruotsalainen, V.; Tyystjärvi, E.; Salminen, T.; Tyystjärvi, T. Characterization of single and double inactivation strains reveals new physiological roles for group 2 sigma factors in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol. 2008, 147, 1994-2005.
108. Tyystjärvi, T.; Huokko, T.; Rantamäki, S.; Tyystjärvi, E. Impact of different group 2 sigma factors on light use efficiency and high salt stress in the cyanobacterium Synechocystis sp. PCC 6803. PLoS One 2013, 8, e63020.
109. Shoumskaya, M.A.; Paithoonrangsarid, K.; Kanesaki, Y.; Los, D.A.; Zinchenko, V.V.; Tanticharoen, M.; Suzuki, I.; Murata, N. 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. 2005, 280, 21531-21538.
110. Li, T.; Yang, H.M.; Cui, S.X.; Suzuki, I.; Zhang, L.F.; Li, L.; Bo, T.T.; Wang, J.; Murata, N.; Huang, F. Proteomic study of the impact of Hik33 mutation in Synechocystis sp. PCC 6803 under normal and salt stress conditions. J. Proteome Res. 2012, 11, 502-514.
111. Schwartz, S.H.; Black, T.A.; Jäger, K.; Panoff, J.M.; Wolk, C.P. Regulation of an osmoticum-responsive gene in Anabaena sp. strain PCC 7120. J. Bacteriol. 1998, 180, 6332-6337.
112. Ehira, S.; Kimura, S.; Miyazaki, S.; Ohmori, M. Sucrose synthesis in the nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120 is controlled by the two-component response regulator OrrA. Appl. Environ. Microbiol. 2014, 80, 5672-5679.
113. Chen, L.; Wu, L.; Zhu, Y.; Song, Z.; Wang, J.; Zhang, W. An orphan two-component response regulator Slr1588 involves salt tolerance by directly regulating synthesis of compatible solutes in photosynthetic Synechocystis sp. PCC 6803. Mol. Biosyst. 2014, 10, 1765-1774.
114. Liang, C.; Zhang, X.; Chi, X.; Guan, X.; Li, Y.; Qin, S.; Shao, H.B. Serine/threonine protein kinase SpkG is a candidate for high salt resistance in the unicellular cyanobacterium Synechocystis sp. PCC 6803. PLoS One 2011, 6, e18718.
115. Wang, F.K.; Latifi, A.; Chen, W.L.; Zhang, C.C. The inositol monophosphatase All2917 (IMPA1) is involved in osmotic adaptation in Anabaena sp. PCC7120. Environ. Microbiol. Rep. 2012, 4, 622-632.
116. Algenol Biofuels. Available online: http://www.algenol.com/ (accessed on 23 December 2014).
117. Chisti, Y. Constraints to commercialization of algal fuels. J. Biotechnol. 2013, 167, 201-214.
118. Guschina; I.A.; Harwood, J.L. Lipids and lipid metabolism in eukaryotic algae. Prog. Lipid Res. 2006, 45, 160-186.
119. Hu, Q.; Sommerfeld, M.; Jarvis, E.; Ghirardi, M.; Posewitz, M.; Seibert, M.; Darzins, A. Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances. Plant J. 2008, 54, 621-639.
120. Singh, N.K.; Dhar, D.W. Microalgae as second generation biofuel. A review. Agron. Sustain. Dev. 2011, 31, 605-629.
121. Bernstein, H.C.; Konopka, A.; Melnicki, M.R.; Hill, E.A.; Kucek, L.A.; Zhang, S.; Shen, G.; Bryant, D.A.; Beliaev, A.S. Effect of mono- and dichromatic light quality on growth rates and photosynthetic performance of Synechococcus sp. PCC 7002. Front. Microbiol. 2014, 5, doi:10.3389/fmicb.2014.00488
122. Carrieri, D.; Momot, D.; Brasg, I.A.; Ananyev, G.; Lenz, O.; Bryant, D.A.; Dismukes, G.C. Boosting autofermentation rates and product yields with sodium stress cycling: application to production of renewable fuels by cyanobacteria. Appl. Environ. Microbiol. 2010, 76, 6455-6462.
123. Guerra, L.T.; Xu, Y.; Bennette, N.; McNeely, K.; Bryant, D.A.; Dismukes, G.C. Natural osmolytes are much less effective substrates than glycogen for catabolic energy production in the marine cyanobacterium Synechococcus sp. strain PCC 7002. J. Biotechnol. 2013, 166, 65-75.
124. bitop AG Extremolytes. Available online: http://www.bitop.de/cms/website.php?id=/en/index/ extremolyte.htm (accessed on 23 December 2014).
125. Kovacevic, V.; Wesseler, J. Cost-effectiveness analysis of algae energy production in the EU. Energy Policy 2010, 38, 5749-5757.
126. Du, W.; Liang, F.; Duan, Y.; Tan, X.; Lu, X. Exploring the photosynthetic production capacity of sucrose by cyanobacteria. Metab. Eng. 2013, 19, 17-25.
127. Reed, R.H.; Warr, S.R.C.; Kerby, N.W.; Stewart, W.D.P. Osmotic shock-induced release of low molecular weight metabolites from free-living and immobilized cyanobacteria. Enzyme Microb. Technol. 1986, 8, 101-104.
128. Fulda, S.; Hagemann, M.; Libbert, E. Release of glucosylglycerol from the cyanobacterium Synechocystis spec. SAG 92.79 by hypoosmotic shock. Arch. Microbiol. 1990, 153, 405-408.
129. Erdmann, N.; Zuther, E.; Abarzua, S. Comparative studies on the photoproduction of nonhydrogenous resources by cyanobacteria. Curr. Microbiol. 1992, 25, 83-88.
130. Takagi, M.; Karseno; Yoshida, T. Effect of salt concentration on intracellular accumulation of lipids and triacylglyceride in marine microalgae Dunaliella cells. J. Biosci. Bioeng. 2006, 101, 223-226.
131. Pal, D.; Khozin-Goldberg, I.; Cohen, Z.; Boussiba, S. The effect of light, salinity, and nitrogen availability on lipid production by Nannochloropsis sp. Appl. Microbiol. Biotechnol. 2011, 90, 1429-1441.
132. Waditee, R.; Bhuiyan, M.N.; Rai, V.; Aoki, K.; Tanaka, Y.; Hibino, T.; Suzuki, S.; Takano, J.; Jagendorf, A.T.; Takabe, T.; Takabe, T. Genes for direct methylation of glycine provide high levels of glycinebetaine and abiotic-stress tolerance in Synechococcus and Arabidopsis. Proc. Natl. Acad. Sci. USA 2005, 102, 1318-1323.
133. Klähn, S.; Marquardt, D.M.; Rollwitz, I.; Hagemann, M. Expression of the ggpPS gene for glucosylglycerol biosynthesis from Azotobacter vinelandii improves the salt tolerance of Arabidopsis thaliana. J. Exp. Bot. 2009, 60, 1679-1689.
134. Sievers, N.; Muders, K.; Henneberg, M.; Klähn, S.; Effmert, M.; Junghans, H.; Hagemann, M. Establishing glucosylglycerol synthesis in potato (Solanum tuberosum L. cv. Albatros) by expression of the ggpPS gene from Azotobacter vinelandii. J. Plant Sci. Mol. Breed. 2013, doi:10.7143/2050-2389-2-1.
135. Kaczmarzyk, D.; Anfelt, J.; Särnegrim, A.; Hudson, E.P. Overexpression of sigma factor SigB improves temperature and butanol tolerance of Synechocystis sp. PCC6803. J. Biotechnol. 2014, 182-183, 54-60.
136. Takeda, T.; Miyao, K.; Tamoi, M.; Kanaboshi, H.; Miyasaka, H.; Shigeoka, S. Molecular characterization of glutathione peroxidase-like protein in halotolerant Chlamydomonas sp. W80. Physiol. Plant. 2003, 117, 467-475.
137. Yoshimura, K.; Miyao, K.; Gaber, A.; Takeda, T.; Kanaboshi, H.; Miyasaka, H.; Shigeoka, S. Enhancement of stress tolerance in transgenic tobacco plants overexpressing Chlamydomonas glutathione peroxidase in chloroplasts or cytosol. Plant J. 2004, 37, 21-33.