1887

Abstract

Expression of the genes for trehalose synthesis ( and , encoding maltooligosyl trehalose synthase and hydrolase) and trehalose hydrolysis () in sp. PCC 7120 was up-regulated markedly upon dehydration. However, the amount of trehalose accumulated during dehydration was small, whereas a large amount of sucrose was accumulated. Northern blotting analysis revealed that these genes were transcribed as an operon. Gene disruption of resulted in a decrease in the trehalose level and in tolerance during dehydration. In contrast, gene disruption of resulted in an increase in both the amount of trehalose and tolerance. These results suggest that trehalose is important for the dehydration tolerance of this cyanobacterium. The amount of trehalose accumulated during dehydration was small, corresponding to 0·05–0·1 % of dry weight, suggesting that trehalose did not stabilize proteins and membranes directly during dehydration. To reveal the role of trehalose, the expression profiles of the wild-type strain and gene disruptants during dehydration were compared by using oligomeric DNA microarray. It was found that the expression of two genes, one of which encodes a cofactor of a chaperone DnaK, correlated with trehalose content, suggesting that a chaperone system induced by trehalose is important for the dehydration tolerance of sp. PCC 7120.

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2006-04-01
2024-12-13
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References

  1. Avonce N, Leyman B, Mascorro-Gallardo J. O, Van Dijck P, Thevelein J. M, Iturriaga G. 2004; The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiol 136:3649–3659 [CrossRef]
    [Google Scholar]
  2. Becker A, Schloder P, Steele J. E, Wegener G. 1996; The regulation of trehalose metabolism in insects. Experientia 52:433–439 [CrossRef]
    [Google Scholar]
  3. Bell W, Klaassen P, Ohnacker M, Boller T, Herweijer M, Schoppink P, van der Zee P, Wiemken A. 1992; Characterization of the 56 kDa subunit of yeast trehalose-6-phosphate synthase and cloning its genes reveal its identity with the product of CIF1 , a regulator of carbon catabolite inactivation. Eur J Biochem 201:951–959
    [Google Scholar]
  4. Bulman A. L, Nelson H. C. 2005; Role of trehalose and heat in the structure of the C-terminal activation domain of the heat shock transcription factor. Proteins 58:826–835 [CrossRef]
    [Google Scholar]
  5. Cai Y, Wolk C. P. 1990; Use of a conditionally lethal gene in Anabaena sp. strain PCC 7120 to select for double recombinants and to entrap insertion sequences. J Bacteriol 172:3138–3145
    [Google Scholar]
  6. Cansado J, Soto T, Fernandez J, Vicente-Soler J, Gacto M. 1998; Characterization of mutants devoid of neutral trehalase activity in the fission yeast Schizosaccharomyces pombe : partial protection from heat shock and high-salt stress. J Bacteriol 180:1342–1345
    [Google Scholar]
  7. Crowe J. H, Carpenter J. F, Crowe L. M. 1998; The role of vitrification in anhydrobiosis. Annu Rev Physiol 60:73–103 [CrossRef]
    [Google Scholar]
  8. Cumino A, Curatti L, Giarrocco L, Salerno G. L. 2002; Sucrose metabolism: Anabaena sucrose-phosphate synthase and sucrose-phosphate phosphatase define minimal functional domains shuffled during evolution. FEBS Lett 517:19–23 [CrossRef]
    [Google Scholar]
  9. Diamant S, Eliahu N, Rosenthal D, Goloubinoff P. 2001; Chemical chaperones regulate molecular chaperones in vitro and in cells under combined salt and heat stresses. J Biol Chem 276:39586–39591 [CrossRef]
    [Google Scholar]
  10. Dysvik B, Jonassen I. 2001; J-Express: exploring gene expression data using Java. Bioinformatics 17:369–370 [CrossRef]
    [Google Scholar]
  11. Eastmond P. J, van Dijken A. J, Spielman M, Kerr A, Tissier A. F, Dickinson H. G, Jones J. D, Smeekens S. C, Graham I. A. 2002; Trehalose-6-phosphate synthase 1, which catalyses the first step in trehalose synthesis, is essential for Arabidopsis embryo maturation. Plant J 29:225–235 [CrossRef]
    [Google Scholar]
  12. Ehira S, Ohmori M, Sato N. 2003; Genome-wide expression analysis of the responses to nitrogen deprivation in the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120. DNA Res 10:97–113 [CrossRef]
    [Google Scholar]
  13. Elbein A. D, Pan Y. T, Pastuszak I, Carroll D. 2003; New insights on trehalose: a multifunctional molecule. Glycobiology 13:17R–27R [CrossRef]
    [Google Scholar]
  14. Elhai J, Wolk C. P. 1988; Conjugal transfer of DNA to cyanobacteria. Methods Enzymol 167:747–754
    [Google Scholar]
  15. Giaever H. M, Styrvold O. B, Kaasen I, Strom A. R. 1988; Biochemical and genetic characterization of osmoregulatory trehalose synthesis in Escherichia coli . J Bacteriol 170:2841–2849
    [Google Scholar]
  16. Goloubinoff P, Mogk A, Zvi A. P, Tomoyasu T, Bukau B. 2001; Sequential mechanism of solubilization and refolding of stable protein aggregates by a bichaperone network. Proc Natl Acad Sci U S A 96:13732–13737
    [Google Scholar]
  17. Goyal K, Walton L. J, Tunnacliffe A. 2005; LEA proteins prevent protein aggregation due to water stress. Biochem J 388:151–157 [CrossRef]
    [Google Scholar]
  18. Hagemann M, Marin K. 1999; Salt-induced sucrose accumulation is mediated by sucrose-phosphate-synthase in cyanobacteria. J Plant Physiol 155:424–430 [CrossRef]
    [Google Scholar]
  19. 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 185:1719–1725 [CrossRef]
    [Google Scholar]
  20. Hill D. R, Peat A, Potts M. 1994; Biochemistry and structure of the glycan secreted by desiccation-tolerant Nostoc commune (cyanobacteria). Protoplasma 182:126–148 [CrossRef]
    [Google Scholar]
  21. Horlacher R, Uhland K, Klein W, Ehrmann M, Boos W. 1996; Characterization of a cytoplasmic trehalase of Escherichia coli . J Bacteriol 178:6250–6257
    [Google Scholar]
  22. Hottiger T, De Virgilio C, Hall M. N, Boller T, Wiemken A. 1994; The role of trehalose synthesis for the acquisition of thermotolerance in yeast. II. Physiological concentrations of trehalose increase the thermal stability of proteins in vitro . Eur J Biochem 219:187–193 [CrossRef]
    [Google Scholar]
  23. Inaba M, Suzuki I, Szalontai B, Kanesaki Y, Los D. A, Hayashi H, Murata N. 2003; Gene-engineered rigidification of membrane lipids enhances the cold inducibility of gene expression in Synechocystis . J Biol Chem 278:12191–12198 [CrossRef]
    [Google Scholar]
  24. Kandror O, DeLeon A, Goldberg A. L. 2002; Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. Proc Natl Acad Sci U S A 99:9727–9732 [CrossRef]
    [Google Scholar]
  25. Kaneko T, Nakamura Y, Wolk C. P. & 19 other authors; 2001; Complete genomic sequence of the filamentous nitrogen-fixing cyanobacterium Anabaena sp. strain PCC 7120. DNA Res 8:227–253 [CrossRef]
    [Google Scholar]
  26. Kanesaki Y, Suzuki I, Allakhverdiev S. I, 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 290:339–348 [CrossRef]
    [Google Scholar]
  27. Katoh H, Siga S, Nakahira Y, Ohmori M. 2003; Isolation and characterization of a drought-tolerant cyanobacterium, Nostoc sp. HK-01. Microb Environ 18:82–88 [CrossRef]
    [Google Scholar]
  28. Katoh H, Asthana R. K, Ohmori M. 2004; Gene expression in the cyanobacterium Anabaena sp. PCC 7120 under desiccation. Microb Ecol 47:164–174 [CrossRef]
    [Google Scholar]
  29. Kopp M, Muller H, Holzer H. 1993; Molecular analysis of the neutral trehalase gene from Saccharomyces cerevisiae . J Biol Chem 268:4766–4774
    [Google Scholar]
  30. Mackinney G. 1941; Absorption of light by chlorophyll solution. J Biol Chem 140:315–322
    [Google Scholar]
  31. Maruta K, Nakada T, Kubota M, Chaen H, Sugimoto T, Kurimoto M. 1995; Formation of trehalose from maltooligosaccharides by a novel enzymatic system. Biosci Biotechnol Biochem 59:1829–1834 [CrossRef]
    [Google Scholar]
  32. Maruta K, Mitsuzumi H, Nakada T, Kubota M, Chaen H, Fukuda S, Sugimoto T, Kurimoto M. 1996; Cloning and sequencing of a cluster of genes encoding novel enzyme of trehalose biosynthesis from thermophilic archaebacterium Sulfolobus acidocaldarius . Biochim Biophys Acta 1291:177–181 [CrossRef]
    [Google Scholar]
  33. Nakada T, Ikegami S, Chaen H, Kubota M, Fukuda S, Sug-imoto T, Kurimoto M, Tsujisaka Y. 1996a; Purification and characterization of thermostable maltooligosyl trehalose synthase from the thermoacidophilic archaebacterium Sulfolobus acidocaldarius . Biosci Biotechnol Biochem 60:263–266 [CrossRef]
    [Google Scholar]
  34. Nakada T, Ikegami S, Chaen H, Kubota M, Fukuda S, Sug-imoto T, Kurimoto M, Tsujisaka Y. 1996b; Purification and characterization of thermostable maltooligosyl trehalose trehalohydrolase from the thermoacidophilic archaebacterium Sulfolobus acidocaldarius . Biosci Biotechnol Biochem 60:267–270 [CrossRef]
    [Google Scholar]
  35. Paithoonrangsarid K, Shoumskaya M. A, Kanesaki Y. 8 other authors 2004; Five histidine kinases perceive osmotic stress and regulate distinct sets of genes in Synechocystis . J Biol Chem 279:53078–53086 [CrossRef]
    [Google Scholar]
  36. Paul M, Pellny T, Goddijn O. 2001; Enhancing photosynthesis with sugar signals. Trends Plant Sci 6:197–200 [CrossRef]
    [Google Scholar]
  37. Potts M. 1994; Desiccation tolerance of prokaryotes. Microbiol Mol Biol Rev 58:755–805
    [Google Scholar]
  38. Potts M. 1999; Mechanisms of desiccation tolerance in cyanobacteria. Eur J Phycol 34:319–328 [CrossRef]
    [Google Scholar]
  39. Potts M. 2001; Desiccation tolerance: a simple process?. Trends Microbiol 9:553–559 [CrossRef]
    [Google Scholar]
  40. Reed R. H, Richardson D. L, Warr S. R. C, Stewart W. D. P. 1984; Carbohydrate accumulation and osmotic stress in cyanobacteria. J Gen Microbiol 130:1–4
    [Google Scholar]
  41. 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. 1986; Organic solute accumulation in osmotically stressed cyanobacteria. FEMS Microbiol Rev 39:51–56 [CrossRef]
    [Google Scholar]
  42. Sano F, Asakawa N, Inoue Y, Sakurai M. 1999; A dual role for intracellular trehalose in the resistance of yeast cells to water stress. Cryobiology 39:80–87 [CrossRef]
    [Google Scholar]
  43. Scherer S, Potts M. 1989; Novel water stress protein from a desiccation-tolerant cyanobacterium. J Biol Chem 264:12546–12553
    [Google Scholar]
  44. Schluepmann H, Pellny T, van Dijken A, Smeekens S, Paul M. 2003; Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana . Proc Natl Acad Sci U S A 100:6849–6854 [CrossRef]
    [Google Scholar]
  45. Shirkey B, McMaster N. J, Smith S. C, Wright D. J, Rodriguez H, Jaruga P, Birincioglu M, Helm R. F, Potts M. 2003; Genomic DNA of Nostoc commune (Cyanobacteria) becomes covalently modified during long-term (decades) desiccation but is protected from oxidative damage and degradation. Nucleic Acids Res 31:2995–3005 [CrossRef]
    [Google Scholar]
  46. Shorter J, Lindquist S. 2005; Navigating the ClpB channel to solution. Nat Struct Mol Biol 12:4–6 [CrossRef]
    [Google Scholar]
  47. Silva Z, Alarico S, Nobre A, Horlacher R, Marugg J, Boos W, Mingote A. I, da Costa M. S. 2003; Osmotic adaptation of Thermus thermophilus RQ-1: lesson from a mutant deficient in synthesis of trehalose. J Bacteriol 185:5943–5952 [CrossRef]
    [Google Scholar]
  48. Singer M. A, Lindquist S. 1998; Multiple effects of trehalose on protein folding in vitro and in vivo . Mol Cell 1:639–648 [CrossRef]
    [Google Scholar]
  49. Watanabe A. 1960; List of algal strains in collection at the Institute of Applied Microbiology, University of Tokyo. J Gen Appl Microbiol 6:283–292 [CrossRef]
    [Google Scholar]
  50. Wingler A. 2002; The function of trehalose biosynthesis in plants. Phytochemistry 60:437–440 [CrossRef]
    [Google Scholar]
  51. Wolf A, Krämer R, Morbach S. 2003; Three pathways for trehalose metabolism in Corynebacterium glutamicum ATCC13032 and their significance in response to osmotic stress. Mol Microbiol 49:1119–1134 [CrossRef]
    [Google Scholar]
  52. Zähringer H, Thevelein J. M, Nwaka S. 2000; Induction of neutral trehalase Nth1 by heat and osmotic stress is controlled by STRE elements and Msn2/Msn4 transcription factors: variations of PKA effect during stress and growth. Mol Microbiol 35:397–406 [CrossRef]
    [Google Scholar]
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