1887

Abstract

This paper reports an investigation of salinity-induced glycolate metabolism in the cyanobacterium sp. PCC 7120 (hereafter PCC 7120). Quantitative analysis of transcripts for the photosynthesis-associated genes encoding ribulose-1,5-bisphosphate carboxylase oxygenase (Rubisco), phosphoribulokinase and transketolase, as well as those involved in glycolate metabolism (phosphoglycolate phosphatase, glycolate oxidase, alanine-glyoxylate aminotransferase and serine hydroxymethyltransferase) was performed. The expression of all investigated photosynthesis-associated genes except Rubisco was downregulated after 24 h NaCl treatment. However, under the same conditions, the transcripts encoding enzymes involved in glycolate metabolism were overexpressed. This was further confirmed by the quantitative analysis of the intermediates involved in glycolate metabolism. The intracellular levels of organic acids (glyceric, glycolic and glyoxylic acids) and amino acids (glycine and serine) were elevated in salt-treated cells as compared to those in the control cells. Transcriptional inhibition of photosynthesis-associated genes, and upregulation of genes and enhanced synthesis of intermediates associated with glycolate metabolism, indicate the occurrence of this photorespiratory metabolic pathway metabolism in PCC 7120 under salt stress.

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2011-03-01
2024-04-25
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References

  1. Alia E. A., Gahiza I. A. 2007; Accumulation of amino acids in Anabaena oryzae in response to sodium chloride salinity. J Appl Sci Res 3:263–266
    [Google Scholar]
  2. Badger M. R., Price G. D. 2003; CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot 54:609–622
    [Google Scholar]
  3. Bauwe H., Hagemann M., Fernie A. R. 2010; Photorespiration: players, partners and origin. Trends Plant Sci 15:330–336
    [Google Scholar]
  4. Bergman B. 1986; Glyoxylate induced changes in the carbon and nitrogen metabolism of the cyanobacterium Anabaena cylindrica . Plant Physiol 80:698–701
    [Google Scholar]
  5. Bergman B., Codd G. A., Hällbom L. 1984; Glycolate excretion by N2-fixing cyanobacteria treated with photorespiratory inhibitors. Z Pflanzenphysiol 113:451–460
    [Google Scholar]
  6. Bergman B., Renström E., Hallborn L., Codd G. A. 1985; Effects of aminooxyacetate and aminoacetonitrile on glycolate and ammonia release by the cyanobacterium Anabaena cylindica . Plant Physiol 77:536–539
    [Google Scholar]
  7. Betsche T., Schaller D., Melkonian M. 1992; Identification and characterization of glycolate oxidase and related enzymes from the endocyanotic algae Cyanophora paradoxa and from pea leaves. Plant Physiol 98:887–893
    [Google Scholar]
  8. Bhargava P., Mishra Y., Srivastava A. K., Narayan O. P., Rai L. C. 2008; Excess copper induces anoxygenic photosynthesis in Anabaena doliolum : a homology based proteomic assessment of its survival strategy. Photosynth Res 96:61–74
    [Google Scholar]
  9. Buick R. 1992; The antiquity of oxygenic photosynthesis: evidence from stromatolites in sulphate-deficient Archaean lakes. Science 255:74–77
    [Google Scholar]
  10. Chaves M. M., Flexas J., Pinheiro C. 2009; Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot (Lond 103:551–560
    [Google Scholar]
  11. Colman B., Norman E. G. 1997; Serine synthesis in cyanobacteria by a nonphotorespiratory pathway. Physiol Plant 100:133–136
    [Google Scholar]
  12. Dubey R. S., Rani M. 1989; Salinity induced accumulation of free amino acids in germinating rice seeds differing in salt tolerance. J Agron Crop Sci 163:236–247
    [Google Scholar]
  13. Eckardt N. A. 2005; Photorespiration revisited. Plant Cell 17:2139–2141
    [Google Scholar]
  14. Eisenhut M., Kahlon S., Hasse D., Ewald R., Lieman-Hurwitz J., Ogawa T., Ruth W., Bauwe H., Kaplan A., Hagemann M. 2006; The plant-like C2 glycolate cycle and the bacterial-like glycerate pathway cooperate in phosphoglycolate metabolism in cyanobacteria. Plant Physiol 142:333–342
    [Google Scholar]
  15. Eisenhut M., Ruth W., Haimovich M., Bauwe H., Kaplan A., Hagemann M. 2008; The photorespiratory glycolate metabolism is essential for cyanobacteria and might have been conveyed endosymbiontically to plants. Proc Natl Acad Sci U S A 105:17199–17204
    [Google Scholar]
  16. Ferjani A., Mustardy L., Sulpice R., Marin K., Suzuki I., Hagemann M., Murata N. 2003; Glucosylglycerol, a compatible solute, sustains cell division under salt stress. Plant Physiol 131:1628–1637
    [Google Scholar]
  17. Fulda S., Huckauf J., Schoor A., Hagemann M. 1999; Analysis of stress responses in the cyanobacterial strains Synechococcus sp. PCC 7942 Synechocystis PCC 6803, and Synechococcus sp. PCC 7418: osmolyte accumulation and stress protein synthesis. J Plant Physiol 154:240–249
    [Google Scholar]
  18. Fulda S., Mikkat S., Huang F., Huckauf J., Marin K., Norling B., Hagemann M. 2006; Proteome analysis of salt stress response in the cyanobacterium Synechocystis sp. strain PCC 6803: Proteomics 62733–2745
    [Google Scholar]
  19. Ginn H. P., Pearson L. A., Neilan B. A. 2010; NtcA from Microcystis aeruginosa PCC 7806 is autoregulatory and binds to the microcystin promoter. Appl Environ Microbiol 76:4362–4368
    [Google Scholar]
  20. Görg A., Obermaier C., Boguth G., Weiss W. 1999; Recent developments in two-dimensional gel electrophoresis with immobilized pH gradients: wide pH gradients up to pH 12, longer separation distances and simplified procedures. Electrophoresis 20:712–717
    [Google Scholar]
  21. Huang F., Fulda S., Hagemann M., Norling B. 2006; Proteomic screening of salt-stress-induced changes in plasma membranes of Synechocystis sp. strain PCC 6803: Proteomics 6910–920
    [Google Scholar]
  22. 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
    [Google Scholar]
  23. Kirst G. O., Bisson M. A. 1979; Regulation in turgor pressure in marine algae: ions and low molecular weight organic compounds. Aust J Plant Physiol 6:539–556
    [Google Scholar]
  24. López J. L. 2007; Two-dimensional electrophoresis in proteome expression analysis. J Chromatogr B Analyt Technol Biomed Life Sci 849:190–202
    [Google Scholar]
  25. Lu C., Zhang J. 2000; Role of light in the response of PSII photochemistry to salt stress in the cyanobacterium Spirulina platensis . J Exp Bot 51:911–917
    [Google Scholar]
  26. Marin K., Kanesaki Y., Los D. A., Murata N., Suzuki I., Hagemann M. 2004; Gene expression profiling reflects physiological processes in salt acclimation of Synechocystis sp. strain PCC 6803. Plant Physiol 136:3290–3300
    [Google Scholar]
  27. Measures J. C. 1975; Role of amino acids in osmoregulation of non-halophilic bacteria. Nature 257:398–400
    [Google Scholar]
  28. Moisander P. H., McClinton E. III, Paerl H. W. 2002; Salinity effects on growth, photosynthetic parameters, and nitrogenase activity in estuarine planktonic cyanobacteria. Microb Ecol 43:432–442
    [Google Scholar]
  29. Neilan B. A., Jacobs D., Del Dot T., Blackall L. L., Hawkins P. R., Cox P. T., Goodman A. E. 1997; rRNA sequences and evolutionary relationships among toxic and nontoxic cyanobacteria of the genus Microcystis . Int J Syst Bacteriol 47:693–697
    [Google Scholar]
  30. Norman E. G., Colman B. 1988; Evidence for an incomplete glycolate pathway in cyanobacteria. J Plant Physiol 132:766–768
    [Google Scholar]
  31. Norman E. G., Colman B. 1992; Formation and metabolism of glycolate in cyanobacterium Coccochloris peniocystis . Arch Microbiol 157:375–380
    [Google Scholar]
  32. Pfaffl M. W. 2001; A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45
    [Google Scholar]
  33. Rai L. C., Raizada M. 1985; Effect of nickel and silver ion on survival, growth, carbon fixation and nitrogenase activity in Nostoc muscorum : regulation of toxicity by EDTA and calcium. J Gen Appl Microbiol 31:329–337
    [Google Scholar]
  34. Rani G. 2007; Changes in protein profile and amino acids in Cladophora vagabunda (Chlorophyceae) in response to salinity stress. J Appl Phycol 19:803–807
    [Google Scholar]
  35. Renström E., Bergman B. 1989; Glycolate metabolism in cyanobacteria. I Glycolate excretion and phosphoglycolate phosphatase activity. Physiol Plant 75:137–143
    [Google Scholar]
  36. Renström-Kellner E., Bergman B. 1989; Glycolate metabolism in cyanobacteria. III. Nitrogen controls excretion and metabolism of glycolate in Anabaena cylindrica . Physiol Plant 77:46–51
    [Google Scholar]
  37. Renström-Kellner E., Bergman B. 1990; Glycolate metabolism in cyanobacteria. IV. Uptake, growth and metabolic pathways. Physiol Plant 78:285–292
    [Google Scholar]
  38. Schmidt-Goff C. M., Federspiel N. A. 1993; In vivo and in vitro footprinting of a light-regulated promoter in the cyanobacterium Fremyella diplosiphon . J Bacteriol 175:1806–1813
    [Google Scholar]
  39. Seki M., Ishida J., Narusaka M., Fujita M., Nanjo T., Umezawa T., Kamiya A., Nakajima M., Enju A. other authors 2002; Monitoring the expression pattern of around 7,000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray. Funct Integr Genomics 2:282–291
    [Google Scholar]
  40. Singh R. N. 1961 Role of Blue-Green Algae in the Nitrogen Economy of Indian Agriculture New Delhi: ICAR;
    [Google Scholar]
  41. Sivakumar P., Sharmila P., Pardha Saradhi P. 2000; Proline alleviates salt-stress-induced enhancement in ribulose-1,5-bisphosphate oxygenase activity. Biochem Biophys Res Commun 279:512–515
    [Google Scholar]
  42. Srivastava A. K., Bhargava P., Rai L. C. 2005; Salinity and copper-induced oxidative damage and changes in the antioxidative defense system of Anabaena doliolum . World J Microbiol Biotechnol 21:1291–1298
    [Google Scholar]
  43. Srivastava A. K., Ara A., Bhargava P., Mishra Y., Rai S. P., Rai L. C. 2007; A rapid and cost-effective method of genomic DNA isolation from cyanobacterial culture, mat and soil suitable for genomic fingerprinting and community analysis. J Appl Phycol 19:373–382
    [Google Scholar]
  44. Srivastava A. K., Bhargava P., Thapar R., Rai L. C. 2008; Salinity-induced physiological and proteomic changes in Anabaena doliolum . Environ Exp Bot 64:49–57
    [Google Scholar]
  45. Srivastava A. K., Bhargava P., Kumar A., Rai L. C., Neilan B. A. 2009; Molecular characterization and effect of salinity on cyanobacterial diversity in the rice fields of Eastern Uttar Pradesh, India. Saline Syst 5:4
    [Google Scholar]
  46. Sudhir P. R., Pogoryelov D., Kovàcs L., Garab G., Murthy S. D. S. 2005; The effect of salt stress on photosynthetic electron transport and thylakoid membrane proteins in the cyanobacterium Spirulina platensis . J Biochem Mol Biol 38:481–485
    [Google Scholar]
  47. Thompson A. S., Rhodes J. C., Pettman I. 1988 Culture Collection of Algae and Protozoa, Catalogue of Strains Swindon, UK: National Environment Research Council;
    [Google Scholar]
  48. Winicov I., Seemann J. R. 1990; Expression of genes for photosynthesis and the relationship to salt tolerance of alfalfa ( Medicago sativa ) cells. Plant Cell Physiol 31:1155–1161
    [Google Scholar]
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