1887

Abstract

Glycine betaine (GB) is an important osmolyte synthesized in response to different abiotic stresses, including salinity. The two known pathways of GB synthesis involve: 1) two step oxidation of choline (choline → betaine aldehyde → GB), generally found in plants, microbes and animals; and 2) three step methylation of glycine (glycine → sarcosine → dimethylglycine → GB), mainly found in halophilic archaea, sulphur bacteria and the cyanobacterium () Here, we transformed a salt-sensitive freshwater diazotrophic filamentous cyanobacterium () with -methyltransferase genes ( from using the triparental conjugation method. The transformed synthesized and accumulated GB in cells, and showed increased salt tolerance and protection to nitrogenase activity. The salt responsiveness of the transformant was also apparent as GB synthesis increased with increasing concentrations of NaCl in the nutrient solution, and maximal [12.92 µmol (g dry weight)] in cells growing at 0.5 M NaCl. Therefore, the transformed cyanobacterium has changed its behaviour from preferring freshwater to halophily. This study may have important biotechnological implications for the development of stress tolerant nitrogen-fixing cyanobacteria as biofertilizers for sustainable agriculture.

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2013-03-01
2024-04-26
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References

  1. Allen M. B., Arnon D. I. ( 1955). Studies on nitrogen-fixing blue-green algae. I. Growth and nitrogen fixation by Anabaena cylindrical Lemm. Plant Physiol 30:366–372 [View Article][PubMed]
    [Google Scholar]
  2. Atkinson D. E. ( 1977). Cellular Energy Metabolism and its Regulation New York: Academic Press;
    [Google Scholar]
  3. Chen T. H. H., Murata N. ( 2002). Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5:250–257 [View Article][PubMed]
    [Google Scholar]
  4. Chen T. H. H., Murata N. ( 2011). Glycinebetaine protects plants against abiotic stress: mechanisms and biotechnological applications. Plant Cell Environ 34:1–20 [View Article][PubMed]
    [Google Scholar]
  5. Codd G. A., Cook C. M., Stewart W. D. P. ( 1979). Purification and subunit structure of D-ribulose 1,5-bisphosphate carboxylase from the cyanobacterium Aphanothece halophytica . FEMS Microbiol Lett 6:81–86
    [Google Scholar]
  6. Curatti L., Ludden P. W., Rubio L. M. ( 2006). NifB-dependent in vitro synthesis of the iron-molybdenum cofactor of nitrogenase. Proc Natl Acad Sci U S A 103:5297–5301 [View Article][PubMed]
    [Google Scholar]
  7. Curatti L., Hernandez J. A., Igarashi R. Y., Soboh B., Zhao D., Rubio L. M. ( 2007). In vitro synthesis of the iron-molybdenum cofactor of nitrogenase from iron, sulfur, molybdenum, and homocitrate using purified proteins. Proc Natl Acad Sci U S A 104:17626–17631 [View Article][PubMed]
    [Google Scholar]
  8. Dubey A. K., Rai A. K. ( 1995). Application of algal biofertilizers (Aulosira fertilissima var. tenuis and Anabaena doliolum Bharadwaja) for sustained paddy cultivation in Northern India. Israel J Plant Sci 43:41–51 [CrossRef]
    [Google Scholar]
  9. Elhai J. ( 1993). Strong and regulated promoters in the cyanobacterium Anabaena PCC 7120. FEMS Microbiol Lett 114:179–184 [View Article][PubMed]
    [Google Scholar]
  10. Elhai J., Wolk C. P. ( 1988). Conjugal transfer of DNA to cyanobacteria. Methods Enzymol 167:747–754 [View Article][PubMed]
    [Google Scholar]
  11. Epstein E., Bloom A. J. ( 2005). Mineral Nutrition of Plants: Principles and Perspectives, 2nd edn. New York: Wiley;
    [Google Scholar]
  12. Fogg G. E., Stewart W. D. P., Fay P., Walsby A. E. ( 1973). New York: Academic Press;
  13. Garlick S., Oren A., Padan E. ( 1977). Occurrence of facultative anoxygenic photosynthesis among filamentous and unicellular cyanobacteria. J Bacteriol 129:623–629[PubMed]
    [Google Scholar]
  14. Gorham J., Wyn Jones R. G., McDonnell E. ( 1985). Some mechanisms of salt tolerance in crop plants. Plant Soil 89:15–40 [View Article]
    [Google Scholar]
  15. Hibino T., Waditee R., Araki E., Ishikawa H., Aoki K., Tanaka Y., Takabe T. ( 2002). Functional characterization of choline monooxygenase, an enzyme for betaine synthesis in plants. J Biol Chem 277:41352–41360 [View Article][PubMed]
    [Google Scholar]
  16. Holmström K. O., Somersalo S., Mandal A., Palva T. E., Welin B. ( 2000). Improved tolerance to salinity and low temperature in transgenic tobacco producing glycine betaine. J Exp Bot 51:177–185 [View Article][PubMed]
    [Google Scholar]
  17. Klähn S., Hagemann M. ( 2011). Compatible solute biosynthesis in cyanobacteria. Environ Microbiol 13:551–562 [View Article][PubMed]
    [Google Scholar]
  18. Lai M. C., Sowers K. R., Robertson D. E., Roberts M. F., Gunsalus R. P. ( 1991). Distribution of compatible solutes in the halophilic methanogenic archaebacteria. J Bacteriol 173:5352–5358[PubMed]
    [Google Scholar]
  19. Lai M. C., Yang D. R., Chuang M. J. ( 1999). Regulatory factors associated with synthesis of the osmolyte glycine betaine in the halophilic methanoarchaeon Methanohalophilus portucalensis . Appl Environ Microbiol 65:828–833[PubMed]
    [Google Scholar]
  20. Nomura M., Ishitani M., Takabe T., Rai A. K., Takabe T. ( 1995). Synechococcus sp. PCC 7942 transformed with Escherichia coli bet genes produces glycine betaine from choline and acquires resistance to salt stress. Plant Physiol 107:703–708[PubMed]
    [Google Scholar]
  21. Nyyssölä A., Kerovuo J., Kaukinen P., von Weymarn N., Reinikainen T. ( 2000). Extreme halophiles synthesize betaine from glycine by methylation. J Biol Chem 275:22196–22201 [View Article][PubMed]
    [Google Scholar]
  22. Nyyssölä A., Reinikainen T., Leisola M. ( 2001). Characterization of glycine sarcosine N-methyltransferase and sarcosine dimethylglycine N-methyltransferase. Appl Environ Microbiol 67:2044–2050 [View Article][PubMed]
    [Google Scholar]
  23. Oren A. ( 2000). Salts and Brine. The Ecology of Cyanobacteria: in Space and Time281–306 Whitton B. A., Potts M. Dordrecht: Kluwer Academic Publishers;
    [Google Scholar]
  24. Oren A. ( 2011). Thermodynamic limits to microbial life at high salt concentrations. Environ Microbiol 13:1908–1923 [View Article][PubMed]
    [Google Scholar]
  25. Rai A. K. ( 1990). Biochemical characteristics of photosynthetic response to various external salinities in halotolerant and fresh water cyanobacteria. FEMS Microbiol Lett 69:177–180 [View Article]
    [Google Scholar]
  26. Rai A. K., Tiwari S. P. ( 1999). Response to NaCl of nitrate assimilation and nitrogenase activity of the cyanobacterium Anabaena sp. PCC 7120 and its mutants. J Appl Microbiol 87:877–883 [View Article][PubMed]
    [Google Scholar]
  27. Reaston J., van den Hondel C. A., van Arkel G. A., Stewart W. D. ( 1982). A physical map of plasmid pDU1 from the cyanobacterium Nostoc PCC 7524. Plasmid 7:101–104 [View Article][PubMed]
    [Google Scholar]
  28. 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 [View Article]
    [Google Scholar]
  29. Rippka R., Deurelles J., Waterburry J. B., Herdman M., Stanier R. Y. ( 1979). Genetic assignments, strain histories and properties of pure culture of cyanobacteria. J Gen Microbiol 111:1–61 [CrossRef]
    [Google Scholar]
  30. Roger P. A., Kulasooriya S. A. ( 1993). Blue Green Algae and Rice Los Baros, Philippines: International Rice Research Institute;
    [Google Scholar]
  31. Rontein D., Basset G., Hanson A. D. ( 2002). Metabolic engineering of osmoprotectant accumulation in plants. Metab Eng 4:49–56 [View Article][PubMed]
    [Google Scholar]
  32. Rubio L. M., Ludden P. W. ( 2008). Biosynthesis of the iron-molybdenum cofactor of nitrogenase. Annu Rev Microbiol 62:93–111 [View Article][PubMed]
    [Google Scholar]
  33. Stewart W. D. P., Fitzgerald G. P., Burris R. H. ( 1968). Acetylene reduction by nitrogen-fixing blue-green algae. Arch Mikrobiol 62:336–348 [View Article][PubMed]
    [Google Scholar]
  34. Sulpice R., Tsukaya H., Nonaka H., Mustardy L., Chen T. H. H., Murata N. ( 2003). Enhanced formation of flowers in salt-stressed Arabidopsis after genetic engineering of the synthesis of glycine betaine. Plant J 36:165–176 [View Article][PubMed]
    [Google Scholar]
  35. Waditee R., Tanaka Y., Aoki K., Hibino T., Jikuya H., Takano J., Takabe T., Takabe T. ( 2003). Isolation and functional characterization of N-methyltransferases that catalyze betaine synthesis from glycine in a halotolerant photosynthetic organism Aphanothece halophytica . J Biol Chem 278:4932–4942 [View Article][PubMed]
    [Google Scholar]
  36. Waditee R., Bhuiyan M. N. H., Rai V., Aoki K., Tanaka Y., Hibino T., Suzuki S., Takano J., Jagendorf A. T. & other authors ( 2005). Genes for direct methylation of glycine provide high levels of glycinebetaine and abiotic-stress tolerance in Synechococcus and Arabidopsis . Proc Natl Acad Sci U S A 102:1318–1323 [View Article][PubMed]
    [Google Scholar]
  37. Waditee-Sirisattha R., Singh M., Kageyama H., Sittipol D., Rai A. K., Takabe T. ( 2012). Anabaena sp. PCC7120 transformed with glycine methylation genes from Aphanothece halophytica synthesized glycine betaine showing increased tolerance to salt. Arch Microbiol 194:909–914 [View Article][PubMed]
    [Google Scholar]
  38. Wall J. S., Christianson D. D., Dimler R. J., Senti F. R. ( 1960). Spectrophotometric determination of betaines and other quarternary nitrogen compounds as their periodides. Anal Chem 32:870–874 [View Article]
    [Google Scholar]
  39. Wolk C. P., Vonshak A., Kehoe P., Elhai J. ( 1984). Construction of shuttle vectors capable of conjugative transfer from Escherichia coli to nitrogen-fixing filamentous cyanobacteria. Proc Natl Acad Sci U S A 81:1561–1565 [View Article][PubMed]
    [Google Scholar]
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