Archives of Microbiology

, Volume 191, Issue 7, pp 595–601 | Cite as

Involvement of digalactosyldiacylglycerol in cellular thermotolerance in Synechocystis sp. PCC 6803

  • Naoki Mizusawa
  • Shinya Sakata
  • Isamu Sakurai
  • Naoki Sato
  • Hajime WadaEmail author
Original Paper


The effects of digalactosyldiacylglycerol (DGDG) deficiency on photosynthesis at high temperatures were examined using a dgdA mutant of Synechocystis sp. PCC 6803 incapable of DGDG biosynthesis. The dgdA mutant cells showed significant growth retardation when the temperature was increased from 30 to 38°C, although wild-type cells grew normally. The degree of growth retardation was enhanced by increasing light intensity. In addition, dgdA mutant cells showed increased sensitivity to the photoinhibition of photosynthesis when illuminated at 38°C. Analysis of photosynthesis in intact cells suggested that the inhibition of repair processes and accelerated photodamage resulted in growth retardation in dgdA mutant cells at high temperatures.


Digalactosyldiacylglycerol High-temperature stress Photoinhibition Photosynthesis Photosystem II 



This work was supported by Grants-in-Aid for Scientific Research (no. 20608002 to N. M., no. 20017006 to N. S., and no. 20570031 to H. W.) from the Ministry of Education, Culture, Sports, Science, and Technology of Japan


  1. Arnon DI, McSwain BD, Tsujimoto HY, Wada K (1974) Photochemical activity and components of membrane preparations from blue-green algae, I. Coexistence of two photosystems in relation to chlorophyll a and removal of phycocyanin. Biochim Biophys Acta 357:231–245PubMedCrossRefGoogle Scholar
  2. Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134PubMedCrossRefGoogle Scholar
  3. Awai K, Watanabe H, Benning C, Nishida I (2007) Digalactosyldiacylglycerol is required for better photosynthetic growth of Synechocystis sp. PCC6803 under phosphate limitation. Plant Cell Physiol 48:1517–1523PubMedCrossRefGoogle Scholar
  4. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917PubMedGoogle Scholar
  5. Blubaugh DJ, Cheneae GM (1990) Kinetics of photoinhibition in hydroxylamine-extracted photosystem II membranes: relevance to photoactivation and sites of electron donation. Biochemistry 29:5109–5118PubMedCrossRefGoogle Scholar
  6. Dörmann P, Hoffmann-Benning S, Balbo I, Benning C (1995) Isolation and characterization of an Arabidopsis mutant deficient in the thylakoid lipid digalactosyl diacylglycerol. Plant Cell 7:1801–1810PubMedCrossRefGoogle Scholar
  7. Ghanotakis DF, Topper JN, Yocum CF (1984) Structural organization of the oxidizing side of photosystem II. Exogenous reductants reduce and destroy the Mn-complex in photosystem II membranes depleted of the 17 and 23 kDa polypeptides. Biochim Biophys Acta 767:524–531CrossRefGoogle Scholar
  8. Gombos Z, Wada H, Murata N (1991) Direct evaluation of effects of fatty-acid unsaturation on the thermal properties of photosynthetic activities, as studied by mutation and transformation of Synechocystis PCC6803. Plant Cell Physiol 32:205–211Google Scholar
  9. Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W (2009) Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol 16:334–342PubMedCrossRefGoogle Scholar
  10. Härtel H, Lokstein H, Dörmann P, Grimm B, Benning C (1997) Changes in the composition of the photosynthetic apparatus in the galactolipid-deficient dgd1 mutant of Arabidopsis thaliana. Plant Physiol 115:1175–1184PubMedCrossRefGoogle Scholar
  11. Inoue-Kashino N, Kashino Y, Satoh K, Terashima I, Pakrasi HB (2005) PsbU provides a stable architecture for the oxygen-evolving system in cyanobacterial photosystem II. Biochemistry 44:12214–12228PubMedCrossRefGoogle Scholar
  12. Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauß N (2001) Three dimensional structure of cyanobacterial photosystem I at 2.5 Å. Nature 411:909–917PubMedCrossRefGoogle Scholar
  13. Kelly AA, Froehlich JE, Dörmann P (2003) Disruption of the two digalactosyldiacylglycerol synthase genes DGD1 and DGD2 in Arabidopsis reveals the existence of an additional enzyme of galactolipid synthesis. Plant Cell 15:2694–2706PubMedCrossRefGoogle Scholar
  14. Kimura A, Eaton-Rye JJ, Morita EH, Nishiyama Y, Hayashi H (2002) Protection of the oxygen-evolving machinery by the extrinsic proteins of photosystem II is essential for development of cellular thermotolerance in Synechocystis sp. PCC 6803. Plant Cell Physiol 43:932–938PubMedCrossRefGoogle Scholar
  15. Kurisu G, Zhang H, Smith JL, Cramer WA (2003) Structure of the cytochrome b 6 f complex of oxygenic photosynthesis: tuning the cavity. Science 302:1009–1014PubMedCrossRefGoogle Scholar
  16. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438:1040–1044PubMedCrossRefGoogle Scholar
  17. Malkin R, Niyogi K (2000) Photosynthesis. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, pp 568–628Google Scholar
  18. Mizusawa N, Sakurai I, Sato N, Wada H (2009) Lack of digalactosyldiacylglycerol increases the sensitivity of Synechocystis sp. PCC 6803 to high light stress. FEBS Lett 583:718–722PubMedCrossRefGoogle Scholar
  19. Nash D, Miyao M, Murata N (1985) Heat inactivation of oxygen evolution in photosystem II particles and its acceleration by chloride depletion and exogenous manganese. Biochim Biophys Acta 1186:52–58Google Scholar
  20. Nishiyama Y, Los DA, Murata N (1999) PsbU, a protein associated with photosystem II, is required for the acquisition of cellular thermotolerance in Synechococcus species PCC 7002. Plant Physiol 120:301–308PubMedCrossRefGoogle Scholar
  21. Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757:742–749PubMedCrossRefGoogle Scholar
  22. Roose JL, Kashino Y, Pakrasi HB (2007) The PsbQ protein defines cyanobacterial photosystem II complexes with highest activity and stability. Proc Natl Acad Sci USA 104:2548–2553PubMedCrossRefGoogle Scholar
  23. Sakurai I, Mizusawa N, Wada H, Sato N (2007) Digalactosyldiacylglycerol is required for stabilization of the oxygen-evolving complex in photosystem II. Plant Physiol 145:1361–1370PubMedCrossRefGoogle Scholar
  24. Somerville C, Browse J, Jaworski JG, Ohlrogge JB (2000) Lipids. In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. American Society of Plant Physiologists, Rockville, pp 456–527Google Scholar
  25. Steffen R, Kelly AA, Huyer J, Dörmann P, Renger G (2005) Investigations on the reaction pattern of photosystem II in leaves from Arabidopsis thaliana wild type plants and mutants with genetically modified lipid content. Biochemistry 44:3134–3142PubMedCrossRefGoogle Scholar
  26. Stroebel D, Choquest Y, Popot JL, Picot D (2003) An atypical haem in the cytochrome b 6 f complex. Nature 426:413–418PubMedCrossRefGoogle Scholar
  27. Takahashi S, Whitney SM, Badger MR (2009) Different thermal sensitivity of the repair of photodamaged photosynthetic machinery in cultured Symbiodinium species. Proc Natl Acad Sci USA 106:3237–3242PubMedCrossRefGoogle Scholar
  28. Tyystjärvi E (2008) Photoinhibition of photosystem II and photodamage of the oxygen evolving manganese cluster. Coord Chem Rev 252:361–376CrossRefGoogle Scholar
  29. Wada H, Murata N (1989) Synechocystis PCC6803 mutants defective in desaturation of fatty acids. Plant Cell Physiol 30:971–978Google Scholar
  30. Yamashita T, Butler WL (1968) Inhibition of chloroplasts by UV-irradiation and heat-treatment. Plant Physiol 43:2037–2040PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Naoki Mizusawa
    • 1
  • Shinya Sakata
    • 1
  • Isamu Sakurai
    • 1
  • Naoki Sato
    • 1
  • Hajime Wada
    • 1
    Email author
  1. 1.Department of Life Sciences, Graduate School of Arts and SciencesUniversity of TokyoTokyoJapan

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