Advertisement

Russian Journal of Plant Physiology

, Volume 51, Issue 1, pp 53–62 | Cite as

Changes in Lipid Metabolism during Adaptation of the Dunaliella salina Photosynthetic Apparatus to High CO2 Concentration

  • E. A. Muradyan
  • G. L. Klyachko-Gurvich
  • L. N. Tsoglin
  • T. V. Sergeyenko
  • N. A. Pronina
Article

Abstract

The effects of CO2 on the content and composition of lipid fatty acids (FA) and on the photosynthetic characteristics of unicellular halophilic green alga Dunaliella salina (known to be susceptible to CO2 stress) were investigated. It was shown that even one-day-long increase in the CO2 concentration (from 2 to 10%) provoked an increase in the total amount of FA on the dry weight basis by 30%. After 7-day-long growth at 10% CO2, this value was 2.7-fold higher than that at 2% CO2. The difference in the FA content and composition indicated the activation of FA synthesis de novo and inhibition of their elongation and desaturation, as well as the increase in the relative content of saturated FA at 10% CO2. It was demonstrated that, after one-day-long CO2 stress, the MGDG/DGDG ratio increased fourfold without change in the sum of their FA, which indicates the increase in the proportion of lipids predisposed to micellar (hexagonal phase) but not lamellar structure formation. Under short-term CO2 stress, the ratio of ω3/ω6 FA increased and the content of E-16:1ω13 FA in phosphatidylglycerols increased sharply. The drop in protein content especially in the photosystem I (PSI) preparations, as well as diminishing the ratio of F700-to-F686 nm fluorescence (F700/F686) under short-term CO2 stress argued for the significant damage to PSI. The reversibility of these changes at more prolonged treatment (7 and 10 days) demonstrated that D. salina cells could restore the functional activity of PSI. The lower level of F700/F686, chlorophyll a (Chla)/Chlb, and ω3/ω6 FA ratio in line with the higher level of E-16:1ω13 in the cells growing for a long time at the high CO2 concentration is characteristic for the new structural and functional state of the photosynthetic apparatus providing for the effective photosynthesis of D. salina under these conditions.

Dunaliella salina extremely high CO2 concentration composition of lipid fatty acids thylakoid membranes photosystems adaptation 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

REFERENCES

  1. 1.
    Kodama, M., Iremoto, H., and Miyachi, S.A., New Species of Highly CO2-Tolerant Fast Growing Marine Microalga Suitable for High Density Culture, J. Mar. Biotechnol., 1993, vol. 1, pp. 21-25.Google Scholar
  2. 2.
    Sergeenko, T.V., Muradyan, E.A., Pronina, N.A., Klyachko-Gurvich, G.L., Mishina, I.M, and Tsoglin, L.N., The Effect of Extremely High CO2 Concentration on the Growth and Biochemical Composition of Microalgae, Fiziol. Rast. (Moscow) 2000, vol. 47, pp. 722-729 (Russ. J. Plant Physiol., Engl. Transl.).Google Scholar
  3. 3.
    Semenenko, V.E., Vladimirova, M.G., Tsoglin, L.N., and Popova, M.A., Growth, Productivity, and the Photosynthesis Rate of Chlorella Culture as Dependent on the CO2 Concentration in Gas Mixture and on the Specific Rate of Air Inflow, Controlled Biosynthesis, Ierusalimskii, N.D. and Kovrov, B.G., Eds., Moscow: Nauka, 1966, pp. 128-136.Google Scholar
  4. 4.
    Seckbach, J., Gross, H., and Nathan, M.B., Growth and Photosynthesis of Cianidium caldarium Cultured under Pure CO2, Israel J. Bot., 1971, vol. 20, pp. 84-90.Google Scholar
  5. 5.
    Tsuzuki, M., Ohnuma, E., Sato, A., Takaku, S., and Kanagochi, N., Effects of CO2 Concentration during Growth on Fatty Acid Composition in Microalgae, Plant Physiol., 1990, vol. 93, pp. 851-856.Google Scholar
  6. 6.
    Pronina, N.A., Rogova, N.B., Furnadzhieva, S., Klyachko-Gurvich, G.L., and Semenenko, V.E., Effect of CO2 Concentration on the Fatty Acid Composition of Lipids in Chlamydomonas reinhardtii Cia-3, a Mutant Deficient in CO2 Concentrating Mechanism, Fiziol. Rast. (Moscow), 1998, vol. 45, pp. 529-538 (Russ. J. Plant Physiol., Engl. Transl.).Google Scholar
  7. 7.
    Mouradian, E.A., Klyachko-Gurvich, G.L., and Pronina, N.A., Lipid Metabolism of Spirulina platensis under CO2-Stress, Advances in Plant Lipid Research, Sanchez, J. et al., Eds., Sevilla: Univ. de Sevilla, 1998, pp. 511-513.Google Scholar
  8. 8.
    Manuilskaya, S.V., The Role of Thylakoid Membrane Components in Functioning of the Photosynthetic Apparatus and Adaptation to Environmental Conditions, Fiziol. Biokhim. Kul't. Rast., 1987, vol. 19, pp. 29-41.Google Scholar
  9. 9.
    Klyachko-Gurvich, G.L., Ladygin, V.G., Pronina, N.A., Ryabykh, I.B., and Semenenko, V.E., Specific Composition of Fatty Acids in Lipids of Chlamydomonas reinhardtii Mutants with Different Organization of Chloroplast Photosystems, Fiziol. Rast. (Moscow), 1991, vol. 38, pp. 1171-1179 (Sov. Plant Physiol., Engl. Transl.).Google Scholar
  10. 10.
    Thompson, G.A., Jr., Lipids and Membrane Function in Green Algae, Biochim. Biophys. Acta, 1996, vol. 1302, pp. 17-45.Google Scholar
  11. 11.
    Klyachko-Gurvich, G.L., Tsoglin, L.N., Doucha, J., Kopetskii, J., Shebalina, I.B., and Semenenko, V.E., Desaturation of Fatty Acids as an Adaptive Response to Shifts in Light Intensity, Physiol. Plant., 1999, vol. 107, pp. 240-249.Google Scholar
  12. 12.
    Iwasaki, I., Hu, Q., Kurano, N., and Miyachi, S., Effect of Extremely High CO2 Stress on Energy Distribution between Photosystem I and Photosystem II in a “High-CO2” Tolerant Green Alga Chlorococcum littorale and the Intolerant Green Alga Stichococcus bacillaris, J. Photochem. Photobiol. B: Biol., 1998, vol. 44, pp. 184-190.Google Scholar
  13. 13.
    Catalogue of Microalgal Cultures in the Collections of the USSR, Semenenko, V.E., Ed., Moscow: Akad. Nauk SSSR, 1991.Google Scholar
  14. 14.
    Abdullaev, A.A. and Semenenko, V.E., Some Characteristics of Intense Culture of Dunaliella salina, Fiziol. Rast. (Moscow), 1979, vol. 21, pp. 1145-1153 (Sov. Plant Physiol., Engl. Transl.).Google Scholar
  15. 15.
    Klyachko-Gurvich, G.L., Pronina, N.A., Furnadzhieva, S., Ramazanov, Z.M., and Petkov, G., Lipid Composition and Membrane State of Dunaliella salina Cells Subjected to Suboptimal Temperature, Fiziol. Rast. (Moscow), 1997, vol. 44, pp. 212-221 (Russ. J. Plant Physiol., Engl. Transl.).Google Scholar
  16. 16.
    Kaits, M., Techniques of Lipidology, Amsterdam: North Holland, 1972.Google Scholar
  17. 17.
    Roughan, P.G., Slack, C.R., and Holland, R., Generation of Phosholipid Artefacts during Extraction of Developing Soybean Seeds with Methanolic Solvents, Lipids, 1978, vol. 13, pp. 497-503.Google Scholar
  18. 18.
    Eichenberger, W., Araki, S., and Muller, D.G., Betaine Lipids and Phospholipids in Brown Algae, Phytochemistry, 1993, vol. 34, pp. 1323-1333.Google Scholar
  19. 19.
    Bruse, B.D. and Malkin, R., Structural Aspects of Photosystem I from Dunaliella salina, Plant Physiol., 1988, vol. 88, pp. 1204-1206.Google Scholar
  20. 20.
    Porra, R.J., Thompson, W.A., and Kriedemann, P.E., Determination of Accurate Extinction Coefficients and Simultaneous Equation for Assaying Chlorophyll a and b with Four Different Solvents: Verification of the Concentration of Chlorophyll by Atomic Absorption Spectroscopy, Biochim. Biophis. Acta, 1989, vol. 975, pp. 384-394.Google Scholar
  21. 21.
    Lowry, D., Rosebrough, N., Farr, A.L., and Randal, R.L., Protein Measurement with the Folin Phenol Reagent, J. Biol. Chem., 1951, vol. 193, pp. 265-275.Google Scholar
  22. 22.
    Chen, F. and Johns, M., Effect of C/N Ratio and Aeration on the Fatty Acid Composition of Heterotrophic Chlorella sorokiniana, J. Appl. Phycol., 1991, vol. 3, pp. 203-209.Google Scholar
  23. 23.
    Linch, D.V. and Thompson, G.A., Jr., Low Temperature Induced Alterations in the Chloroplast and Microsomal Membranes of Dunaliella salina, Plant Physiol., 1982, vol. 69, pp. 1369-1375.Google Scholar
  24. 24.
    Fried, A., Tietz, A., Ben-Amotz, A., and Eichenberger, W., Lipid Composition of the Halotolerant Alga, Dunaliella bardawil, Biochim. Biophys. Acta, 1982, vol. 713, pp. 419-426.Google Scholar
  25. 25.
    Makewicz, A., Radunz, A., and Schmid, G.H., Detection of Phosphatidylglycerol and Monogalactosyldigliceride on Peptides of Photosystem I in Nicotiana tabacum Species, Plant Lipid Metabolism, Kader, J.-C. and Mazliak, V., Eds., Dordrecht: Kluwer, 1995, pp. 156-160.Google Scholar
  26. 26.
    Klyachko-Gurvich, G.L., Pronina, N.A., Ladygin, V.G., Tsoglin, L.N., and Semenenko, V.E., Uncoupled Functioning of Separate Photosystems: 1. Characteristics of Fatty Acid Desaturation and Its Role, Fiziol. Rast. (Moscow), 2000, vol. 47, pp. 688-698 (Russ. J. Plant Physiol., Engl. Transl.).Google Scholar
  27. 27.
    Hartel, H., Lokstein, H., Dormann, P., Grimm, B., and Benning, Ch., Changes in the Composition of the Photosynthetic Apparatus in the Galactolipid-Deficient dgd1 Mutant of Arabidopsis thaliana, Plant Physiol., 1997, vol. 115, pp. 1175-1184.Google Scholar
  28. 28.
    Reifarth, F., Christen, G., Seeliger, A.G., Dormann, P., Benning, C., and Renger, G., Modification of the Water Oxidizing Complex in Leaves of the dgd1 Mutant of Arabidopsis thaliana Deficient in the Galactolipid Digalactosyldiacylglycerol, Biochemistry, 1997, vol. 36, pp. 11769-11776.Google Scholar
  29. 29.
    Somerville, Ch. and Browse, I., Plant Lipids: Metabolism, Mutants, and Membranes, Science, 1991, vol. 252, pp. 80-87.Google Scholar
  30. 30.
    Trémoliéres, A., Dainese, P., and Bassi, R., Heterogenous Lipid Distribution among Chlorophyll-Binding Proteins of Photosystem II in Maize Mesophyll Chloroplasts, Eur. J. Biochem., 1994, vol. 221, pp. 721-730.Google Scholar
  31. 31.
    Demidov, E., Iwasaki, I., Satoh, A., Kurano, N., and Miyachi, S., Short-Term Responses of Photosynthetic Reactions to Extremely High CO2 Stress in a “High-CO2” Tolerant Green Alga Chlorococcum littorale and an Intolerant Green Alga Stichococcus bacillaris, Fiziol. Rast. (Moscow), 2000, vol. 47, pp. 710-721 (Russ. J. Plant Physiol., Engl. Transl.).Google Scholar
  32. 32.
    Pesheva, I., Kodama, M., Dionisio-Sese, M.L., and Miyachi, S., Changes in Photosynthetic Characteristics Induced by Transferring Air-Grown Cells of Chlorococcum littorale to High-CO2 Conditions, Plant Cell Physiol., 1994, vol. 35, pp. 379-387.Google Scholar
  33. 33.
    Satoh, A., Kurano, N., Senger, H., and Miyachi, S., Regulation of Energy Balance in Photosystems in Response to Changes in CO2 Concentrations and Light Intensities during Growth in Extremely-High-CO2-Tolerant Green Microalgae, Plant Cell Physiol., 2002, vol. 43, pp. 440-451.Google Scholar

Copyright information

© MAIK “Nauka/Interperiodica” 2004

Authors and Affiliations

  • E. A. Muradyan
    • 1
  • G. L. Klyachko-Gurvich
    • 1
  • L. N. Tsoglin
    • 1
  • T. V. Sergeyenko
    • 1
  • N. A. Pronina
    • 1
  1. 1.Timiryazev Institute of Plant Physiology, Russian Academy of SciencesMoscowRussia

Personalised recommendations