Russian Journal of Plant Physiology

, Volume 53, Issue 2, pp 153–162 | Cite as

The effect of nitrogen starvation on the ultrastructure and pigment composition of chloroplasts in the acidothermophilic microalga Galdieria sulphuraria

  • M. P. SinetovaEmail author
  • A. G. Markelova
  • D. A. Los


We studied the effect of nitrogen starvation on growth indices, vitality, ultrastructure, and the photosynthetic apparatus of unique acidothermophilic microalga Galdieria sulphuraria (Galdieri) Merola. Long-term nitrogen starvation ceased G. sulphuraria growth and cell division. During the first days of starvation, phycobiliproteins degraded first, then the content of chlorophyll and carotenoids decreased to trace amounts, chloroplast reduced, cell wall became thinner, and storage compounds accumulated. However, the cells were alive. A comparison with the effects of nitrogen starvation on other photosynthesizing organisms showed that suppression of cell division, reduction of the photosynthetic apparatus to some minimum, and accumulation of storage compounds are a universal response to this stress.

Key words

Galdieria sulphuraria nitrogen starvation ultrastructure pigments 


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  1. 1.
    Doemel, W.N. and Brock, T.D., The Physiological Ecology of Cyanidium caldarium, J. Gen. Microbiol., 1971, vol. 67, pp. 17–32.Google Scholar
  2. 2.
    Baily, R.W. and Staehelin, L.A., The Chemical Composition of Isolated Cell Walls of Cyanidium caldarium, J. Gen. Microbiol., 1968, vol. 54, pp. 269–275.Google Scholar
  3. 3.
    Muravenko, O.V., Selyakh, I.O., Kononenko, N.V., and Stadnichuk, I.N., Chromosome Numbers and Nuclear DNA Contents in the Red Microalgae Cyanidium caldarium and Three Galdieria Species, Eur. J. Phycol., 2001, vol. 36, pp. 227–232.CrossRefGoogle Scholar
  4. 4.
    Gross, W., Revision of Comparative Traits for Acido-and Thermophilic Red Algae Cianidium and Caldieria, Enigmatic Microorganisms and Life in Extreme Environments, Seckbach, J., Ed., Dordrecht: Kluwer, 1999, pp. 439–446.Google Scholar
  5. 5.
    Sentsova, O.Yu., Multiplicity of Unicellular Acido-Thermophilic Algae from Galdieria Spice (Rhodophyta, Cyanidiophyceae), Bot. Zh. (St. Petersburg), 1991, vol. 76, pp. 69–79.Google Scholar
  6. 6.
    Sentsova, O.Yu., Kravtsova, T.R., and Gusev, M.V., Physiological and Biochemical Features of Acido-Thermophilic Algae Cyanidium caldarium and Caldieria sulphuraria and Their Growth in Combined Culture under Photoautotrophic, Mixotrophic, and Heterotrophic Conditions, Fiziol. Rast. (Moscow), 1988, vol. 35, pp. 516–525 (Sov. Plant Physiol., Engl. Transl.).Google Scholar
  7. 7.
    Gromov, B.V., Avilov, I.A., Andreev, L.V., Lyutikov, V.N., and Nikitina, V.N., Acidophilic Alga Cyanidium caldarium from Thermal Springs on Far East, Biol. Nauki, 1979, vol. 10, pp. 78–82.Google Scholar
  8. 8.
    Ignat’evskaya, M.A. and Mineeva, L.A., Effects of Medium Acidity on the Growth and Pigment Content in Cyanidium caldarium as Dependent on the Mode of Their Existence, Fiziol. Rast. (Moscow), 1982, vol. 29, pp. 586–590 (Sov. Plant Physiol., Engl. Transl.).Google Scholar
  9. 9.
    Selyakh, I.O., Mineeva, L.A., and Gusev, M.V., Features of Cell Ultrastructure in Cyanidium caldarium at Different Growth Stages of Periodic Culture, Izv. Akad. Nauk SSSR, Ser. Biol., 1984, pp. 74–81.Google Scholar
  10. 10.
    Stadnichuk, I.N., Rakhimberdieva, M.G., Boichenko, V.A., Karapetyan, N.V., Selyakh, I.O., and Bolychevtseva, Yu.V., Glucose-Induced Inhibition of the Photosynthetic Pigment Apparatus in Heterotrophically-Grown Galdieria partita, Fiziol. Rast. (Moscow), 2000, vol. 47, pp. 668–675 (Russ. J. Plant Physiol., Engl. Transl., pp. 585–592).Google Scholar
  11. 11.
    Gerasimenko, L.M., Pusheva, M.A., and Goryunova, S.V., Developmental Cycle of and Ultrastructure of Cyanidium caldarium, Mikrobiologiya, 1972, vol. 41, pp. 324–326.Google Scholar
  12. 12.
    Nichols, K.E. and Bogorad, L., Studies on Phycobilin Formation with Mutants of Cyanidium caldarium, Nature, 1960, vol. 188, pp. 126–128.Google Scholar
  13. 13.
    Troxler, R.F. and Bogorad, L., Studies on the Formation of Phycocyanin, Porphyrins and a Blue Phycobilin by Wild-Type and Mutant Strains of Cyanidium caldarium, Plant Physiol., 1966, vol. 41, pp. 491–499.PubMedGoogle Scholar
  14. 14.
    Diner, B.A. and Wollman, F.A., Functional Comparison of the Photosystem II Center-Antenna Complex of a Phycocyanin-Less Mutant of Cyanidium caldarium with That of Chlorella pyrenoidosa, Plant Physiol., 1979, vol. 63, pp. 20–25.Google Scholar
  15. 15.
    Vladimirova, M.G., Klyachko-Gurvich, G.L., Kurnosova, T.A., and Zhukova, T.S., A Comparative Characterization of Growth and Biosynthesis Direction in Different Chlorella Strains under Nitrogen Starvation: 1. Investigation of Growth and Productivity, Fiziol. Rast. (Moscow), 1968, vol. 15, pp. 993–1001 (Sov. Plant Physiol., Engl. Transl.).Google Scholar
  16. 16.
    Garciaferris, C., Delosrios, A., Ascaso, C., and Moreno, J., Correlated Biochemical and Ultrastructural Changes in Nitrogen Starved Euglena gracilis, J. Phycol., 1996, vol. 32, pp. 953–963.Google Scholar
  17. 17.
    Görl, M., Sauer, J., Baier, T., and Forchhammer, K., Nitrogen-Starvation-Induced Chlorosis in Synechococcus PCC 7942: Adaptation to Long-Term Survival, Microbiology, 1998, vol. 144, pp. 2449–2458.PubMedGoogle Scholar
  18. 18.
    Zhukova, T.S., Klyachko-Gurvich, G.L., Vladimirova, M.G., and Kurnosova, T.A., A Comparative Characterization of Growth and Biosynthesis Direction in Different Chlorella Strains under Nitrogen Starvation: 2. Carbohydrate and Lipid Production, Fiziol. Rast. (Moscow), 1969, vol. 16, pp. 96–101 (Sov. Plant Physiol., Engl. Transl.).Google Scholar
  19. 19.
    Klyachko-Gurvich, G.L., About the Metabolism Directionality for Protein, Carbohydrate, and Lipids Biosynthesis in Chlorella, Upravlyaemyi biosintez (Guided Biosynthesis), Moscow: Nauka, 1966, pp. 116–121.Google Scholar
  20. 20.
    Allen, M.M. and Smith, A.J., Nitrogen Chlorosis in Blue-Green Algae, Arch. Microbiology, 1969, vol. 69, pp. 114–120.Google Scholar
  21. 21.
    Vladimirova, M.G., Changes in Ultrastructure during Functional Cell Reconstruction in Chlorella sp. K., Fiziol. Rast. (Moscow), 1976, vol. 23, pp. 1180–1187 (Sov. Plant Physiol., Engl. Transl.).Google Scholar
  22. 22.
    Lau, R.H., MacKenzie, M.M., and Doolittle, W.F., Phycocyanin Synthesis and Degradation in the Blue-Green Bacterium Anacystis nidulans, J. Bacteriol., 1977, vol. 132, pp. 771–778.PubMedGoogle Scholar
  23. 23.
    Chemeris, Yu.K., Popova, A.V., and Aratyunyan, A.A., Effect of Nutrition Deficiency on the Photosynthetic Apparatus in Clorella, Fiziol. Rast. (Moscow), 1989, vol. 36, pp. 49–56 (Sov. Plant Physiol., Engl. Transl.).Google Scholar
  24. 24.
    Chemeris, Yu.K., Venediktov, P.S., and Rubin, A.B., Role of Chloroplast Respiration in the Inactivation of Photosystem II in Chlorella, Fiziol. Rast. (Moscow), 1996, vol. 43, pp. 833–841 (Russ. J. Plant Physiol., Engl. Transl., pp. 716–723).Google Scholar
  25. 25.
    Berges, J.A., Charlebois, D.O., Mauzerall, D.C., and Falkowski, P.G., Differential Effects of Nitrogen Limitation on Photosynthetic Efficiency of Photosystem I and II in Microalgae, Plant Physiol., 1996, vol. 110, pp. 689–696.PubMedGoogle Scholar
  26. 26.
    Sauer, J., Schreiber, U., Schmid, R., Volker, U., and Forchhamer, K., Nitrogen Starvation-Induced Chlorosis in Synechococcus PCC 7942. Low-Level Photosynthesis as a Mechanism of Long-Term Survival, Plant Physiol., 2001, vol. 126, pp. 233–243.CrossRefPubMedGoogle Scholar
  27. 27.
    Vladimirova, M.G., Bartsevich, E.D., Zholdakov, I.A., Epifanova, O.O., Markelova, A.G., Maslova, I.P., and Kuptsova, E.S., IPPAS — Collection of Microalgae of Timiryazev Institute of Plant Physiology, Acad. Sci. USSR, Katalog kul’tur mikrovodoroslei v kollektsiyakh SSSR (Catalogue of Microalgal Cultures in the Collections of USSR), Semenenko, V.E., Ed., Moscow: Inst. Plant Physiol., Russ. Acad. Sci., 1991, pp. 8–61.Google Scholar
  28. 28.
    Markelova, A.G., Vladimirova, M.G., and Kuptsova, E.S., A Comparison of Cytochemical Methods for the Rapid Evaluation of Microalgal Viability, Fiziol. Rast. (Moscow), 2000, vol. 47, pp. 924–929 (Russ. J. Plant Physiol., Engl. Transl., pp. 815–819).Google Scholar
  29. 29.
    Merzlyak, M.N. and Naqvi, K.R., On Recording the True Absorption Spectrum and the Scattering Spectrum of a Turbid Sample: Application to Cell Suspensions of the Cyanobacterium Anabaena variabilis, J. Photochem. Photobiol., Ser. B: Biol., 2000, vol. 58, pp. 123–129.Google Scholar
  30. 30.
    Lichtenthaler, H.K., Chlorophylls and Carotenoids: Pigments of Photosynthetic Biomembrans, Methods Enzymol., 1987, vol. 148, pp. 351–382.Google Scholar
  31. 31.
    Markelova, A.G., Vladimirova, M.G., and Semenenko, V.E., Ultrastructura of RBPC in Algal Cells, Fiziol. Rast. (Moscow), 1990, vol. 37, pp. 907–911 (Sov. Plant Physiol., Engl. Transl.).Google Scholar
  32. 32.
    Reynolds, E.S., The Use of Lead Citrate at High pH as an Electronopaque Stain in Electron Microscopy, J. Cell Biol., 1963, vol. 17, pp. 208–212.CrossRefPubMedGoogle Scholar
  33. 33.
    Mercer, F.V., Bogorad, L., and Mullens, R., Studies with Cyanidium caldarium. I. The Fine Structure and Systematic Position of the Organism, J. Cell Biol., 1962, vol. 13, pp. 393–403.CrossRefPubMedGoogle Scholar
  34. 34.
    South, G.R. and Whittick, A., Introduction to Phycology, London: Blackwell, 1987.Google Scholar
  35. 35.
    Bhattacharya, D., The Phylogeny and Evolution of the Thermoacidophilic Cyanidiales,
  36. 36.
    Baier, K., Nicklisch, S., Nitsche, Y., and Schöfer, H., Phycobilisome Degradation in Cyanobacteria, FEMS Microbiol. Lett., 2001, vol. 195, pp. 35–45.PubMedGoogle Scholar

Copyright information

© MAIK “Nauka/Interperiodica” 2006

Authors and Affiliations

  1. 1.Timiryazev Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia

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