1887

Abstract

Cyanobacteria can utilize nitrate or ammonium as a source of fixed nitrogen for cell growth. In the filamentous sp. strain PCC 7601, these two sources of nitrogen differently influenced the phycobiliprotein composition of the phycobilisomes, the major light-harvesting antennae. When compared to nitrate, growth in the presence of ammonium resulted in intracellular steadystate levels 35% lower for phycoerythrin and 46% higher for phycocyanin. Besides these differences in cell pigmentation, a rapid but transient accumulation of cyanophycin granule polypeptide occurred in ammoniumgrown cells, while these macromolecules were not detected in cells grown with nitrate. In contrast, glycogen reserves displayed a dynamic pattern of accumulation and disappearance during cell growth which varied only slightly with the nitrogen source. The observed changes in cell pigmentation are reminiscent of the phenomenon of complementary chromatic adaptation, in which green and red wavelengths promote the syntheses of phycoerythrin and phycocyanin-2, respectively. As in complementary chromatic adaptation, the regulation of synthesis of phycoerythrin and phycocyanin-2 by the nitrogen source occurred mainly at the mRNA level. Moreover, the transcriptional start sites for the expression of the and the operons, which respectively encode the two subunits of phycoerythrin and phycocyanin-2, were the same in cells grown in nitrate or ammonium, and identical to those in green-and red-light-grown cells. The results of this study suggest that acclimation to the spectral light quality and to the nitrogen source share some common regulatory elements.

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1996-03-01
2024-12-12
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References

  1. Abeliovich A., Azov Y. 1976; Toxicity of ammonia to algae in sewage oxidation ponds. Appl Environ Microbiol 31:801–806
    [Google Scholar]
  2. Allen M. M. 1984; Cyanobacterial cell inclusions. Annu Rev Microbiol 38:1–25
    [Google Scholar]
  3. Allen M. M., Hutchison F. 1980; Nitrogen limitation and recovery in the cyanobacterium Aphanocapsa 6308. Arch Microbiol 128:1–7
    [Google Scholar]
  4. Allen M. M., Smith A. J. 1969; Nitrogen chlorosis in bluegreen algae. Arch Mikrobiol 69:114–120
    [Google Scholar]
  5. Allen M. M., Weathers P. J. 1980; Structure and composition of cyanophycin granules in the cyanobacterium Aphanocapsa 6308. J Bacterial 141:959–962
    [Google Scholar]
  6. Allen M. M., Hutchison F., Weathers P. J. 1980; Cyanophycin granule polypeptide formation and degradation in the cyanobacterium Aphanocapsa 6308. J Bacterial 141:687–693
    [Google Scholar]
  7. Beale S. I. 1994; Biosynthesis of Cyanobacterial tetrapyrrole pigments : hemes, chlorophylls, and phycobilins. In Fhe Molecular Biologf of Cyanobacteria519–558 Bryant D. A. Dordrecht: Kluwer;
    [Google Scholar]
  8. Boussiba S., Gibson J. 1991; Ammonia translocation in cyanobacteria. FEMS Microbiol Rev 88:1–14
    [Google Scholar]
  9. Boussiba S., Richmond A. E. 1980; C-phycocyanin as a storage protein in the blue-green alga Spirulina platensis. Arch Microbiol 125:143–147
    [Google Scholar]
  10. Boussiba S., Resch C. M., Gibson J. 1984; Ammonia uptake and retention in some cyanobacteria. Arch Microbiol 138:287–292
    [Google Scholar]
  11. Bryant D. A. 1987; The Cyanobacterial photosynthetic apparatus : comparison of those of higher plants and photosynthetic bacteria. In Photosynthetic Picoplankton (Can Bull Fish Aquat Sci 214:423–500 Platt T., Li W. K. W.
    [Google Scholar]
  12. Bryant D. A. 1991; Cyanobacterial phycobilisomes : progress toward complete structural and functional analysis via molecular genetics. In Cell Culture and Somatic Cell Genetics of Plants. 7B The Photosynthetic Apparatus: Molecular Biology and Operation257–300 Bogorad L., Vasil I. K. New York: Academic Press;
    [Google Scholar]
  13. Bryant D. A., Cohen-Bazire G. 1981; Effects of chromatic illumination on Cyanobacterial phycobilisomes. Evidence for the specific induction of a second pair of phycocyanin subunits in Pseudanabaena 7409 grown in red light. Eur J Biochem 119:415–424
    [Google Scholar]
  14. Campbell D. 1994; Relations entre l’environnement, le metabolisme intermediaire et la differenciation cellulaire chez une cyano-bacterie filamenteuse. Bull Inst Pasteur 92:27–43
    [Google Scholar]
  15. Campbell D., Houmard J., Tandeau de Marsac N. 1993; Electron transport regulates cellular differentiation in the filamentous cyanobacterium Calothrix. Plant Cell 5:451–463
    [Google Scholar]
  16. Carr N. G. 1988; Nitrogen reserves and dynamic reservoirs in cyanobacteria. In Biochemistry of the Algae and CyanobacteriaAnnual Proceedings of the Phytochemical Society of Europe’13–21 Rogers L. J., Gallon J. R. Oxford: Clarendon Press;
    [Google Scholar]
  17. Collier J. L., Grossman A. R. 1992; Chlorosis induced by nutrient deprivation in Synechococcus sp. strain PCC 7942: not all bleaching is the same. J Bacterial 174:4718–4726
    [Google Scholar]
  18. Collier J. L., Grossman A. R. 1994; A small polypeptide triggers complete degradation of light-harvesting phycobiliproteins in nutrient-deprived cyanobacteria. EMBO J 13:1039–1047
    [Google Scholar]
  19. Conley P. B., Lemaux P. G., Lomax T. L., Grossman A. R. 1986; Genes encoding major light-harvesting polypeptides are clustered on the genome of the cyanobacterium Fremyella diplosiphon. Proc Natl Acad SciUSA 833924–3928
    [Google Scholar]
  20. Conley P. B., Lemaux P. G., Grossman A. 1988; Molecular characterization and evolution of sequences encoding light-harvesting components in the chromatically adapting cyanobacterium Fremyella diplosiphon. J Mol Biol 199:447–465
    [Google Scholar]
  21. Coronil T., Lara C., Guerrero M. G. 1993; Shift in carbon flow and stimulation of amino-acid turnover induced by nitrate and ammonium assimilation in Anacystis nidulans. Planta 189:461–467
    [Google Scholar]
  22. De Lorimier R. M., Smith R. L., Stevens S. E. Jr 1992; Regulation of phycobilisome structure and gene expression by light intensity. Plant Physiol 95:1003–1010
    [Google Scholar]
  23. De Philippis R., Sili C., Vincenzini M. 1992; Glycogen and poly-β-hydroxy butyrate synthesis in Spirulina maxima. J Gen Microbiol 138:1623–1628
    [Google Scholar]
  24. Ernst A., Böger P. 1985; Glycogen accumulation and the induction of nitrogenase activity in the heterocyst-forming cyanobacterium Anabaena variabilis. J Gen Microbiol 131:3147–3153
    [Google Scholar]
  25. Ernst A., Kirschenlohr H., Diez J., Böger P. 1984; Glycogen content and nitrogenase activity in Anabaena variabilis. Arch Microbiol 140:120–125
    [Google Scholar]
  26. Erokhina L. G. 1992; Spectral effects of chromatic adaptation of nitrogen-fixing cyanobacteria growing on different nitrogen sources. Microbiology (English translation of Mikrobiologiya) 61:673–679
    [Google Scholar]
  27. van Eykelenburg C. 1980; Ecophysiological studies on Spirulina platensis. Effect of temperature, light intensity and nitrate concentration on growth and ultrastructure. Antonie Leeuwenhoek 46:113–127
    [Google Scholar]
  28. Fay P. 1992; Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol Rev 56:340–373
    [Google Scholar]
  29. Federspiel N. A., Grossman A. R. 1990; Characterization of the light-regulated operon encoding the phycoerythrin-associated linker proteins from the cyanobacterium Fremyella diplosiphon. J Bacteriol 172:4072–4081
    [Google Scholar]
  30. Flores E., Herrero A. 1994; Assimilatory nitrogen metabolism and its regulation. In The Molecular Biology of Cyanobacteria487–517 Bryant D. A. Dordrecht: Kluwer;
    [Google Scholar]
  31. García-González M., Sivak M. N., Guerrero M. G., Preiss J., Lara C. 1992; Depression of carbon flow to the glycogen pool induced by nitrogen assimilation in intact cells of Anacystis nidulans. Physiol Plant 86:360–364
    [Google Scholar]
  32. Glazer A. N. 1989; Light guides: directional energy transfer in a photosynthetic antenna. J Biol Chem 264:1–4
    [Google Scholar]
  33. Golden S. S., Brusslan J., Haselkorn R. 1986; Expression of a family of psbA genes encoding a photosystem II polypeptide in the cyanobacterium Anacystis nidulans R2. EMBO J 5:2789–2798
    [Google Scholar]
  34. Grossman A. R., Schaefer M., Chiang G. G., Collier J. L. 1993; The phycobilisome, a light-harvesting complex responsive to environmental conditions. Microbiol Rev 57:725–749
    [Google Scholar]
  35. Guerrero M. G., Lara C. 1987; Assimilation of inorganic nitrogen. In The Cyanobacteria163–186 Fay P., Van Baalen C. Amsterdam: Elsevier;
    [Google Scholar]
  36. Houmard J., Capuano V., Coursin T., Tandeau de Marsac N. 1988; Genes encoding core components of the phycobilisome in the cyanobacterium Calothrix sp. strain PCC 7601 : occurrence of a multigene family. J Bacteriol 170:5512–5521
    [Google Scholar]
  37. Kallas T., Coursin T., Rippka R. 1985; Different organization of nif genes in nonheterocystous and heterocystous cyanobacteria. Plant Mol Biol 5:321–329
    [Google Scholar]
  38. Lawry N. H., Simon R. D. 1982; The normal and induced occurrence of cyanophycin inclusion bodies in several blue-green algae. J Phycol 18:391–399
    [Google Scholar]
  39. Lehmann M., Wöber G. 1976; Accumulation, mobilization and turn-over of glycogen in the blue-green bacterium Anacystis nidulans. Arch Microbiol 111:93–97
    [Google Scholar]
  40. Mackerras A. H., de Chazal N. M., Smith G. D. 1990; Transient accumulations of cyanophycin in Anabaena cylindrica and Synechocystis 6308. J Gen Microbiol 136:2057–2065
    [Google Scholar]
  41. Martín-Nieto J., Herrero A., Flores E. 1989; Regulation of nitrate and nitrite reductases in dinitrogen-fixing cyanobacteria and Nifs mutants. Arch Microbiol 151:475–478
    [Google Scholar]
  42. Mazel D., Guglielmi G., Houmard J., Sidler W., Bryant D. A., Tandeau de Marsac N. 1986; Green light induces transcription of the phycoerythrin operon in the cyanobacterium Calothrix 7601. Nucleic Acids Res 14:8279–8290
    [Google Scholar]
  43. Ohmori M., Ohmori K. 1990; Ammonium-nitrogen partitioning under different balances of nitrogen and carbon in the cyanobacterium Anabaena cylindrica. J Gen Appl Microbiol 36:171–177
    [Google Scholar]
  44. Rippka R., Stanier R. Y. 1978; The effects of anaerobiosis on nitrogenase synthesis and heterocyst development by nostocacean cyanobacteria. J Gen Microbiol 105:83–94
    [Google Scholar]
  45. Rippka R., Deruelles J., Waterbury J. B., Herdman M., Stanier R. Y. 1979; Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61
    [Google Scholar]
  46. Romero J. M., Lara C. 1987; Photosynthetic assimilation of by intact cells of the cyanobacterium Anacystis nidulans. Influence of and assimilation on CO2 fixation. Plant Physiol 83:208–212
    [Google Scholar]
  47. Schyns G., Sobczyk A., Tandeau de Marsac N., Houmard J. 1994; Specific initiation of transcription at a Cyanobacterial promoter with RNA polymerase purified from Calothrix sp. PCC 7601. MolMicrobiol 13:887–896
    [Google Scholar]
  48. Simon R. D. 1971; Cyanophycin granules from the blue-green alga Anabaena cylindrica: a reserve material consisting of copolymers of aspartic acid and arginine. Proc Natl Acad SciUSA 68265–267
    [Google Scholar]
  49. Simon R. D. 1973a; The effect of chloramphenicol on the production of cyanophycin granule polypeptide in the blue-green alga Anabaena cylindrica. Arch Mikrobiol 92:115–122
    [Google Scholar]
  50. Simon R. D. 1973b; Measurement of the cyanophycin granule polypeptide contained in the blue-green alga Anabaena cylindrica. J Bacterial 114:1213–1216
    [Google Scholar]
  51. Simon R. D. 1976; The biosynthesis of multi-L-arginyl-poly(L-aspartic acid) in the filamentous cyanobacterium Anabaena cylindrica. Biochim Biophys Acta 422:407–418
    [Google Scholar]
  52. Smith A. J. 1982; Modes of Cyanobacterial carbon metabolism. In The Biology of Cyanobacteria (Botanical Monographs 1947–85 Carr N. G., Whitton B. A. Oxford: Blackwell Scientific Publications;
    [Google Scholar]
  53. Sobczyk A., Schyns G., Tandeau de Marsac N., Houmard J. 1993; Transduction of the light signal during complementary chromatic adaptation in the cyanobacterium Calothrix sp. PCC 7601 : DNA-binding proteins and modulation by phosphorylation. EMBO J 12:997–1004
    [Google Scholar]
  54. Sobczyk A., Bely A., Tandeau de Marsac N., Houmard J. 1994; A phosphorylated DNA-binding protein is specific for the red-light signal during complementary chromatic adaptation in cyanobacteria. Mol Microbiol 13:875–885
    [Google Scholar]
  55. Tandeau de Marsac N., Houmard J. 1988; Complementary chromatic adaptation : physiological conditions and action spectra. Methods Enzymol 167:318–328
    [Google Scholar]
  56. Tandeau de Marsac N., Houmard J. 1993; Adaptation of cyanobacteria to environmental stimuli: new steps towards molecular mechanisms. FEMS Microbiol Rer 104:119–190
    [Google Scholar]
  57. Tandeau de Marsac N., Mazel D., Damerval T., Guglielmi G., Capuano V., Houmard J. 1988; Photoregulation of gene expression in the filamentous cyanobacterium Calothrix sp. PCC 7601 : light-harvesting complexes and cell differentiation. Photosynth Res 18:99–132
    [Google Scholar]
  58. Vioque A. 1992; Analysis of the gene encoding the RNA subunit of ribonuclease P from cyanobacteria. Nucleic Acids Res 20:6331–6337
    [Google Scholar]
  59. Wyman M., Gregory R. P. F., Carr N. G. 1985; Novel role for phycoerythrin in a marine cyanobacterium, Synechococcus strain DC2. Science 230:818–820
    [Google Scholar]
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