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Planta

, Volume 198, Issue 4, pp 526–531 | Cite as

Changes in intracellular amino acids and organic acids induced by nitrogen starvation and nitrate or ammonium resupply in the cyanobacterium Phormidium laminosum

  • María I. Tapia
  • Jesús A. G. Ochoa de Alda
  • María J. Llama
  • Juan L. SerraEmail author
Article

Abstract

In Phormidium laminosum cells, nitrogen starvation caused a decrease in the intracellular levels of all amino acids, except glutamate, and an increase in the total level of the analyzed organic acids. The addition of nitrate or ammonium to N-starved cells resulted in substantial increases in the pool size of most amino acids. Upon addition of ammonium the total level of organic acids diminished, whereas it increased upon addition of nitrate, after a transient decay during the first minutes. Nitrogen resupply stimulated amino acid synthesis, the effect being faster and higher when ammonium was assimilated. The data indicate that nitrate and ammonium assimilation induced an enhancement of carbon flow through the glycolytic and the tricarboxylic-acid pathways to amino acid biosynthesis, with a concurrent decrease in the carbohydrate reserves. The results suggest that the availability of carbon skeletons limited the rate of ammonium assimilation, whereas the availability of reducing equivalents limited the rate of nitrate assimilation.

Key words

Ammonium assimilation Carbon-nitrogen interactions Cyanobacteria Nitrate assimilation Nitrogen starvation Phormidium 

Abbreviations

Chl

chlorophyll

GOGAT

ferredoxin-dependent glutamate synthase (EC 1.4.7.1)

GS

glutamine synthetase (EC 6.3.1.2)

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References

  1. Allen MM, Law A, Evans EH (1990) Control of photosynthesis during nitrogen depletion and recovery in a non-nitrogen-fixing cyanobacterium. Arch Microbiol 153: 428–431CrossRefGoogle Scholar
  2. Arizmendi JM, Fresnedo O, Martnez-Bilbao M, Alaña A, Serra JL (1987) Inorganic nitrogen assimilation in the non-N2-fixing cyanobacterium Phormidium laminosum. II. Effect of the nitrogen source on the nitrite reductase levels. Physiol Plant 70: 703–707CrossRefGoogle Scholar
  3. Bassham JA, Larsen PO, Lawyer AL, Cornwell KL (1981) Relationships between nitrogen metabolism and photosynthesis. In: Bewley JD (ed) Nitrogen and carbon metabolism. M Nijhoff-Dr Junk, The Hague, pp 135–163CrossRefGoogle Scholar
  4. Buchanan BB (1992) Carbon dioxide assimilation in oxygenic and anoxygenic photosynthesis. Photosynth Res 33: 147–162CrossRefPubMedGoogle Scholar
  5. Castenholz RW (1970) Laboratory culture of thermophilic cyanophytes. Schweiz Z Hydrol 32: 538–551Google Scholar
  6. Coronil T, Lara C, Guerrero MG (1993) Shift in carbon flow and stimulation of amino-acid turnover induced by nitrate and ammonium in Anacystis nidulans. Planta 189: 461–467CrossRefPubMedGoogle Scholar
  7. Elrifi IR, Turpin DH (1986) Nitrate and ammonium induced photosynthetic suppression in N-limited Selenastrum minutum. Plant Physiol 81: 273–279CrossRefPubMedPubMedCentralGoogle Scholar
  8. Flores E, Ramos JL, Herrero A, Guerrero MG (1983) Nitrate assimilation by cyanobacteria. In: Papageorgiu G, Packer L (eds) Photosynthetic prokaryotes: cell differentiation and function. Elsevier/North Holland, New York, pp 363–387Google Scholar
  9. Fresnedo O, Serra JL (1992) Effect of nitrogen starvation on the biochemistry of Phormidium laminosum (Cyanophyceae). J Phycol 28: 786–793CrossRefGoogle Scholar
  10. Garbisu C, Hall DO, Serra JL (1992) Nitrate and nitrite uptake by free-living and immobilized N-starved cells of Phormidium laminosum. J Appl Phycol 4: 139–148CrossRefGoogle Scholar
  11. García-González M, Sivak MN, Guerrero MG, 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: 360–364CrossRefGoogle Scholar
  12. Huppe HC, Turpin DH (1994) Integration of carbon and nitrogen metabolism in plant and algal cells. Annu Rev Plant Physiol Plant Mol Biol 45: 577–607CrossRefGoogle Scholar
  13. Huppe HC, Vanlerberghe GC, Turpin DH (1992) Evidence for activation of the oxidative pentose phosphate pathway during photosynthetic assimilation of NO3 but not NH4+ by a green alga. Plant Physiol 100: 2096–2099CrossRefPubMedPubMedCentralGoogle Scholar
  14. Lara C (1992) Photosynthetic nitrate assimilation: Interactions with CO2 fixation. In: Barber J, Medrano H, Guerrero MG (eds) Trends in photosynthesis research. Intercept, London, pp 195–208Google Scholar
  15. Lara C, Romero JM, Coronil T, Guerrero MG (1987) Interactions between photosynthetic nitrate assimilation and CO2 fixation in cyanobacteria. In: Ullrich WR, Aparicio PJ, Syrett PJ, Castillo F (eds) Inorganic nitrogen metabolism. Springer-Verlag, Berlin, pp 45–52CrossRefGoogle Scholar
  16. Lawrie AC, Codd GA, Stewart WDP (1976) The incorporation of nitrogen into products of recent photosynthesis in Anabaena cylindrica Lemm. Arch Microbiol 107: 15–24CrossRefPubMedGoogle Scholar
  17. MacKinney G (1941) Absorption of light by chlorophyll solutions. J Biol Chem 140: 315–322Google Scholar
  18. Ochoa de Alda JAG, Tapia MI, Llama MJ, Serra JL (1996) Bioenergetic processes are modified during nitrogen starvation and recovery in Phormidium laminosum (Cyanophyceae). J Phycol: in pressGoogle Scholar
  19. Ohmori M, Satoh Y, Urata K (1989) Light-induced accumulation of lactate and succinate in Anabaena cylindrica. Arch Microbiol 151: 101–104CrossRefGoogle Scholar
  20. Peterson GL (1983) Determination of total protein. Methods Enzymol 91:95–119CrossRefPubMedGoogle Scholar
  21. Romero JM, Lara C (1987) Photosynthetic assimilation of NO3 by intact cells of the cyanobacterium Anacystis nidulans. Influence of NO3 and NH4+ assimilation on CO2 fixation. Plant Physiol 83: 208–212CrossRefPubMedPubMedCentralGoogle Scholar
  22. Romero JM, Lara C, Guerrero MG (1985) Dependence of nitrate utilization upon active CO2 fixation in Anacystis nidulans: A regulatory aspect of the interaction between photosynthetic carbon and nitrogen metabolism. Arch Biochem Biophys 237: 396–401CrossRefPubMedGoogle Scholar
  23. Rowell P, Simpson GG (1990) Regulation of cyanobacterial glucose-6-phosphate dehydrogenase by thioredoxin and amino acids. In: Ullrich WR, Rigano C, Fuggi A (eds) Inorganic nitrogen metabolism in plants and microorganisms. Uptake and metabolism. Springer-Verlag, Heidelberg, pp 137–144CrossRefGoogle Scholar
  24. Rowell P, Enticott S, Stewart WDP (1977) Glutamine synthetase and nitrogenase activity in the blue-green alga Anabaena cylindrica. New Phytol 79: 41–54CrossRefGoogle Scholar
  25. Smith AJ (1982) Modes of cyanobacterial carbon metabolism. In: Carr NG, Whitton BA (eds) The biology of cyanobacteria. Blackwell Scientific Publications, Oxford, pp 47–86Google Scholar
  26. Smith RG, Vanlerberghe GC, Stitt M, Turpin DH (1989) Short-term metabolite changes during transient ammonium assimilation by the N-limited green alga Selenastrum minutum. Plant Physiol 91: 749–755CrossRefPubMedPubMedCentralGoogle Scholar
  27. Tapia MI, Llama MJ, Serra JL (1995a) Regulation of nitrate assimilation in the cyanobacterium Phormidium laminosum. Planta 198: 24–30Google Scholar
  28. Tapia MI, Ochoa de Alda JAG, Llama MJ, Serra JL (1995b) Determination of 2-oxoglutarate in the presence of citrate and/or isocitrate after ion-exclusion high-performance liquid chromatography. Anal Lett 28: 1959–1971CrossRefGoogle Scholar
  29. Weger H, Turpin DH (1989) Mitochondrial respiration can support NO3 and NO2 reduction during photosynthesis. Plant Physiol 89: 409–415CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • María I. Tapia
    • 1
  • Jesús A. G. Ochoa de Alda
    • 1
  • María J. Llama
    • 1
  • Juan L. Serra
    • 1
    Email author
  1. 1.Departamento de Bioquímica y Biología Molecular, Facultad de CienciasUniversidad del País VascoBilbaoSpain

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