Archives of Microbiology

, Volume 159, Issue 6, pp 506–511 | Cite as

Ornithine cycle in Nostoc PCC 73102. Arginase, OCT and arginine deiminase, and the effects of addition of external arginine, ornithine, or citrulline

  • Antera Martel
  • Eva Jansson
  • Guillermo García-Reina
  • Peter Lindblad
Original Papers


Arginase, ornithine carbamoyl transferase (OCT) and arginine deiminase activities were found in cell-free extracts of Nostoc PCC 73102, a free-living cyanobacterium originally isolated from the cycad Macrozamia. Addition of either arginine, ornithine or citrulline to the growth medium induced significant changes in their in vitro activities. Moreover, growth in darkness, compared to in light, induced higher in vitro activities. The in vitro activities of arginase and arginine deiminase, two catabolic enzymes primarily involved in the breakdown of arginine, increased substantially by a combination of growth in darkness and addition of either arginine, or ornithine, to the growth medium. The most significant effects on the in vitro OCT activities where observed in cells grown with the addition of ornithine. Cells grown in darkness exhibited about 6% of the in vivo nitrogenase activity observed in cells grown in light. However, addition of external carbon (glucose and fructose) to cells grown in darkness resulted in in vivo nitrogenase activity levels similar to, or even higher than, cells grown in light. Growth with high in vivo nitrogenase activity or in darkness with the addition of external carbon, resulted in repressed levels of in vitro arginase and arginine deiminase activities. It is suggested that nitrogen starvation induces a mobilization of the stored nitrogen, internal release of the amino compound arginine, and an induction of two catabolic enzymes arginase and arginine deiminase. A similar and even more pronunced induction can be observed by addition of external arginine to the growth medium.

Key words

Arginase Arginine deiminase Cyanobacterium Nitrogenase activity Nostoc Ornithine carbamoyl transferase 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Allen MM (1988) Inclusions: cyanophycin. In: Packer L, Glazer AN (eds) Cyanobacteria. (Methods in enzymology, vol 167) Academic Press, San Diego, pp 207–213Google Scholar
  2. Archibald RM (1944) Colorimetric determination of urea. J Biol Chem 157: 507–518Google Scholar
  3. Bednarz J, Schmid GH (1991) Induction of nitrate reductase activity by arginine in the filamentous cyanobacterium Oscillatoria chalybea. Z Naturforsch [C] 46: 591–596CrossRefGoogle Scholar
  4. Bottomley PL, Stewart WDP (1977) ATP and nitrogenase activity in nitrogen-fixing heterocystous blue-green algae. New Phytol 79: 625–638CrossRefGoogle Scholar
  5. Boyde TRC, Rahmatullah M (1980) Optimization of conditions for the colorimetric determination of citrulline, using diacetyl monoxime. Anal Biochem 107: 424–431CrossRefGoogle Scholar
  6. Carr NG (1983) Biochemical aspects of heterocyst differentiation and function. In: Papageorgiou GC, Packer L (eds) Photosynthetic procaryotes: cell differentiation and functions. Elsevier, Amsterdam, pp 265–280Google Scholar
  7. Fay P (1992) Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol Rev 56: 340–373PubMedPubMedCentralGoogle Scholar
  8. Guerrero MG, Lara C (1987) Assimilation of inorganic nitrogen. In: Fay P, Van Baalen C (eds) The cyanobacteria. Elsevier, Amsterdam, New York, pp 163–186Google Scholar
  9. Gupta M, Carr NG (1981a) Enzymology of arginine metabolism in heterocyst-forming cyanobacteria. FEMS Microbiol Lett 12: 179–181CrossRefGoogle Scholar
  10. Gupta M, Carr NG (1981b) Enzyme activities related to cyanophycin metabolism in heterocysts and vegetative cells of Anabaena spp. J Gen Microbiol 125: 17–23Google Scholar
  11. Harborne JB (1973) Recommended techniques, chlorophyll estimation. In: Harborne JB eds., Phytochemical methods. Chapman & Hall, London, pp 205–207Google Scholar
  12. Haselkorn R, Buikema W (1992) Nitrogen fixation in cyanobacteria. In: Stacey G, Burris RH, Evans HJ (eds) Biological nitrogen fixation. Chapman & Hall, New York, pp 166–190Google Scholar
  13. Holm-Hansen O, Brown GW (1963) Ornithine cycle enzymes in the blue-green alga Nostoc muscorum. Plant Cell Physiol 4: 299–306Google Scholar
  14. Hood W, Carr NG (1971) Apparent lack of control by repression of arginine metabolism in blue-green algae. J Bacteriol 107: 365–367PubMedPubMedCentralGoogle Scholar
  15. Hood W, Leaver AG, Carr NG (1969) Extracellular nitrogen and the control of arginine biosynthesis in Anabaena variabilis. Biochem J 114: 12–13CrossRefGoogle Scholar
  16. Houchins JP (1985) Electron transfer chains of cyanobacterial heterocysts. In: Ludden PW, Burris RH (eds) Nitrogen fixation and CO2 metabolism. Elsevier, New York, pp 261–268Google Scholar
  17. Jansson E, Martel A, Lindblad P (1993) Ornithine cycle in Nostoc PCC 73102. Stimulation of in vitro ornithine carbamoyl transferase activity by addition of arginine. Curr Microbiol 26: 75–78CrossRefGoogle Scholar
  18. Lehninger AL (1982) Principles of biochemistry. Worth, New YorkGoogle Scholar
  19. Lindblad P (1989) Immunocytochemical localization of carbamyl phosphate synthetase in the filamentous heterocystous cyanobacterium Nostoc PCC 73102. Protoplasma 152: 87–95CrossRefGoogle Scholar
  20. Lindblad P (1992) Ornithine cycle in Nostoc PCC 73102. Occurrence and localization of ornithine carbamoyl transferase and the effects of external carbon and ornithine on nitrogenase activity and citrulline synthesis. Physiol Plant 84: 275–282CrossRefGoogle Scholar
  21. Lindblad P, Bergman B (1986) Glutamine synthetases: activity and localization in cyanobacteria of the cycads Cycas revoluta and Zamia skinneri. Planta 169: 1–7CrossRefGoogle Scholar
  22. Lindblad P, Guerrero MG (1993) Nitrogen fixation and nitrate reduction. In: Hall DO, Scurlock JMO, Bolhàr-Nordenkampf HR, Leegood RC, Long SP (eds) Photosynthesis and production in a changing environment. A field and laboratory guide. Chapman & Hall, London, pp 299–312Google Scholar
  23. Mackerras AH, Younes BN, Weir RC, Smith GD (1990a) Is cyanophycin involved in the integration of nitrogen and carbon metabolism in cyanobacteria Anabaena cylindrica and Gloeothece grown on light/dark cycles? J Gen Microbiol 136: 2049–2056CrossRefGoogle Scholar
  24. Mackerras AG, De Chazal NM, Smith GD (1990b) Transient accumulations of cyanophycin in Anabaena cylindrica and Synechocystis 6308. J Gen Microbiol 136: 2057–2065CrossRefGoogle Scholar
  25. 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: 171–177CrossRefGoogle Scholar
  26. Peterson GL (1983) Determination of total protein. Methods Enzymol 91: 95–119CrossRefGoogle Scholar
  27. Postgate JR (1987) Nitrogen fixation, 2nd edn. Edward Arnold, LondonGoogle Scholar
  28. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Generic assignment, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111: 1–61Google Scholar
  29. Schubert KR, Boland MJ (1990) The ureides. In: Miflin BJ, Lea PJ (eds) The biochemistry of plants. A comprehensive treatise, vol 16. Academic Press, San Diego, pp 197–282Google Scholar
  30. Simon RD (1976) The biosynthesis of multi-l-arginyl poly(l-aspartic acid) in the filamentous cyanobacterium Anabaena cylindrica. Biochim Biophys Acta 422: 407–418CrossRefGoogle Scholar
  31. Sprent JI, Sprent P (1990) Nitrogen fixing organisms. Pure and applied aspects. Chapman & Hall, London Cambridge University Press, CambridgeCrossRefGoogle Scholar
  32. Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bact Rev 35: 171–205PubMedGoogle Scholar
  33. Steinberg NA, Meeks JC (1991) Physiological sources of reductant for nitrogen fixation activity in Nostoc sp. strain UCD 7801 in symbiotic association with Anthoceros punctatus. J Bacteriol 173: 7324–7329CrossRefGoogle Scholar
  34. Stewart WDP, Haystead A, Dharmawardene MWN (1975) Nitrogen assimilation and metabolism in blue-green algae. In: Stewart WDP (ed) Nitrogen fixation in free-living microorganisms. Cambridge University Press, Cambridge, pp 129–158Google Scholar
  35. Tel-Or E, Stewart WDP (1977) Photosynthetic components and activities of nitrogen-fixing isolated heterocysts of Anabaena cylindrica. Proc R Soc Lond [Biol] 198: 61–87CrossRefGoogle Scholar
  36. Weathers PJ, Chee HL, Allen MM (1978) Arginine catabolism in Aphanocapsa 6308. Arch Microbiol 118: 1–6CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • Antera Martel
    • 1
    • 2
  • Eva Jansson
    • 1
  • Guillermo García-Reina
    • 2
  • Peter Lindblad
    • 1
  1. 1.Department of Physiological BotanyUppsala UniversityUppsalaSweden
  2. 2.Institute of Applied AlgologyUniversity of Las PalmasLas Palmas, Gran CanariaSpain

Personalised recommendations