Skip to main content

Relationship between nitrogen fixation and nitrate metabolism in the Nodularia strains M1 and M2

Abstract

Nitrogen fixation and nitrate-reduction activities were determined in photoautotrophic cultures of two wild-type strains of cyanobacterium Nodularia, spp. M1 and M2. Air could support growth of the two strains at a similar rate in the presence or absence of exogenous nitrate, ammonium and/or bicarbonate. Nitrogenase activity in air-grown cultures varied with culture age, and totally disappeared after 6 h of darkness. Recovery took place upon culture re-illumination. Ammonium at a concentration of 1 mM resulted in the total disappearance of nitrogenase activity and of heterocysts. In contrast, 20 mM nitrate hardly affected nitrogenase activity and heterocyst formation after ten generations. Under the same conditions, either ammonium or nitrate completely abolished nitrogenase activity and heterocyst formation in Anabaena sp. PCC 7119, a typical heterocystous strain. The inefficiency of nitrate in inhibiting nitrogen fixation in Nodularia M1 and M2 seemed to be caused by a low nitrate-reductase activity, and not by an impairment of nitrate-uptake activity. On the other hand, the presence of nitrate was not required for uptake activity to be expressed in Nodularia.

This is a preview of subscription content, access via your institution.

Abbreviations

NR:

nitrate reductase

References

  • Allen, M.M., Arnon, D. (1955) Studies on nitrogen fixing blue-green algae. II. The sodium requirement of Anabaena cylindrica. Physiol. Plant. 8, 653–660

    Google Scholar 

  • Bagchi, S.N., Singh, H.N. (1984) Genetic control of nitrate reduction in the cyanobacterium Nostoc muscorum. Mol. Gen. Genet. 193, 82–84

    Google Scholar 

  • Böhme, H. (1986) Inhibition of nitrogen fixation by nitrite in Anabaena variabilis. Arch. Microbiol. 146, 99–103

    Google Scholar 

  • Bothe, H. (1982) Nitrogen fixation. In The biology of cyanobacteria, pp. 87–104, Carr, N.G., Whitton, B.A., eds. Blackwell Scientific Publications, Oxford

    Google Scholar 

  • Bottomley, P.J., Stewart, W.D.P. (1977) ATP and nitrogenase activity in nitrogen-fixing heterocystous blue-green algae. New Phytol. 9, 625–638

    Google Scholar 

  • Bottomley, P.J., Grillo, J.F., Van Baalen, C., Tabita F.R. (1979) Synthesis of nitrogenase and heterocysts by Anabaena sp. CA in the presence of high levels of ammonia. J. Bacteriol. 140, 938–943

    Google Scholar 

  • Cawse, P.A. (1967) The determination of nitrate in soil solutions by ultraviolet spectrophotometry. Analyst 92, 311–315

    Article  CAS  Google Scholar 

  • Codd, G.A., Poon, G.K. (1988) Cyanobacterial toxins. In Biochemistry of the algae and cyanobacteria, pp. 283–297, Rogers, L.J., Gallon, J.R., eds. Clarendon Press, Oxford

    Google Scholar 

  • Codd, G.A., Edwards, C., Beattle, K.A., Barr, W.M., Gunn, G.J. (1992) Fatal attraction to cyanobacteria? Nature 359, 110–111

    Google Scholar 

  • Del Campo, F.F., Sanz-Alférez, S., Real-Valcárcel, M., Pérez-Silva, G. (1988) Is Nodularia nitrogenase controlled by nitrate? In VI International symposium on photosynthetic prokaryotes, p. 125, Mur, L.R., Burger-Wiersma, T., eds. Noordwijkerhout, The Netherlands

    Google Scholar 

  • Flores, E., Guerrero, M.G., Losada, M. (1983) Photosynthetic nature of nitrate uptake and reduction in the cyanobacterium Anacystis nidulans. Biochim. Biophys. Acta 722, 408–416

    Google Scholar 

  • Gallon, J.R., Chaplin, A.E. (1988) Nitrogen fixation. In Biochemistry of the algae and cyanobacteria, pp. 147–173, Rogers, L.J., Gallon, J.R., eds. Clarendon Press, Oxford

    Google Scholar 

  • Guerrero, M.G., Lara, C. (1987) Assimilation of inorganic nitrogen. In: The cyanobacteria, pp. 163–186, Fay, P., Van Baalen, C., eds. Elsevier Science Publishers, Amsterdam

    Google Scholar 

  • Hattori, A. (1962) Adaptive formation of nitrate reducing system in Anabaena cylindrica. Plant Cell Physiol. 3, 371–377

    Google Scholar 

  • Herrero, A., Flores, E., Guerrero, M.G. (1981) Regulation of nitrate reductase levels in the cyanobacteria Anacystis nidulans, Anabaena sp. strain 7119, and Nostoc sp. strain 6719. J. Bacteriol. 145, 175–180

    Google Scholar 

  • Herrero, A., Flores, E., Guerrero, M.G. (1985) Regulation of nitrate reductase cellular levels in the cyanobacteria Anabaena variabilis and Synechocystis sp. FEMS Microbiol. Lett. 26, 21–25

    Google Scholar 

  • Lowry, O.H., Rosebrough, N.J., Farr, A.L., Randall, R.J. (1951) Protein measurement with the folin phenol reagent. J. Biol. Chem. 193, 265–275

    CAS  PubMed  Google Scholar 

  • Marker, A.F.M. (1972) The use of acetone and methanol in the estimation of chlorophyll in the presence of phaeophytin. Freshwater Biol. 2, 361–385

    Google Scholar 

  • Martín-Nieto, J., Herrero, A., Flores, E. (1989) Regulation of nitrate and nitrite reductases in dinitrogen-fixing cyanobacteria and Nif mutants. Arch. Microbiol. 151, 475–478

    Google Scholar 

  • Martín-Nieto, J., Flores, E., Herrero, A. (1992) Biphasic kinetic behavior of nitrate reductase from heterocystous, nitrogen-fixing cyanobacteria. Plant Physiol. 100, 157–163

    Google Scholar 

  • Meeks, J.C., Wycoff, K.L., Chapman, J.S., Enderlin, C.S. (1983) Regulation of expression of nitrate and dinitrogen assimilation by Anabaena species. App. Environ. Microbiol. 45, 1351–1359

    Google Scholar 

  • Ohmori, K., Hattori, A. (1970) Induction of nitrate and nitrite reductases in Anabaena cylindrica. Plant Cell Physiol. 11, 873–878

    Google Scholar 

  • Ohmori, K., Hattori, A. (1972) Effect of nitrate on nitrogen fixation by the blue-green alga Anabaena cylindrica. Plant Cell Physiol. 13, 589–599

    Google Scholar 

  • Pandey, K.D., Singh, P.K. (1984) Isolation and characterisation of nitrate reductase mutants and regulation of nitrate reductase and nitrogenase in the cyanobacterium Nostoc muscorum. Mol. Gen. Genet. 195, 180–185

    Google Scholar 

  • Ramos, J.L., Madueño, F., Guerrero, M.G. (1985) Regulation of nitrogenase levels in Anabaena sp. strain ATCC 33047 and other filamentous cyanobacteria. Arch. Microbiol. 141, 105–111

    Google Scholar 

  • 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 

  • Rowell, P., Enticott, S., Stewart, W.D.P. (1977) Glutamine synthetase and nitrogenase activity in the blue green alga Anabaena cylindrica. New Phytol. 79, 41–54

    Google Scholar 

  • Rowell, P., Reed, R.H., Hawkesford, M.J., Ernst, A., Díez, J., Stewart, W.D.P. (1981) Some aspects of the regulation of nitrogenase activity in the cyanobacterium Anabaena variabilis. In: Current perspectives in nitrogen fixation, pp. 186–189, Gibson, A.H., Newton, W.E., eds. Australian Academy of Science, Canberra

    Google Scholar 

  • Singh, H.N., Rai, U.N., Rao, V.V., Bagchi, S.N. (1983) Evidence for ammonia as an inhibitor of heterocyst and nitrogenase formation in the cyanobacterium Anabaena cycadeae. Biochem. Biophys. Res. Commun. 111, 180–187

    Google Scholar 

  • Šmarda, J., Komárek, J., Cáslavská, J., Hübel, M. (1988) The Nodularia studies. Arch. Hydrobiol. 80, 109–129

    Google Scholar 

  • Snell, F.D., Snell, C.T. (1949) Colorimetric methods of analysis, 3rd edn., vol. 2, Van Nostrand, New York

    Google Scholar 

  • Stewart, W.D.P. (1980) Some aspects of structure and function in N2-fixing cyanobacteria. Annu. Rev. Microbiol. 34, 497–536

    Google Scholar 

  • Stewart, W.D.P., Rowell, P. (1975) Effects of l-methionine, d,l-sulfoximine on the assimilation of newly fixed NH3, acetylene reduction and heterocyst production in Anabaena cylindrica. Biochem. Biophys. Res. Commun. 65, 846–856

    Google Scholar 

  • Stewart, W.D.P., Fitzgerald, G.P., Burris, R.H. (1968) Acetylene reduction by nitrogen-fixing blue-green algae. Arch. Microbiol. 62, 336–348

    Google Scholar 

  • Turpin, D.H., Edie, S.A., Canvin, D.T. (1984) In vivo nitrogenase regulation by ammonium and methylamine and the effect of MSX on ammonium transport in Anabaena flos-aquae. Plant Physiol. 74, 701–704

    Google Scholar 

  • Van Baalen, C. (1987) Nitrogen fixation. In: The cyanobacteria, pp. 187–198, Fay, P., Van Baalen, C., eds. Elsevier Science Publishers, Amsterdam

    Google Scholar 

  • Weare, N.M., Benemann, J.R. (1974) Nitrogen fixation by Anabaena cylindrica. I. Localization of nitrogen fixation in the heterocyst. Arch. Microbiol. 90, 322–332

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

We thank C. Fernández-Cabrera (Consejo Superior de Investigaciones Científicas, CSIC, Madrid, Spain) for technical assistance, and Dr. G. Pérez-Silva (CSIC) for his collaboration in the Anabaena NR assays. This work was supported by grants from Spanish CI-CyT (PB 87-0204 and PB 92-0497).

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Sanz-Alférez, S., del Campo, F.F. Relationship between nitrogen fixation and nitrate metabolism in the Nodularia strains M1 and M2. Planta 194, 339–345 (1994). https://doi.org/10.1007/BF00197533

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00197533

Key words

  • Blue-green alga
  • Cyanobacterium
  • Nitrate (reduction, uptake)
  • Nitrogen fixation
  • Nodularia