Skip to main content
Log in

Hydrogen metabolism in isolated heterocysts of Anabaena 7120

  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Isolated heterocysts of Anabaena 7120 evolve H2 in an ATP-dependent nitrogenase-catalyzed process that is inhibited by N2 and C2H2. Heterocysts have an active uptake hydrogenase that only requires an electron acceptor of positive redox potential, e.g., methylene blue, dichlorophenolindophenol or potassium ferricyanide. O2 supplied at low partial pressures is a very effective physiological oxidant for H2 uptake. High concentrations of O2 are inhibitory to H2 uptake. The oxyhydrogen reaction in heterocysts appears to be mediated by a cytochrome-cytochrome oxidase system, and it supports ATP synthesis via oxidative phosphorylation. Attempts to demonstrate acetylene reduction in isolated heterocysts employing H2 as an electron donor were unsuccessful. It is suggested that the uptake hydrogenase functions to conserve reductant that otherwise would be dissipated via nitrogenase-catalyzed H2 evolution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Allen, M. B., Arnon, D. I.: Studies on N-fixing blue-green algae. I. Growth and N-fixation by Anabaena cylindrica Lemm. Plant Physiol. 30, 366–372 (1955)

    Google Scholar 

  • Ben-Amotz, A., Erbes, D. L., Riederer-Henderson, M. A., Peavey, D. G., Gibbs, M.: H2 metabolism in photosynthetic organisms. I. Dark H2 evolution and uptake by algae and mosses. Plant Physiol. 56, 72–77 (1975)

    Google Scholar 

  • Benemann, J. R., Weare, N. M.: Nitrogen fixation by Anabaena cylindrica. III. Hydrogen-supported nitrogenase activity. Arch. Microbiol. 101, 401–408 (1974a)

    Google Scholar 

  • Benemann, J. R., Weare, N. M.: H2 evolution by N2-fixing Anabaena cylindrica. Science 184, 174 (1974b)

    Google Scholar 

  • Bothe, H., Tennigkeit, J., Eisbrenner, G., Yates, M. G.: The hydrogenase-nitrogenase relationship in the blue-green algae Anabaena cylindrica. Planta (Berl.) 133, 237–242 (1977)

    Google Scholar 

  • Bulen, W. A., Burns, R. C., LeComte, J. R.: Nitrogen fixation: hydrosulfite as electron donor with cell-free preparations of Azotobacter vinelandii and Rhodospirillum rubrum. Proc. Nat. Acad. Sci. U.S.A. 53, 532–539 (1965)

    Google Scholar 

  • Burris, R. H., Peterson, R. B.: Nitrogen-fixing blue-green algae: Their H2 metabolism and their activity in freshwater lakes. In: Environmental role of nitrogen-fixing blue-green algae and asymbiotic bacteria (U. Granhall, ed.). Ecol. Bull (Stockh.) 26 (in press)

  • Conover, T. E., Prairie, R. L., Racker, E.: Partial resolution of the enzymes catalyzing oxidative phosphorylation. III. A new coupling factor required by submitochondrial particles extracted with phosphatides. J. Biol. Chem. 238, 2831–2837 (1963)

    PubMed  Google Scholar 

  • Dixon, R. O. D.: Hydrogen uptake and exchange by pea root nodules. Ann. Bot 31, 179–188 (1967)

    Google Scholar 

  • Dixon, R. O. D.: Hydrogenase in legume root nodule bacteroids. Occurrence and properties. Arch. Mikrobiol. 85, 193–201 (1972)

    Google Scholar 

  • Fay, P., Walsby, A. E.: Metabolic activities of isolated heterocysts of the blue-green alga Anabaena cylindrica. Nature (Lond.) 209, 94–95 (1966)

    Google Scholar 

  • Fisher, H. F., Krasna, A. I., Rittenberg, D.: The interaction of hydrogenase with oxygen. J. Biol. Chem. 209, 569–578 (1954)

    PubMed  Google Scholar 

  • Fujita, Y., Myers, J.: Hydrogenase and NADP-reduction reactions by a cell-free preparation of Anabaena cylindrica. Arch. Biochem. Biophys. 111, 619–625 (1965)

    PubMed  Google Scholar 

  • Gaffron, H.: Reduction of carbon dioxide coupled with the oxyhydrogen reaction in algae. J. Gen. Physiol. 26, 241–267 (1942)

    Google Scholar 

  • Gaffron, H., Rubin, J.: Fermentative and photochemical production of hydrogen in algae. J. Gen. Physiol. 26, 195–240 (1942)

    Google Scholar 

  • Gest, H., Kamen, M. D.: Photoproduction of molecular hydrogen by Rhodospirillum rubrum. Science 109, 558–559 (1949)

    Google Scholar 

  • Haystead, A., Robinson, R., Stewart, W. D. P.: Nitrogenase activity in extracts of heterocystous and non-heterocystous blue-green algae. Arch. Mikrobiol. 74, 235–243 (1970)

    PubMed  Google Scholar 

  • Heytler, P. G., Prichard, G.: A new class of uncoupling agents: carbonylcyanide phenylhydrazones. Biochem. Biophys. Res. Commun. 7, 272–275 (1962)

    PubMed  Google Scholar 

  • Hoberman, H. D., Rittenberg, D.: Biological catalysis of the exchange reaction between water and hydrogen. J. Biol. Chem. 147, 211–227 (1943)

    Google Scholar 

  • Hoch, G. E., Schneider, K. C., Burris, R. H.: Hydrogen evolution and exchange, and conversion of N2O to N2 by soybean root nodules. Biochim. Biophys. Acta 37, 273–279 (1960)

    PubMed  Google Scholar 

  • Horwitz, L.: Observations on the oxyhydrogen reaction in Scenedesmus and its relation to respiration and photosynthesis. Arch. Biochem. Biophys. 66, 23–44 (1957)

    PubMed  Google Scholar 

  • Hyndman, L. A., Burris, R. H., Wilson, P. W.: Properties of hydrogenase from Azotobacter vinelandii. J. Bacteriol. 65, 522–531 (1953)

    PubMed  Google Scholar 

  • Jones, L. W., Bishop, N. I.: Simultaneous measurement of oxygen and hydrogen exchange from the blue-green alga Anabaena. Plant Physiol. 57, 659–665 (1976)

    Google Scholar 

  • Keilin, D.: The history of cell respiration and cytochrome. London: Cambridge University Press 1966

    Google Scholar 

  • Lindberg, O., Ernster, L.: In: Biochemical methods of analysis (D. Glick, ed.) Vol. III. New York: Interscience 1956

    Google Scholar 

  • Ooyama, J.: N2 fixing hydrogen bacteria. In: Biological solar energy conversion (A. Mitsui et al., eds.) New York: Academic Press 1977

    Google Scholar 

  • Packer, L., Tel-Or, E., Luijk, L.: Hydrogenase in heterocysts and vegetative cells of N2-fixing blue-green algae. Fed. Proc. 36, 881 (1977)

    Google Scholar 

  • Peters, G. A., Evans, W. R., Toia, R. E.: Azolla-Anabaena azollae relationship. IV. Photosynthetically driven, nitrogenase-catalyzed H2 production. Plant Physiol. 58, 119–126 (1976)

    Google Scholar 

  • Peterson, R. B.: N2 fixation by blu-green algae: I. Field studies on N2 fixation by aquatic blue-green algae. II. N2 fixation and H2 metabolism in heterocysts of the blue-green alga Anabaena 7120. Ph.D. thesis, Department of Biochemistry, University of Wisconsin, Madison, Wisconsin (1976)

    Google Scholar 

  • Peterson, R. B., Burris, R. H.: Properties of heterocysts isolated with colloidal silica. Arch. Microbiol. 108, 35–40 (1976)

    PubMed  Google Scholar 

  • Rivera-Ortiz, J. M., Burris, R. H.: Interactions among substrates and inhibitors of nitrogenase. J. Bacteriol. 123, 537–545 (1975)

    PubMed  Google Scholar 

  • Schubert, K. R., Evans, H. J.: Hydrogen evolution: A major factor affecting the efficiency of nitrogen fixation in nodulated symbionts. Proc. Nat. Acad. Sci. U.S.A. 73, 1207–1211 (1976)

    Google Scholar 

  • Scott, W. E., Fay, P.: Phosphorylation and amination in heterocysts of Anabaena variabilis. Br. Phycol. J. 7, 283–284 (1972)

    Google Scholar 

  • Smith, L. A., Hill, S., Yates, M. G.: Inhibition by acetylene of conventional hydrogenase in nitrogen-fixing bacteria. Nature 262, 209–210 (1976)

    PubMed  Google Scholar 

  • Tel-Or, E., Stewart, W. D. P.: Photosynthetic electron transport, ATP synthesis and nitrogenase activity in isolated heterocysts of Anabaena cylindrica. Biochim. Biophys. Acta 423, 189–195 (1976)

    PubMed  Google Scholar 

  • Umbreit, W. W., Burris, R. H., Stauffer, J. F.: Manometric and biochemical techniques. Minneapolis: Burgess 1972

    Google Scholar 

  • Wang, R., Healey, F. P., Myers, J.: Amperometric measurement of hydrogen evolution in Chlamydomonas. Plant Physiol. 48, 108–110 (1971)

    Google Scholar 

  • Winter, H. C., Burris, R. H.: Stoichiometry of the adenosine triphosphate requirement for N2 fixation and H2 evolution by a partially purified preparation of Clostridium pasteurianum. J. Biol. Chem. 243, 940–944 (1968)

    PubMed  Google Scholar 

  • Wolk, C. P., Wojciuch, E.: Photoreduction of acetylene by heterocysts. Planta (Berl.) 97, 126–134 (1971)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Peterson, R.B., Burris, R.H. Hydrogen metabolism in isolated heterocysts of Anabaena 7120. Arch. Microbiol. 116, 125–132 (1978). https://doi.org/10.1007/BF00406027

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00406027

Key words

Navigation