Skip to main content
Log in

The utilization of molecular hydrogen by the blue-green alga Anabaena cylindrica

  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

The blue-green alga Anabaena cylindrica is found to consume molecular hydrogen in a hydrogenase dependent reaction. This hydrogen uptake proceeds in the dark and is strictly dependent on oxygen, thus representing a Knallgas reactions. Its rate is almost as high as that of the endogenous respiration in Anabaena. Studies with inhibitors reveal that hydrogen is utilized via the complete respiratory chain providing additional energy for the alga. CO plus C2H2 completely block the Knallgas reaction which explains the previously reported considerable increase in the total H2 formation representing the difference between the nitrogenase-dependent H2-evolution and the reutilization of the gas catalysed by the hydrogenase in intact Anabaena.

H2 is able to support the C2H2-reduction in the dark in a reaction again strictly dependent on oxygen. Moreover, H2 is also consumed in experiments carried out under far red light and in the presence of dichlorophenyl-dimenthyl-urea (DCMU) where the energy for nitrogen fixation is no longer provided by respiration but by cyclic photophosphorylation. Under these conditions, H2 is found to supply electrons for the formation of C2H4 from C2H2 in a reaction no longer dependent on the presence of oxygen. Moreover, in these experiments, the presence of H2 stabilizes the C2H2-reduction activity against the deleterious effect of oxygen.

Thus, this communication provides evidence for a triplicate function of the H2-uptake catalysed by hydrogenase in intact Anabaena which is (a) to provide energy by the Knallgas reaction, (b) to supply reducing equivalents for nitrogenase, (c) to protect nitrogenase from damage by oxygen.

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

Abbreviations

DCMU:

N′-(3,4-dichlorophenyl)N,N-dimethylurea

DNP:

2-4-dinitrophenol

FCCP:

carbonylcyanid-p-trifluormethoxyphenyl-hydrazone(=p-CF3-CCP)

Chl:

chlorophyll

References

  • Benemann, J. R., Weare, N. M.: Hydrogen-evolution by nitrogenfixing Anabaena cylindrica cultures. Sciences 184, 174–175 (1974a)

    Google Scholar 

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

    Google Scholar 

  • Biggins, J.: Respiration in blue-green algae. J. Bact. 99, 570–575 (1969)

    Google Scholar 

  • Bothe, H.: Ferredoxin als Kofaktor der zyklischen Photophosphorylierung in einem zellfreien Extrakt aus der Blaualge Anacystis. Z. Naturforschg. 24b, 1574–1582 (1969)

    Google Scholar 

  • Bothe, H.: Photosynthetische Stickstoffixierung mit einem zellfreien Extrakt aus der Blaualge Anabaena cylindrica. Ber. Dtsch. Bot. Ges. 83, 421–423 (1970)

    Google Scholar 

  • Bothe, H., Falkenberg, B., Nolteernsting, U.: Properties and function of the pyruvate: ferredoxin oxidoreductase from the blue-green alga Anabaena cylindrica. Arch. Microbiol. 96, 291–304 (1974)

    Google Scholar 

  • Bothe, H., Loos, E.: Effect of far red light and inhibitors on nitrogen fixation and photosynthesis in the blue-green alga Anabaena cylindrica. Arch. Mikrobiol. 86, 241–254 (1972)

    Google Scholar 

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

    Google Scholar 

  • Brotonegoro, S.: Nitrogen fixation and nitrogenase activity in Azotobacter chroococcum. Thesis, Wageningen (Netherlands), Agricultural University (1974)

    Google Scholar 

  • Codd, G. A., Rowell, P., Stewart, W. D. P.: Pyruvate and nitrogenase activity in cell-free extracts of the blue-green alga Anabaena cylindrica. Biochem. Biophys. Res. Comm. 61, 424–431 (1974)

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Hardy, R. W. F., Burns, R. C. Biological nitrogen fixation. Ann. Rev. Biochem. 37, 331–358 (1968)

    Google Scholar 

  • Hillmer, P., Gest, H.: H2-metabolism in the photosynthetic bacterium Rhodopseudomonas capsulata: H2 production by growing cultures. J. Bact. 129, 724–731 (1977a)

    Google Scholar 

  • Hillmer, P., Gest, H.: H2-metabolism in the photosynthetic bacterium Rhodopseudomonas capsulata: Production and utilization of H2 by resting cells. J. Bact. 129, 732–739 (1977b)

    Google Scholar 

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

    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 

  • Kessler, E.: Hydrogenase, photoreduction and anaerobic growth. In: Algal physiology and biochemistry (W. D. P. Stewart, ed.). Botanical monograph, Vol. 10, pp. 456–473. Oxford: Blackwell 1974

    Google Scholar 

  • Klemme, J. H.: Untersuchungen zur Photoautotrophie mit molekularem Wasserstoff bei neu isolierten schwefelfreien Purpurbakterien. Arch. Mikrobiol. 64, 29–42 (1968)

    Google Scholar 

  • Newton, J. W.: Photoproduction of molecular hydrogen by a plantalgal symbiotic system. Science 191, 559–560 (1976)

    Google Scholar 

  • Peschek, G. A.: Die bioenergetischen Prozesse der Blaualge Anacystis nidulans. Thesis, The University of Vienna, Austria, pp. 1–252 (1974)

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Thauer, R. K., Käufer, B., Zähringer, M., Jungermann, K.: The reaction of the iron-sulfur protein hydrogenase with carbon monoxide. Eur. J. Biochem. 42, 447–452 (1974)

    Google Scholar 

  • Umbreit, W. W., Burris, R. H., Stauffer, J. F.: Manometric and biochemical techniques, 5th ed., pp. 61–62. Minneapolis, Minnesota (U.S.A.) Burgess 1972

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bothe, H., Tennigkeit, J. & Eisbrenner, G. The utilization of molecular hydrogen by the blue-green alga Anabaena cylindrica . Arch. Microbiol. 114, 43–49 (1977). https://doi.org/10.1007/BF00429628

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00429628

Key words

Navigation