Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

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

  • 102 Accesses

  • 76 Citations

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 to check access.

Abbreviations

DCMU:

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

DNP:

2-4-dinitrophenol

FCCP:

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

Chl:

chlorophyll

References

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

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

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

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

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

  6. 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)

  7. 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)

  8. 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)

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

  10. 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)

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

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

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

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

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

  16. 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)

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

  18. 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)

  19. 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

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

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

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

  23. 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)

  24. 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)

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

  26. 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)

  27. 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

Download references

Author information

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

Key words

  • Cyanobacteria
  • Anabaena
  • Hydrogenase
  • Hydrogen-uptake
  • Nitrogenase
  • Nitrogen fixation
  • Protection mechanism
  • Inhibitors