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The hydrogenase-nitrogenase relationship in the blue-green algaAnabaena cylindrica

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Abstract

Nitrogen-fixingAnabaena cylindrica cells are found to evolve hydrogen in high quantities in the presence of CO plus C2H2. Studies with the inhibitors dichlorophenyldimethylurea (DCMU), disalicylidenepropanediamine (DSPD), dibromothymoquinone (DBMIB), undecylbenzimidazole (UDB) and chloro-carbonyl-cyanide-phenylhydrazone (CCCP) and also withAnabaena grown on nitrate- and ammonia-nitrogen show that the H2-formation is due to the ATP-dependent H3O+-reduction catalysed by nitrogenase. In control experiments CO plus C2H2 inhibited the activities of a cell-free hydrogenase fromClostridium pasteurianum. It is concluded that Anabaena has a hydrogenase whose natural function is to recycle the H2 lost by the action of nitrogenase.

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Abbreviations

Cl-CCP:

m-chloro-carbonyl-cyanide-phenylhydrazone

DSPD:

disalicylidenepropanediamine(1–3)

DBMIB:

dibromothymoquinone

DCMU:

N-(3,4-dichlorophenyl) NN-dimethyl-urea

UDB:

2-undecyl-benzimidazole

References

  • Ben-Amotz, A., Erbes, D.L., Riederer-Henderson, A., Peavey, D.G., Gibbs, M.: H2-metabolism in photosynthetic organisms. Plant Physiol.56, 72–77 (1975)

    Google Scholar 

  • Benemann, J.R., Berenson, J.A., Kaplan, N.O., Kamen, M.D.: Hydrogen evolution by a chloroplast-ferredoxin-hydrogenase system. Proc. nat. Acad. Sci. (Wash.)70, 2317–2320 (1973)

    Google Scholar 

  • Benemann, J.R., Weare, N.M.: Hydrogen evolution by nitrogen-fixingAnabaena cylindrica. Science N.Y.184, 174–175 (1974a)

    Google Scholar 

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

    Google Scholar 

  • Biggins, J.: Photosynthetic reactions by lysed protoplasts and paticle preparations from the blue-green alga,Phormidium luridum. Plant Physiol.42, 1447–1456 (1967)

    Google Scholar 

  • Bose, S.K., Gest, H.: Relationship between energy generation and net electron transfer in bacterial photosynthesis.In: Energy-linked functions of mitochondria, B. Chance (ed.), p. 207–231. New York: Acad. Press 1963

    Google Scholar 

  • Bothe, H., Falkenberg, B., Nolteernsting, U.: Properties and function of the pyruvate: ferredoxin oxidoreductase from the blue-green algaAnabaena 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 algaAnabaena cylindrica. Arch. Mikrobiol.86, 241–254 (1972)

    Google Scholar 

  • Brotonegoro, S.: Nitrogen fixation and nitrogenase activity ofAzotobacter chroococcum. Thesis. Wageningen/Netherlands: Agricultural University 1974

  • Burns, R.C., Hardy, R.W.F.: Nitrogen fixation in bacteria and higher plants. Molecular Biology, Biochemistry and Biophysics Vol.21, Berlin-Heidelberg-New York: Springer 1975

    Google Scholar 

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

    Google Scholar 

  • Eady, R.R., Postgate, J.R.: Nitrogenase. Nature (London)249, 805–810 (1974)

    Google Scholar 

  • Frenkel, A.W., Rieger, C.: Photoreduction in algae. Nature (London)167, 1030 (1951)

    Google Scholar 

  • Fujita, S., Ohama, H., Hattori, A.: Hydrogenase activity of cell-free-preparations obtained from the blue-green algae. Plant and Cell Physiol.5, 305–314 (1964)

    Google Scholar 

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

    Google Scholar 

  • Gaffron, H.: Carbondioxyde reduction with molecular hydrogen in green algae. Amer. J. Bot.27, 273–283 (1940)

    Google Scholar 

  • Gest, H., Ormerod, J.G., Ormerod, K.S.: Photometabolism ofRhodospirillum rubrum: light dependent dissimilation of organic compounds to carbon dioxyde and molecular hydrogen by an anaerobic citric acid cycle. Arch. Biochem. Biophys.97, 21–33 (1962)

    Google Scholar 

  • Gray, C.T., Gest, H.: Biological formation of molecular hydrogen. Science, N.Y.148, 186–192 (1965)

    Google Scholar 

  • Healey, F.P.: Hydrogen evolution by several algae. Planta (Berl.)91, 220–226 (1970)

    Google Scholar 

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

    Google Scholar 

  • Hattori, A.: Effect of hydrogen on nitrite reduction byAnabaena cylindrica. Studies on microalgae and photosynthetic bacteria. Jap. Soc. Plant Cell Physiol. pp. 485–492. Tokyo: University Press 1963

    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)

    Google Scholar 

  • Haystead, A., Stewart, W.D.P.: Characteristics of the nitrogenase system of the blue-green algaAnabaena cylindrica. Arch. Mikrobiol.82, 325–336 (1972)

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Kaltwasser, H., Stuart, T.S., Gaffron, H.: Light dependent hydrogen evolution byScenedesmus. Planta (Berl.)89, 309–322 (1969)

    Google Scholar 

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

    Google Scholar 

  • Mortenson, L.E., Chen, J.-S.: Hydrogenase.In: Microbial iron metabolism, Neilands, J.B. (ed.), p. 231–282. New York-London: Academic Press 1974

    Google Scholar 

  • Newton, J.W.: Photoproduction of molecular hydrogen by a plant-algal symbiotic system. Science, N.Y.191, 559–560 (1976)

    Google Scholar 

  • Phelps, A.S., Wilson, P.W.: Occurrence of hydrogenase in nitrogen-fixing organisms. Proc. Soc. exp. Biol. Med. (N.Y.)47, 473–476 (1941)

    Google Scholar 

  • Rao, K.K., Rosa, L., Hall, D.O.: Prolonged production of hydrogen gas by a chloroplast biocatalytic system. Biochem. biophys. Res. Comman.68, 21–27 (1976)

    Google Scholar 

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

    Google Scholar 

  • Schubert, R.K., Evans, H.J.: Hydrogen evolution: a major factor affecting the efficiency of nitrogen fixation in nodulated symbionts. Proc. nat. Acad. Sci. (Wash.)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 

  • Stewart, W.D.P.: Nitrogen fixation by photosynthetic microorganisms. Ann. Rev. Microbiol.27, 283–316 (1973)

    Google Scholar 

  • Stewart, W.D.P., Haystead, A., Dharmawadene, M.W.N.: Nitrogen assimilation and metabolism in blue-green algae.In: Stewart, W.D.P. (ed.) Nitrogen fixation by free-living micro-organisms. Intern. Biol. Programme, Vol. 6, p. 129–158. Cambridge: University Press 1975

    Google Scholar 

  • Sweetser, P.B.: Colorimetric determination of trace levels of oxygen in gases with the photochemically generated methyl viologen cation. Anal. Chem.39, 979–982 (1967)

    Google Scholar 

  • Thauer, R.K., Fuchs, G., Kaeufer, B., Schnitker, U.: Carbon monoxide oxidation in cell-free extracts ofClostridium pasteurianum. Europ. J. Biochem.45, 343–349 (1974)

    Google Scholar 

  • Ward, M.A.: Whole cell and cell-free hydrogenases of algae. Phytochemistry9, 259–266 (1970)

    Google Scholar 

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Authors and Affiliations

  1. Botanisches Institut der Universität Heidelberg, Hofmeisterweg 4, D-6900, Heidelberg, Germany

    H. Bothe, J. Tennigkeit & G. Eisbrenner

  2. ARC Unit of Nitrogen Fixation, The University of Sussex, BN1 9QJ, Brighton, UK

    M. G. Yates

Authors
  1. H. Bothe
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  2. J. Tennigkeit
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  3. G. Eisbrenner
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  4. M. G. Yates
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Bothe, H., Tennigkeit, J., Eisbrenner, G. et al. The hydrogenase-nitrogenase relationship in the blue-green algaAnabaena cylindrica . Planta 133, 237–242 (1977). https://doi.org/10.1007/BF00380683

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  • DOI: https://doi.org/10.1007/BF00380683

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