Archives of Microbiology

, Volume 123, Issue 1, pp 37–45 | Cite as

Modes of electron transfer from molecular hydrogen in Anabaena cylindrica

  • G. Eisbrenner
  • H. Bothe
Article
Received:

Abstract

Several natural and artificial electron donors were assayed in the C2H2-reduction of heterocysts isolated from the cyanobacterium Anabaena cylindrica. Among these, molecular hydrogen was the most effective one when the assays were performed in the light. The C2H2-reduction and the Knallgas reaction of intact Anabaena filaments as well as the H2-supported C2H2-reduction of isolated heterocysts were compared for their sensitivity towards several inhibitors known to affect the photosynthetic or respiratory electron flow. Among these, dibromothymoquinone (DBMIB) affected all three reactions equally indicating that plastoquinone is a common intermediate of the H2-consumptions by either the respiratory or the photosynthetic electron transport. Metronidazole inhibited the H2-utilization via photosynthesis but did not affect the consumption of this gas by respiration and therefore allows to differentiate between the two pathways of hydrogen utilization. The studies with the inhibitors are suggestive for a segment of electron carriers on the membranes common to both photosynthesis and respiration in heterocysts of Anabaena.

Key words

Cyanobacteria Blue-green algae Hydrogen metabolism Nitrogen fixation Isolated heterocysts Inhibitors Plastoquinone 

Abbreviations

BNT

2-bromo-4-nitrothymol

DAD

diaminodurene

DBMIB

2,5-dibromothymoquinome

DCMU

dichlorophenyl dimethylurea

DCPIP

dichlorophenol indophenol

DMSO

dimethylsulphoxide

TMPD

N-tetramethyl-p-phenylenediamine

chl

chlorophyll

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References

  1. Apte, S. K., Rowell, P., Stewart, W. D. P.: Electron donation to ferredoxin in heterocysts of the N2-fixing alga Anabaena cylindrica. Proc. R. Soc. Lond. B 200, 1–25 (1978)Google Scholar
  2. Benemann, J. R., Weare, N. M.: Nitrogen fixation by Anabaena cylindrica. III. Hydrogen supported nitrogenase activity. Arch. Microbiol. 101, 401–408 (1974)Google Scholar
  3. Bisalputra, T., Brown, D. L., Weier, T. E.: Possible respiratory sites in a blue-green alga Nostoc sphaericum as demonstrated by potassium tellurite and tetranitro-blue tetrazolium reduction. J. Ultrastruct. Res. 27, 182–197 (1969)Google Scholar
  4. Böhme, H., Reimer, S., Trebst, A.: The effect of dibromothymoquinone, an antagonist of plastoquinone, on noncyclic and cyclic electron flow systems in isolated chloroplasts. Z. Naturforsch. 26b, 341–352 (1971)Google Scholar
  5. Bothe, H.: Photosynthetische Stickstoffixierung mit einem zellfreien Extrakt aus der Blaualge Anabaena cylindrica. Ber. Dtsch. Bot. Ges. 83, 421–432 (1970)Google Scholar
  6. Bothe, H., Eisbrenner, G.: Aspects of hydrogen metabolism in blue-green algae. In: Hydrogenases: Their catalytic activity, structure and function. (H. G. Schlegel, K. Schneider, eds.) Workshop Meeting on Hydrogenases, Göttingen 29–31 August 1978, Goltze Verlag, 353–369 (1978)Google Scholar
  7. Bothe, H., Distler, E., Eisbrenner, G.: Hydrogen metabolism in blue-green algae. Biochimie 60, 277–289 (1978)PubMedGoogle Scholar
  8. 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
  9. 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
  10. Bothe, H., Tennigkeit, J., Eisbrenner, G.: The utilization of molecular hydrogen by the blue-green alga Anabaena cylindrica. Arch. Microbiol. 114, 43–49 (1977a)PubMedGoogle Scholar
  11. 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 (1977b)Google Scholar
  12. Bradley, S., Carr, N. G.: Heterocysts and nitrogenase development in Anabaena cylindrica. J. Gen. Microbiol. 96, 175–184 (1976)PubMedGoogle Scholar
  13. Brown, A. W., Webster, G. C.: The influence of light on the rate of respiration of the blue-green alga, Anabaena. Am. J. Bot. 40, 753–758 (1953)Google Scholar
  14. Carr, N. G., Exell, G., Flynn, V., Hallaway, M., Talukdar, S.: Minor quinones of some Myxophyceae. Arch. Biochem. Biophys. 120, 503–507 (1967)Google Scholar
  15. Codd, G. A., Cossar, J. D.: The site of inhibition of photosystem II by 3-(3,4-dichlorophenyl) N-N′-dimethylurea in thylakoids of the cyanobacterium Anabaena cylindrica. Biochem. biophys. Res. Comm. 83, 342–346 (1978)PubMedGoogle Scholar
  16. Edwards, D. F., Mathison, G. E., Platt, D. J.: Metronidazole — an antimicrobial drug which inhibits photosynthesis. Z. Pflanzenphysiol. 71, 424–427 (1974)Google Scholar
  17. Edwards, D. J., Mathison, G. E.: The mode of action of metronidazole against Trichomonas vaginalis. J. Gen. Microbiol. 63, 297–302 (1970)PubMedGoogle Scholar
  18. Eisbrenner, G., Distler, E., Floener, L., Bothe, H.: The occurrence of the hydrogenase in some blue-green algae. Arch. Microbiol. 118, 177–184 (1978)Google Scholar
  19. Grunberg, E., Titsworth, E.: Chemotherapeutic properties of heterocyclic compounds: monocyclic compounds with five membered rings. Ann. Rev. Microbiol. 27, 317–347 (1974)CrossRefGoogle Scholar
  20. Haselkorn, R.: Heterocysts. Ann. Rev. Plant Physiol. 29, 319–344 (1978)CrossRefGoogle Scholar
  21. Ho, K. K., Ulrich, E. L., Krogmann, D. W., Gomez-Lojero, C.: Isolation of photosynthetic catalysts from cyanobacteria. Biochim. Biophys. Acta. 545, 236–248 (1979)PubMedGoogle Scholar
  22. Hoch, G., Owens, O. v. H., Kok, B.: Photosynthesis and respiration. Arch. Biochem. Biophys. 101, 171–180 (1963)PubMedGoogle Scholar
  23. Kimiura, M., Katoh, S.: Studies on electron transport associated with photosystem I. III. The reduction sites of various Hill oxidants in the photosynthetic electron transport system. Biochim. Biophys. Acta. 325, 167–174 (1973)PubMedGoogle Scholar
  24. Leach, C. K., Carr, N. G.: Pyruvate: ferredoxin oxidoreductase and its activation by ATP in the blue-green alga Anabaena variabilis. Biochim. Biophys. Acta 245, 165–174 (1971)PubMedGoogle Scholar
  25. Lex, M., Carr, N. G.: The metabolism of glucose by heterocysts and vegetative cells of Anabaena cylindrica. Arch. Microbiol. 101, 161–167 (1974)PubMedGoogle Scholar
  26. Lockau, W., Peterson, R. B., Wolk, C. P., Burris, R. H.: Modes of reduction of nitrogenase in heterocysts isolated from Anabaena species. Biochim. Biophys. Acta. 502, 298–308 (1978)PubMedGoogle Scholar
  27. Loschen, G., Azzi, A.: Dibromothymoquinone: a new inhibitor of mitochondrial electron transport at the level of ubiquinone. FEBS Letters 41, 115–117 (1974)CrossRefPubMedGoogle Scholar
  28. Müller, M., Lindmark, D. G.: Uptake of metronidazole and its effect on viability in trichonomads and Entamoeba invadens under anaerobic and aerobic conditions. Antimicrob. Agents Chemother. 9, 696–700 (1976)PubMedGoogle Scholar
  29. Ouitrakul, R., Izawa, S.: Electron transport and photophosphorylation in chloroplasts as a function of the electron acceptor II. Acceptor-specific inhibition by KCN. Biochim. Biophys. Acta 305, 105–118 (1973)PubMedGoogle Scholar
  30. Padan, E., Schuldiner, S.: Energy transduction in the photosynthetic membranes of the cyanobacterium (blue-green alga) Plectonema boryanum. J. Biol. Chem. 253, 3281–3286 (1978)PubMedGoogle Scholar
  31. Peterson, R. B., Burris, R. H.: Hydrogen metabolism in isolated heterocysts of Anabaena 7120. Arch. Microbiol. 116, 125–132 (1978)Google Scholar
  32. Peterson, R. B., Wolk, C. P.: Localisation of an uptake hydrogenase in Anabaena. Plant Physiol. 61, 688–691 (1978)Google Scholar
  33. Poole, R. K., Haddock, B. A.: Dibromothymoquinone: an inhibitor of aerobic electron transport at the level of ubiquinone in Escherichia coli. FEBS Letters 52, 13–16 (1975)CrossRefPubMedGoogle Scholar
  34. Scholes, P., Mitchell, P., Moyle, J.: The polarity of proton translocation in some photosynthetic microorganisms. Eur. J. Biochem. 8, 450–454 (1969)PubMedGoogle Scholar
  35. Selman, B. R.: Phenylenediamine restoration of photosynthetic electron flux in DBMIB-inhibited chloroplasts. J. Bioenerget. Biomembr. 8, 143–156 (1976)Google Scholar
  36. Siedow, J. N., Huber, S. C., Moreland, D. E.: Inhibition of mung bean mitochondrial electron transfer by dibromothymoquinone. In: Plant Mitochondria, (C. Ducet and C. Lance, eds.), Amsterdam, Elsevier/North Holland Biomedical Press, p. 233–240 (1978)Google Scholar
  37. Smith, R. V., Noy, R. J., Evans, M. C. W.: Physiological electron donator systems to the nitrogenase of the blue-green alga Anabaena cylindrica. Biochim. Biophys. Acta 253, 104–109 (1971)PubMedGoogle Scholar
  38. Spiller, H., Ernst, E., Kerfin, W., Böger, P.: Increase and stabilization of photoproduction of hydrogen in Nostoc muscorum by photosynthetic transport inhibitors. Z. Naturforsch. 33c, 541–547 (1978)Google Scholar
  39. Sun, J. L., Crane, F. L.: Coordinated, coenzyme Q reversible, 2,5-dibromothymoquinone inhibition of electron transport and ATPase in Escherichia coli. Biochem. Biophys. Res. Comm. 68, 190–196 (1976)PubMedGoogle Scholar
  40. 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)PubMedGoogle Scholar
  41. Tel-Or, E., Stewart, W. D. P.: Photosynthetic compounds and activities of nitrogen fixing isolated heterocysts of Anabaena cylindrica. Proc. R. Soc. Lond. B 198, 61–86 (1977)Google Scholar
  42. Tel-Or, E., Luijk, L. W., Packer, L.: Hydrogenase in N2-fixing cyanobacteria. Arch. Biochem. Biophy. 185, 185–194 (1978)Google Scholar
  43. Tel-Or, E., Luijk, L. W., Packer, L.: An inducible hydrogenase in cyanobacteria enhances N2-fixation. FEBS Letters 78, 49–51 (1977)CrossRefPubMedGoogle Scholar
  44. Trebst, A., Reimer, S.: Reversal of the inhibition of photosynthetic electron flow in chloroplasts by an internal TMPD bypass. In: Photosynthetic Organelles, Special Issue of Plant and Cell Physiol., pp. 201–209 (1977)Google Scholar
  45. Trebst, A., Wietoska, H., Draber, W., Knops, H. J.: The inhibition of photosynthetic electron flow in chloroplasts by the dinitrophenylether of bromo-or iodo-nitrophenol. Z. Naturforsch. 33c, 919–927 (1978)Google Scholar
  46. Weissman, J. C., Benemann, J. R.: Hydrogen production by notrogen-starved cultures of Anabaena cylindrica. Appl. Environm. Microbiol. 33, 123–131 (1977)Google Scholar
  47. Winkenbach, F., Wolk, C. P.: Activities of Enzymes of the oxidative and the reductive pentosephosphate pathways in heterocysts of a blue-green alga. Plant Physiol. 52, 480–483 (1973)Google Scholar
  48. Wolk, C. P.: Physiology and cytological chemistry of blue-green algae. Bacteriol. Rev. 37, 32–101 (1973)PubMedGoogle Scholar

Copyright information

© Springer-Verlag 1979

Authors and Affiliations

  • G. Eisbrenner
    • 1
  • H. Bothe
    • 1
  1. 1.II. LehrstuhlBotanisches Institut der Universität zu KölnKöln 41Germany

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