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Induction by antimycin A of cyanide-resistant respiration in heterotrophic Euglena gracilis: Effects of growth, respiration and protein biosynthesis

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Abstract

The addition of antimycin A during the logarithmic phase of growth of heterotrophic Euglena gracilis cultures (in lactate or glucose medium) was immediately followed by decreased respiration and a cessation of grwoth. Induced cyanideresistent respiration appeared 5 h after the addition of the inhibitor then the cells started to grow again and could be cultured in the presence of antimycin A. Thus the cells exhibited a cyanide-and antimycin-resistant respiration which was, in addition, sensitive to salicylhydroxamic acid and propylgallate. Antimycin-adapted Euglena and control cells were compared for their biomass production and protein synthesis. The difference in growth yield between control and antimycin-adapted cells was not as high as would be expected if only the first phosphorylation site of the normal respiratory chain was active in the presence of antimycin A. Furthermore, the ability to incorporate labelled valine into proteins, under resting-cell conditions, was not changed. Strong correlations were established between the effects of respiratory effectors on O2 consumption and valine incorporation. These results suggest that sufficient energy for protein synthesis and growth is provided by the operation of the cyanide-resistant respiratory pathway in antimycin-adapted Euglena.

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Abbreviations

DNP:

dinitrophenol

PG:

propylgallate

SHAM:

salicylhydroxamic acid

References

  • Alexandre, A., Lehninger, A.L. (1984) Bypasses of the antimycin A block of mitochondrial electron transport in relation to ubisemiquinones function. Biochim. Biophys. Acta 767, 120–129

    PubMed  Google Scholar 

  • Bonner, W.D., Rich, P.R. (1978) Molecular aspects of cyanide/antimycin resistant respiration. In: Plant mitochondria, pp. 241–247, Ducet, G., Lance, C., eds. Elsevier/North Holland Biomedical Press, Amsterdam

    Google Scholar 

  • Boveris, A., Cadenas, E., Stoppani, A.O.M. (1976) Role of ubiquinone in the mitochondrial generation of hydrogen peroxide. Biochem. J 156, 435–444

    PubMed  Google Scholar 

  • Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254

    Article  PubMed  Google Scholar 

  • Briand, J., Calvayrac, R., Laval-Martin, D., Farineau, J. (1981) Evolution of carboxylating enzymes involved in paramylon synthesis (phosphoenolpyruvate carboxylase and carboxykinase) in heterotrophically grown Euglena gracilis. Planta 151, 168–175

    Google Scholar 

  • Calvayrac, R. (1972) Le cycle des mitochondries chez Euglena gracilis en culture synchrone. Thèse de Doctorat, University of Paris XI

  • Calvayrac, R., Butow, R.A. (1971) Action de l'antimycine A sur la respiration et la structure des mitochondries d'Euglena gracilis Z. Arch. Mikrobiol. 80, 62–69

    PubMed  Google Scholar 

  • Calvayrac, R., Laval-Martin, D., Hubert, M., Best-Belpomme, M., Vuillaume, M. (1985) ATP production and catalatictype activities in etiolated or green Euglena gracilis. Comp. Biochem. Physiol. 81, 1009–1017

    Google Scholar 

  • Calvayrac, R., Levy, M., Vazart, J., Briand, J., Claisse, M. (1978) Activité cytochrome oxydase des mitochondries d'Euglena gracilis Z: comparison de l'oxydation du ferrocytochrome c 558 et de ferrocytochromes c de mammifères. Biol. Cellulaire 31, 141–148

    Google Scholar 

  • Goffeau, A., Crosby, B. (1978) A new type of cyanide-insensitive, azide-sensitive respiration in the yeasts Schizosaccharomyces pombe and Saccharomyces cerevisiae. In: Biochemistry and genetics of yeast, pp. 81–96, Bacila, M., ed. Academic Press, New York

    Google Scholar 

  • Grover, S.D., Laties, G.G. (1981) Disulfiram inhibition of the alternative respiratory pathway in plant mitochondria. Plant Physiol. 68, 393–400

    Google Scholar 

  • Henry, M.F., Nyns, E.J. (1975) Cyanide-insensitive respiration. An alternative mitochondrial pathway. Sub-Cell. Biochem. 4, 1–65

    Google Scholar 

  • Huq, S., Palmer, J.M. (1978) Superoxide and hydrogen peroxide production in cyanide-resistant Arum maculatum mitochondria. Plant Sci. Lett. 11, 351–358

    Google Scholar 

  • Kahn, J.S. (1974) Physiological adaptation of Euglena gracilis to uncouplers and inhibitors of oxidative phosphorylation. Arch. Biochem. Biophys. 164, 266–274

    PubMed  Google Scholar 

  • Keilin, D., Hartree, E.F. (1955) Relationship between certain components of the cytochrome system. Nature 176, 200–206

    PubMed  Google Scholar 

  • Lambers, H. (1982) Cyanide resistant respiration: a non-phosphorylating electron transport pathway acting as an energy overflow. Physiol. Plant 55, 478–485

    Google Scholar 

  • Lambers, H., Day, D.A., Azcon-Bieto, J. (1983) Cyanide-resistant respiration in roots and leaves. Measurements with intact tissues and isolated mitochondria. Physiol. Plant. 58, 148–154

    Google Scholar 

  • Laties, G.G. (1982) The cyanide-resistant alterntive path in higher plant respiration. Annu. Rev. Plant Physiol. 33, 519–555

    Google Scholar 

  • Mitchell, P. (1976) Possible molecular mechanisms of the protonmotive function of cytochrome systems. J. Theor. Biol. 62, 327–367

    PubMed  Google Scholar 

  • Moore, A.L., Rich, P.R. (1980) The bioenergetics of plant mitochondria. Trends Biochem. Sci. 5, 284–288

    Google Scholar 

  • Pajot, P., Claisse, M. (1974) Utilization by yeast of D-lactate and L-lactate as sources of energy in the presence of antimycin A. Eur. J. Biochem 49, 275–285

    PubMed  Google Scholar 

  • Rich, P.R., Bonner, W.D. (1978) The sites of superoxide anion generation in higher plant mitochondria. Arch. Biochem. Biophys. 188, 206–213

    PubMed  Google Scholar 

  • Rich, P.R., Wiegand, N.K., Blum, H., Moore, A.L., Bonner, W.D. (1978) Studies on the mechanism of inhibition of redox enzymes by substituted hydroxamic acids. Biochim. Biophys. Acta 525, 325–337

    PubMed  Google Scholar 

  • Rustin, P., Dupont, J., Lance, C. (1984) Involvement of lipid peroxy radicals in the cyanide-resistant electron transport pathway. Physiol. Vég. 22, 643–663

    Google Scholar 

  • Schonbaum, G.R., Bonner, W.D. Storey, B.T., Bahr, J.T. (1971) Specific inhibition of the cyanide-insensitive respiratory pathway in plant mitochondria by hydroxamic acids. Plant Physiol 47, 124–128

    PubMed  Google Scholar 

  • Sharpless T.K., Butow, R.A. (1970) An inducible alternate terminal oxidase in Euglena gracilis mitochondria. J. Biol. Chem. 245, 58–70

    PubMed  Google Scholar 

  • Siedow, J.N., Bickett, D.M. (1983) Binding of butyl gallate to isolated mung bean mitochondria. Relationship to inhibition of the alternative pathway. Plant Physiol. 72, 339–344

    Google Scholar 

  • Siedow, J.N., Girvin, M.E. (1980) Alternative respiratory pathway. Its role in seed respiration and its inhibition by propyl gallate. Plant Physiol. 65, 669–674

    Google Scholar 

  • Solomos, T. (1977) Cyanide-resistant respiration in higher plants. Annu. Rev. Plant Physiol. 28, 279–297

    Google Scholar 

  • Steingröver, E. (1981) The relationship between cyanide-resistant root respiration and the storage of sugars in the taproot in Daucus carota L. J. Exp. Bot. 32, 911–919

    Google Scholar 

  • Storey, B.T. (1976) Respiratory chain of plant mitochondria. XVIII. Point of interaction of the alternate oxidase with the respiratory chain. Plant Physiol. 58, 521–525

    Google Scholar 

  • Turrens, J.F., Alexandre, A., Lehninger, A.L. (1985) Ubisemiquinone is the electron donor for superoxide, formation by complex III of heart mitochondria. Arch. Biochem. Biophys. 237, 408–414

    PubMed  Google Scholar 

  • Webb, T., Armstrong, W. (1983) Effects of KCN and salicylhydroxamic acid on the root respiration of pea seedlings. Plant Physiol 72, 0280–0286

    Google Scholar 

  • Wilson, S.B. (1980) Energy conservation by the plant mitochondrial cyanide-insensitive oxidase. Biochem. J. 190, 349–360

    PubMed  Google Scholar 

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Benichou, P., Calvayrac, R. & Claisse, M. Induction by antimycin A of cyanide-resistant respiration in heterotrophic Euglena gracilis: Effects of growth, respiration and protein biosynthesis. Planta 175, 23–32 (1988). https://doi.org/10.1007/BF00402878

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