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The glucose dehydrogenase-mediated energization of Acinetobacter calcoaceticus as a tool for evaluating its susceptibility to, and defence against, hazardous chemicals

  • Applied Microbial and Cell Physiology
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Abstract

Cells of Acinetobacter calcoaceticus 69-V could be energized by glucose oxidation after the growth on acetate, ethanol, hexanol and benzoate. The velocities of glucose oxidation-driven ATP syntheses were relatively constant in the range from pH 5.4 to 7.5. With decreasing pH values (7.0, 6.0, 5.4) ATP synthesis was inhibited more strongly by the action of 2,4-dinitrophenol and at the same pH value glucose oxidation was nearly unimpaired or inhibited more weakly. This finding is expressed by a decrease of the P/O ratios, indicating the uncoupling of the electron-transport phosphorylation by 2,4-dinitrophenol. The sensitivity towards this uncoupling effect was higher in ethanol-grown cells of Acinetobacter calcoaceticus 69-V than in hexanol- or acetate-grown cells. This increase in sensitivity was accompanied by a decrease of the ratio of saturated (mainly C16:0) to unsaturated (C16:1, C18:1) fatty acids in ethanol-grown cells compared with hexanol-grown ones. The knowledge of such differences in the susceptibility and its molecular background, e.g. possible substrate-induced changes of the fatty acid composition of the cytoplasmic membranes, should help elucidate mechanisms of poisoning by membrane-active hazardous chemicals and develop defence strategies.

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References

  • Ameyama M, Nonobe M, Hayashi M, Shinagawa E, Matsushita K, Adachi O (1985) Mode of binding of pyrroloquinoline quinone to apo-glucose dehydrogenase. Agric Biol Chem 49:1227–1231

    Google Scholar 

  • Baumann P (1968) Isolation of Acinetobacter from soil and water. J Bacteriol 96:39–42

    Google Scholar 

  • Baumann P, Doudoroff M, Stanier RY (1968) A study of the Moraxella group. 2. Oxidase-negative species (genus Acinetobacter). J Bacteriol 95:1520–1541

    Google Scholar 

  • Benz R, Mc Laughlin S (1983) The molecular mechanism of action of the proton ionophore FCCP (carbonylcyanide p-trifluoromethoxyphenylhydrazone) Biophys J 41:381–398

    Google Scholar 

  • Borneleit P, Hermsdorf T, Claus R, Walter P, Kleber H-P (1988) Effect of hexadecane-induced vesiculation on the outer membrane of Acinetobacter calcoaceticus. J Gen Microbiol 134:1983–1992

    Google Scholar 

  • Bouvet OMM, Grimmont PAD (1988) Extracellular oxidation of d-glucose by some members of the Enterobacteriaceae. Ann Inst Pasteur Microbiol 139:59–77

    Google Scholar 

  • Buurman EdT. Boiardi JL, Joost Teixeira de Mattos M, Neijssel OM (1990) The role of magnesium and calcium ions in the glucose dehydrogenase activity of Klebsiella pneumoniae NCTC 418. Arch Microbiol 153:502–505

    Google Scholar 

  • Clejan S, Guffanti AA, Falk LH, Krulwich TA (1988) The protonophore resistance of Bacillus megaterium is correlated with elevated ratios of saturated to unsaturated fatty acids in membrane phospholipids. Biochim Biophys Acta 932:43–51

    Google Scholar 

  • Diefenbach R, Heipieper HJ, Keweloh H (1992) The conversion of cis into trans unsaturated fatty acids in Pseudomonas putida P8: evidence for a role in the regulation of membrane fluidity. Appl Microbiol Biotechnol 38:382–387

    Google Scholar 

  • Dokter P, Wielink JE van, Kleef MAG van, Duine JA (1988) Cytochrome b-562 from Acinetobacter calcoaceticus L.M.D. 79.41. Its characteristics and role as electron acceptor for quino protein glucose dehydrogenase. Biochem J 254:131–138

    Google Scholar 

  • Duine JA (1991) Energy generation and the glucose dehydrogenase pathway in Acinetobacter. In: The biology of Acinetobacter, taxonomy, clinical importance, molecular biology, physiology, industrial relevance. FEMS Symposium 57. Plenum, New York, pp 295–312

    Google Scholar 

  • Heipieper HJ, Diefenbach R, Keweloh (1992) Conversion of cis unsaturated fatty acids to trans, a possible mechanism for the protection of phenol-degrading Pseudomonas putida P8 from substrate toxicity. Appl Environ Microbiol 58:1847–1852

    CAS  PubMed  Google Scholar 

  • Ingram LO (1976) Adaptation of mebrane lipids to alcohols. J Bacteriol 125:670–678

    Google Scholar 

  • Ingram LO (1984) Effects of alcohols on microorganisms. Adv Microbiol Physiol 25:253–300

    Google Scholar 

  • Keweloh H, Diefenbach R, Rehm H-J (1991) Increase of phenol tolerance of Escherichia coli by alterations of the fatty acid composition of the membrane lipids. Arch Microbiol 157:49–53

    Google Scholar 

  • Kitagawa K, Tateishi A, Nakano F, Matsumoto T, Marohoshi T, Tanino T, Usui, T (1986a) Generation of energy coupled with membrane-bound glucose dehydrogenase in Acinetobacter calcoaceticus. Agric Biol Chem 50:1453–1457

    Google Scholar 

  • Kitagawa K, Tateishi A, Nakano F, Matsumoto T, Marohoshi T, Tanino T, Usui, T (1986b) Sources of energy and energy coupling reactions of the active transport systems in Acinetobacter calcoaceticus. Agric Biol Chem 50:2939–2940

    Google Scholar 

  • Kleber HP, Haferburg D, Asperger O, Schmidt M, Aurich, H (1984) Aufnahme und Oxidation von Monosacchariden bei Acinetobacter calcoaceticus. Z Allg Mikrobiol 24:691–701

    Google Scholar 

  • Krulwich TA, Quirk PG, Guffanti AA (1990) Uncoupler-resistant mutants of bacteria. Microbiol Rev 54:52–65

    Google Scholar 

  • Lenke H, Pieper DH, Brun C, Knackmuss H-J (1992) Degradation of 2,4-dinitrophenol by Rhodococcus erythropolis strains, HL 24–1 and HL 24–2. Appl Environ Microbiol 58:2928–2932

    Google Scholar 

  • Loffhagen N, Babel W (1990) Influence of cytochrome composition of energy conservation of Acinetobacter calcoaceticus 69-V. Acta Biotechnol 10:551–560

    Google Scholar 

  • Lundin A, Thore A (1975) Analytical information obtainable by evaluation of the time course of firefly bioluminescence in the assay of ATP. Anal Biochem 66:47–63

    Google Scholar 

  • Matsushita K, Shinagawa E, Adachi O, Ameyama M (1988) Quinoprotein d-glucose dehydrogenase in Acinetobacter calcoaceticus LMD 79.41: the membrane-bound enzyme is distinct from the soluble enzyme. FEMS Microbiol Lett 55:53–58

    Google Scholar 

  • Mc Laughlin, SGA, Dilger, JP (1980) Transport of protons across membranes by weak acids. Phys Rev 60:825–863

    Google Scholar 

  • Miyoshi H, Takaaki N, Fujita T (1987) Quantitative relationship between protonophoric and uncoupling activities of analogs of SF6847 (2,6-di-t-butyl-4-(2',2'-dicyanovinyl)phenol). Biochim Biophys Acta 891:293–299

    Google Scholar 

  • Müller RH, Babel W (1986) Glucose as an energy donor in acetate growing Acinetobacter calcoaceticus. Arch Microbiol 144:62–66

    Google Scholar 

  • Robinson J, Cooper JM (1970) Method of determining oxygen concentrations in biological media, suitable for calibration of the oxygen electrode. Anal Biochem 33:95–102

    Google Scholar 

  • Rottenberg H (1990) Decoupling of oxidative phosphorylation and photophosphorylation. Biochim Biophys Acta 1018:1–17

    Google Scholar 

  • Schie BJ van, Hellingwerf KJ, Dijken JP van, Elferink MGL, Dijl JM van, Kuenen JG, Konings WN (1985) Energy transduction by electron transfer via a pyrrolo-quinoline quinone-dependent glucose dehydrogenase in Escherichia coli, Pseudomonas aeruginosa, and Acinetobacter calcoaceticus (var. Lwoffi). J Bacteriol 163:493–499

    Google Scholar 

  • Schie van BJ, Pronk JT, Hellingwerf KJ, Dijken JP van, Kuenen JG (1987) Glucose dehydrogenase mediated transport and ATP synthesis in Acinetobacter calcoaceticus. J Gen Microbiol 133:3427–3435

    Google Scholar 

  • Slater JH, Bull AT (1982) Environmental microbiology: biodegradation. Philos Trans R Soc Lond [Biol] 297:575–597

    Google Scholar 

  • Sullivan KH (1979) Alteration of fatty acid composition of Escherichia coli by growth in the presence of normal alcohols. J Bacteriol 138:133–138

    Google Scholar 

  • Veen HW van, Abee T, Kortstee GJJ, Konings WN, Zehnder AJB (1993) Characterization of two phosphate transport systems in Acinetobacter johnsonii 210A. J Bacteriol 175:200–206

    Google Scholar 

  • Yamada M, Sumi K, Matsushita K, Adachi O, Yamada Y (1993) Topological analysis of quinoprotein glucose dehydrogenase in Escherichia coli and its ubiquinone-binding site. J Biol Chem 268:12812–12817

    Google Scholar 

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Loffhagen, N., Härtig, C. & Babel, W. The glucose dehydrogenase-mediated energization of Acinetobacter calcoaceticus as a tool for evaluating its susceptibility to, and defence against, hazardous chemicals. Appl Microbiol Biotechnol 42, 738–743 (1995). https://doi.org/10.1007/BF00171955

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  • DOI: https://doi.org/10.1007/BF00171955

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