1887

Abstract

The draft genome sequence of NBRC 14818 was determined by whole-genome shotgun sequencing and the transcriptome profile in cells exponentially grown on ethanol, acetate or glucose was analysed by using a DNA microarray. The genes for all enzymes that constitute the complete tricarboxylic acid (TCA) cycle and glyoxylate pathway were identified in the genome. The TCA cycle genes showed higher expression levels in cells grown on acetate or glucose and the glyoxylate pathway genes were significantly induced by ethanol or acetate. Many SOS-response genes were upregulated in cells grown on ethanol, indicating that ethanol provoked damage of DNA and proteins. The superoxide dismutase and catalase genes showed high expression levels in culture on glucose, indicating that oxidation of glucose induced oxidative stress. NBRC 14818 was found to have a highly branched respiratory chain. The genes for two type I and one type II NADH dehydrogenase were identified. The genes for one of the type I enzymes were highly expressed when cells were grown on acetate or glucose, but were significantly downregulated in culture on ethanol, probably because ubiquinones were directly reduced by pyrroloquinoline quinone-dependent alcohol dehydrogenase. Four sets of the genes for quinol oxidases, one -type (BO3), one -type and two cyanide-insensitive-types (CIOs), were identified in the genome. The genes for BO3, which might have proton-pumping activity, were highly expressed under the conditions tested, but were downregulated in the glucose culture. In contrast, the genes for one of the CIOs were significantly upregulated in cells grown on glucose. The two CIOs, which are expected to have lower energy-coupling efficiency, seemed to have a higher contribution in glucose-grown cells. These results indicate that energy conservation efficiency is fine-tuned by changing the respiratory components according to the growth conditions in cells.

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2011-03-01
2024-04-25
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References

  1. Asai T. 1968 Acetic Acid Bacteria: Classification and Biochemical Activities Tokyo: University of Tokyo Press;
    [Google Scholar]
  2. Azuma Y., Hosoyama A., Matsutani M., Furuya N., Horikawa H., Harada T., Hirakawa H., Kuhara S., Matsushita K. other authors 2009; Whole-genome analyses reveal genetic instability of Acetobacter pasteurianus . Nucleic Acids Res 37:5768–5783
    [Google Scholar]
  3. Badger J. H., Olsen G. J. 1999; critica: coding region identification tool invoking comparative analysis. Mol Biol Evol 16:512–524
    [Google Scholar]
  4. Bekker M., de Vries S., Ter Beek A., Hellingwerf K. J., Teixeira de Mattos M. J. 2009; Respiration of Escherichia coli can be fully uncoupled via the nonelectrogenic terminal cytochrome bd -II oxidase. J Bacteriol 191:5510–5517
    [Google Scholar]
  5. Bertalan M., Albano R., de Pádua V., Rouws L., Rojas C., Hemerly A., Teixeira K., Schwab S., Araujo J. other authors 2009; Complete genome sequence of the sugarcane nitrogen-fixing endophyte Gluconacetobacter diazotrophicus Pal5. BMC Genomics 10:450
    [Google Scholar]
  6. Bolstad B. M., Irizarry R. A., Astrand M., Speed T. P. 2003; A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19:185–193
    [Google Scholar]
  7. Calhoun M. W., Oden K. L., Gennis R. B., Teixeira de Mattos M. J., Neijssel O. M. 1993; Energetic efficiency of Escherichia coli : effects of mutations in components of the aerobic respiratory chain. J Bacteriol 175:3020–3025
    [Google Scholar]
  8. Chinnawirotpisan P., Matsushita K., Toyama H., Adachi O., Limtong S., Theeragool G. 2003; Purification and characterization of two NAD-dependent alcohol dehydrogenases (ADHs) induced in the quinoprotein ADH-deficient mutant of Acetobacter pasteurianus SKU1108. Biosci Biotechnol Biochem 67:958–965
    [Google Scholar]
  9. Cunningham L., Pitt M., Williams H. D. 1997; The cioAB genes from Pseudomonas aeruginosa code for a novel cyanide-insensitive terminal oxidase related to the cytochrome bd quinol oxidases. Mol Microbiol 24:579–591
    [Google Scholar]
  10. Delcher A. L., Harmon D., Kasif S., White O., Salzberg S. L. 1999; Improved microbial gene identification with glimmer. Nucleic Acids Res 27:4636–4641
    [Google Scholar]
  11. Deppenmeier U., Hoffmeister M., Prust C. 2002; Biochemistry and biotechnological applications of Gluconobacter strains. Appl Microbiol Biotechnol 60:233–242
    [Google Scholar]
  12. el-Mansi E. M., Holms W. H. 1989; Control of carbon flux to acetate excretion during growth of Escherichia coli in batch and continuous cultures. J Gen Microbiol 135:2875–2883
    [Google Scholar]
  13. Greenberg D. E., Porcella S. F., Zelazny A. M., Virtaneva K., Sturdevant D. E., Kupko J. J. III, Barbian K. D., Babar A., Dorward D. W. other authors 2007; Genome sequence analysis of the emerging human pathogenic acetic acid bacterium Granulibacter bethesdensis . J Bacteriol 189:8727–8736
    [Google Scholar]
  14. Gupta A., Singh V. K., Qazi G. N., Kumar A. 2001; Gluconobacter oxydans : its biotechnological applications. J Mol Microbiol Biotechnol 3:445–456
    [Google Scholar]
  15. Hernandez D., François P., Farinelli L., Osteras M., Schrenzel J. 2008; De novo bacterial genome sequencing: millions of very short reads assembled on a desktop computer. Genome Res 18:802–809
    [Google Scholar]
  16. Irizarry R. A., Bolstad B. M., Collin F., Cope L. M., Hobbs B., Speed T. P. 2003; Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31:e15
    [Google Scholar]
  17. Ishikawa M., Okamoto-Kainuma A., Jochi T., Suzuki I., Matsui K., Kaga T., Koizumi Y. 2010a; Cloning and characterization of grpE in Acetobacter pasteurianus NBRC 3283. J Biosci Bioeng 109:25–31
    [Google Scholar]
  18. Ishikawa M., Okamoto-Kainuma A., Matsui K., Takigishi A., Kaga T., Koizumi Y. 2010b; Cloning and characterization of clpB in Acetobacter pasteurianus NBRC 3283. J Biosci Bioeng 110:69–71
    [Google Scholar]
  19. Jucker W., Ettlinger L. 1985; The inhibition of acetate oxidation by ethanol in Acetobacter aceti . Arch Microbiol 143:283–289
    [Google Scholar]
  20. Kondo K., Horinouchi S. 1997; Characterization of the genes encoding the three-component membrane-bound alcohol dehydrogenase from Gluconobacter suboxydans and their expression in Acetobacter pasteurianus . Appl Environ Microbiol 63:1131–1138
    [Google Scholar]
  21. Kornberg H. L., Krebs H. A. 1957; Synthesis of cell constituents from C2-units by a modified tricarboxylic acid cycle. Nature 179:988–991
    [Google Scholar]
  22. Krajewski V., Simic P., Mouncey N. J., Bringer S., Sahm H., Bott M. 2010; Metabolic engineering of Gluconobacter oxydans for improved growth rate and growth yield on glucose by elimination of gluconate formation. Appl Environ Microbiol 76:4369–4376
    [Google Scholar]
  23. Leif H., Sled V. D., Ohnishi T., Weiss H., Friedrich T. 1995; Isolation and characterization of the proton-translocating NADH : ubiquinone oxidoreductase from Escherichia coli . Eur J Biochem 230:538–548
    [Google Scholar]
  24. Marmur J. 1961; A procedure for the isolation of deoxyribonucleic acid from microorganisms. J Mol Biol 3:208–218
    [Google Scholar]
  25. Matsushita K., Nagatani Y., Shinagawa E., Adachi O., Ameyama M. 1989; Effect of extracellular pH on the respiratory chain and energetics of Gluconobacter suboxydans . Agric Biol Chem 53:2895–2902
    [Google Scholar]
  26. Mogi T., Ano Y., Nakatsuka T., Toyama H., Muroi A., Miyoshi H., Migita C. T., Ui H., Shiomi K. other authors 2009; Biochemical and spectroscopic properties of cyanide-insensitive quinol oxidase from Gluconobacter oxydans . J Biochem 146:263–271
    [Google Scholar]
  27. Mullins E. A., Francois J. A., Kappock T. J. 2008; A specialized citric acid cycle requiring succinyl-coenzyme A (CoA) : acetate CoA-transferase (AarC) confers acetic acid resistance on the acidophile Acetobacter aceti . J Bacteriol 190:4933–4940
    [Google Scholar]
  28. Nakano S., Fukaya M., Horinouchi S. 2004; Enhanced expression of aconitase raises acetic acid resistance in Acetobacter aceti . FEMS Microbiol Lett 235:315–322
    [Google Scholar]
  29. Okamoto-Kainuma A., Yan W., Fukaya M., Tukamoto Y., Ishikawa M., Koizumi Y. 2004; Cloning and characterization of the dnaKJ operon in Acetobacter aceti . J Biosci Bioeng 97:339–342
    [Google Scholar]
  30. Okamoto-Kainuma A., Ehata Y., Ikeda M., Osono T., Ishikawa M., Kaga T., Koizumi Y. 2008; Hydrogen peroxide resistance of Acetobacter pasteurianus NBRC3283 and its relationship to acetic acid fermentation. Biosci Biotechnol Biochem 72:2526–2534
    [Google Scholar]
  31. Prust C., Hoffmeister M., Liesegang H., Wiezer A., Fricke W. F., Ehrenreich A., Gottschalk G., Deppenmeier U. 2005; Complete genome sequence of the acetic acid bacterium Gluconobacter oxydans . Nat Biotechnol 23:195–200
    [Google Scholar]
  32. Puustinen A., Finel M., Virkki M., Wikström M. 1989; Cytochrome o ( bo ) is a proton pump in Paracoccus denitrificans and Escherichia coli . FEBS Lett 249:163–167
    [Google Scholar]
  33. Puustinen A., Finel M., Haltia T., Gennis R. B., Wikström M. 1991; Properties of the two terminal oxidases of Escherichia coli . Biochemistry 30:3936–3942
    [Google Scholar]
  34. Saeki A., Taniguchi M., Matsushita K., Toyama H., Theeragool G., Lotong N., Adachi O. 1997; Microbiological aspects of acetate oxidation by acetic acid bacteria, unfavorable phenomena in vinegar fermentation. Biosci Biotechnol Biochem 61:317–323
    [Google Scholar]
  35. Saeki A., Matsushita K., Takeno S., Taniguchi M., Toyama H., Theeragool G., Lotong N., Adachi O. 1999; Enzymes responsible for acetate oxidation by acetic acid bacteria. Biosci Biotechnol Biochem 63:2102–2109
    [Google Scholar]
  36. Soemphol W., Adachi O., Matsushita K., Toyama H. 2008; Distinct physiological roles of two membrane-bound dehydrogenases responsible for d-sorbitol oxidation in Gluconobacter frateurii . Biosci Biotechnol Biochem 72:842–850
    [Google Scholar]
  37. Tamaki T., Fukaya M., Takemura H., Tayama K., Okumura H., Kawamura Y., Nishiyama M., Horinouchi S., Beppu T. 1991; Cloning and sequencing of the gene cluster encoding two subunits of membrane-bound alcohol-dehydrogenase from Acetobacter polyoxogenes . Biochim Biophys Acta 1088:292–300
    [Google Scholar]
  38. Wikström M., Bogachev A., Finel M., Morgan J. E., Puustinen A., Raitio M., Verkhovskaya M., Verkhovsky M. I. 1994; Mechanism of proton translocation by the respiratory oxidases. The histidine cycle. Biochim Biophys Acta 1187106–111
    [Google Scholar]
  39. Yakushi T., Matsushita K. 2010; Alcohol dehydrogenase of acetic acid bacteria: structure, mode of action, and applications in biotechnology. Appl Microbiol Biotechnol 86:1257–1265
    [Google Scholar]
  40. Yamada H., Takashima E., Konishi K. 2007; Molecular characterization of the membrane-bound quinol peroxidase functionally connected to the respiratory chain. FEBS J 274:853–866
    [Google Scholar]
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