1887

Abstract

Summary: The effect of the addition of trimethylamine -oxide (TMAO) in the growth medium on anaerobic fermentative and respiratory pathways was examined. Formate dehydrogenase H (FDH-H) activity was totally repressed by the addition of 40 mM TMAO, whereas the overall hydrogenase (HYD) activity was reduced by 25%. Accordingly, expression of operon fusions with the and structural genes specifying FDH-H and HYD3 was reduced sevenfold and eightfold, respectively, leading to suppression of an active formate hydrogenlyase system. In contrast, global respiratory formate-dependent phenazine methosulphate reductase (FDH-PMS) activity, which consists of both the major anaerobic FDH-N enzyme and the aerobic FDH-Z isoenzyme, was increased approximately twofold. This was corroborated by a 2.5-fold stimulation of the sole transcriptional fusion which reflects the synthesis of the respiratory aerobic FDH-Z enzyme. In or mutants lacking either FDH-PMS activity or TMAO reductase (TOR) activity, the formate hydrogenlyase pathway was no longer inhibited by TMAO. In addition, introduction of 30 mM formate in the growth medium was found to relieve the repressive effect of TMAO in the wild-type strain. When TMAO was added as terminal electron acceptor a significant enhancement of anaerobic growth was observed with the wild-type strain and the mutant. It was associated with the concomitant suppression of the formate hydrogenlyase enzymes. This was in contrast to the and mutants whose growth pattern and fermentative enzymes remained unaffected. Taken together, these results strongly suggest that formate-dependent reduction of TMAO via FDH-N and TOR reduces the amount of formate available for induction of the formate hydrogenlyase pathway.

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1997-08-01
2021-05-18
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References

  1. Abaibou H., Pommier J., Benoit S., Giordano G., Mandrand-Berthelot M. A. 1995; Expression and characterization of the Escherichia coli fdo locus and a possible physiological role for aerobic formate dehydrogenase. J Bacteriol 177:7141–7149
    [Google Scholar]
  2. Barrett E. L., Kwan H. S. 1985; Bacterial reduction of trimethylamine oxide. Annu Rev Microbiol 39:131–149
    [Google Scholar]
  3. Begg Y. A., Whyte J. N., Haddock B. A. 1977; The identification of mutants of Escherichia coli deficient in formate dehydrogenase and nitrate reductase activities using dye indicator plates. FEMS Microbiol Lett 2:47–50
    [Google Scholar]
  4. Berg B. L., Stewart V. 1990; Structural genes for nitrate-inducible formate dehydrogenase in Escherichia coli K-12. Genetics 125:691–702
    [Google Scholar]
  5. Berg B. L., Li J., Heide J., Stewart V. 1991; Nitrate-inducible formate dehydrogenase in Escherichia coli K-12: I. Nucleotide sequence of the fdnGHI operon and evidence that opal (UGA) encodes selenocysteine. J Biol Chem 266:22380–22385
    [Google Scholar]
  6. Bilous P. T., Weiner J. H. 1988; Molecular cloning and expression of the Escherichia coli dimethyl sulfoxide reductase operon. J Bacteriol 170:1511–1518
    [Google Scholar]
  7. Blasco F., Iobbi C., Giordano G., Chippaux M., Bonnefoy V. 1989; Nitrate reductase of Escherichia coli: completion of the nucleotide sequence of the nar operon and reassessment of the role of the α and β subunits in iron binding and electron transfer. Mol Gen Genet 218:249–256
    [Google Scholar]
  8. Blasco F., Iobbi C., Ratouchniak J., Bonnefoy V., Chippaux M. 1990; Nitrate reductases of Escherichia coli: sequence of the second nitrate reductase and comparison with that encoded by narGHJI operon. Mol Gen Genet 222:104–111
    [Google Scholar]
  9. Böck A., Sawers G. 1996; Fermentation. . In Escherichia coli and Salmonella: Cellular and Molecular Biology 2nd edn, pp 262–282 . Edited by Neidhardt F. C. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  10. Casadaban M., Cohen S. N. 1979; Lactose genes fused to exogenous promoters in one step using a Mu-lac bacteriophage: in vivo probe for transcriptional control sequences. Proc Natl Acad Sci USA 76:4530–4533
    [Google Scholar]
  11. Cotter P. A., Gunsalus R. P. 1989; Oxygen, nitrate, and molybdenum regulation of dmsABC gene expression in Escherichia coli. . J Bacteriol 171:3817–3823
    [Google Scholar]
  12. Darwin A., Tormay P., Page L., Griffiths L., Cole J. 1993; Identification of the formate dehydrogenases and genetic determinants of formate-dependent nitrite reduction by Escherichia coli K12. J Gen Microbiol 139:1829–1840
    [Google Scholar]
  13. Daruwala R., Meganathan R. 1991; Dimethyl sulfoxide reductase is not required for trimethylamine N-oxide reduction in Escherichia coli. . FEMS Microbiol Lett 83:255–260
    [Google Scholar]
  14. Gennis R. B., Stewart V. 1996; Respiration. . In Escherichia coli and Salmonella: Cellular and Molecular Biology 2nd edn, pp. 217–261 . Edited by Neidhardt F. C. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  15. Iobbi-Nivol C., Santini C. L., Bonnefoy V., Giordano G. 1987; Biochemical and immunological evidence for a second nitrate reductase in Escherichia coli K-12. Eur J Biochem 168:451–459
    [Google Scholar]
  16. Iobbi-Nivol C., Santini C. L., Blasco F., Giordano G. 1990; Purification and further characterization of the second nitrate reductase of Escherichia coli K-12. Eur J Biochem 188:679–687
    [Google Scholar]
  17. Jones H. M., Gunsalus R. P. 1987; Regulation of Escherichia coli fumarate reductase (frdABCD) operon expression by respiratory electron acceptors and the fnr gene product. J Bacteriol 169:3340–3349
    [Google Scholar]
  18. Jourlin C., Bengrine A., Chippaux M., Méjean V. 1996a; An unorthodox sensor protein (TorS) mediates the induction of the tor structural genes in response to trimethylamine N-oxide in Escherichia coli. . Mol Microbiol 20:1297–1306
    [Google Scholar]
  19. Jourlin C., Simon G., Pommier J., Chippaux M., Méjean V. 1996b; The periplasmic TorT protein is required for trimethylamine-N-oxide reductase gene induction in Escherichia coli. . J Bacteriol 178:1219–1223
    [Google Scholar]
  20. Miller J. H. 1992; Use of P1clr100 . . In A Short Course in Bacterial Genetics. A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria pp. 275–278 Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  21. Pascal M. C., Burini J. F., Ratouchniak J., Chippaux M. 1982; Regulation of the nitrate reductase operon: effect of mutations in chlA, B, D and E genes. Mol Gen Genet 188:103–106
    [Google Scholar]
  22. Pascal M. C., Burini J. F., Chippaux M. 1984; Regulation of trimethylamine N-oxide (TMAO) reductase of Escherichia coli K-12: analysis of tor::MudI fusion. Mol Gen Genet 195:351–355
    [Google Scholar]
  23. Pecher A., Zinoni F., Jatisatienr C., Wirth R., Hennecke H., Böck A. 1983; On the redox control of synthesis of anaerobically induced enzymes in enterobacteriaceae. Arch Microbiol 136:131–136
    [Google Scholar]
  24. Plunkett G., Burland V., Daiels D. L., Blattner F. R. 1993; Analysis of the Escherichia coli genome. III. DNA sequence of the region from 87.2 to 89.2 minutes. Nucleic Acids Res 21:3391–3398
    [Google Scholar]
  25. Pommier J., Mandrand-Berthelot M. A., Holt S. E., Boxer D. H., Giordano G. 1992; A second phenazine methosulphate-linked formate dehydrogenase isoenzyme in Escherichia coli. . Biochim Biophys Acta 1107:305–313
    [Google Scholar]
  26. Rossmann R., Sawers G., Böck A. 1991; Mechanism of regulation of the formate-hydrogenlyase pathway by oxygen, nitrate, and pH: definition of the formate regulon. Mol Microbiol 5:2807–2814
    [Google Scholar]
  27. Rossmann R., Maier T., Lottspeich F., Böck A. 1995; Characterisation of a protease from Escherichia coli involved in hydrogenase maturation. Eur J Biochem 227:545–550
    [Google Scholar]
  28. Sambasivarao D., Weiner J. H. 1991; Differentiation of the multiple S- and N-oxide-reducing activities of Escherichia coli. . Curr Microbiol 23:105–110
    [Google Scholar]
  29. Sauter M., Böhm R., Böck A. 1992; Mutational analysis of the operon (hyc) determining hydrogenase 3 formation in Escherichia coli. . Mol Microbiol 6:1523–1532
    [Google Scholar]
  30. Schlindwein C., Giordano G., Santini C. L., Mandrand M. A. 1990; Identification and expression of the Escherichia coli fdhD and fdhE genes, which are involved in the formation of respiratory formate dehydrogenase. J Bacteriol 172:6112–6121
    [Google Scholar]
  31. Silvestro A., Pommier J., Pascal M. C., Giordano G. 1989; The inducible trimethylamine N-oxide reductase of Escherichia coli K-12: its localization and inducers. Biochim Biophys Acta 994:208–216
    [Google Scholar]
  32. Simon G., Méjean V., Jourlin C., Chippaux M., Pascal M. C. 1994; The torR gene of Escherichia coli encodes a response regulator protein involved in the expression of the trimethylamine-N-oxide reductase genes. J Bacteriol 176:5601–5606
    [Google Scholar]
  33. Sodergren E. J., DeMoss J. A. 1988; narI region of nitrate reductase (nar) operon contains two genes in Escherichia coli. . J Bacteriol 170:1721–1729
    [Google Scholar]
  34. Stewart V. 1993; Nitrate regulation of anaerobic respiratory gene expression in Escherichia coli. . Mol Microbiol 9:425–434
    [Google Scholar]
  35. Stewart V., Lin J. T., Berg B. L. 1991; Genetic evidence that genes fdhD and fdhE do not control synthesis of formate dehydrogenase-N in Escherichia coli K-12. J Bacteriol 173:4417–4423
    [Google Scholar]
  36. Weiner J. H., Macisaac D. P., Bishop R. E., Bilous P. T. 1988; Purification and properties of Escherichia coli DMSO reductase, an iron–sulfur molybdoenzyme with broad substrate specificity. J Bacteriol 170:1505–1510
    [Google Scholar]
  37. Wu L. F., Mandrand-Berthelot M. A. 1986; Genetic and physiological characterization of new Escherichia coli mutants impaired in hydrogenase activity. Biochimie 68:167–179
    [Google Scholar]
  38. Wu L. F., Mandrand-Berthelot M. A. 1987; Regulation of the fdhF gene encoding the selenopolypeptide for benzyl viologen-linked formate dehydrogenase in Escherichia coli. . Mol Gen Genet 209:129–134
    [Google Scholar]
  39. Yamamoto I., Ishimoto M. 1978; Hydrogen-dependent growth of Escherichia coli in anaerobic respiration and the presence of hydrogenases with different functions. J Biochem 84:673–679
    [Google Scholar]
  40. Zinoni F., Birkmann A., Stadman T. C., Böck A. 1986; Nucleotide sequence and expression of selenocysteine-containing polypeptide of formate dehydrogenase (formate-hydrogen-lyase-linked) from Escherichia coli. . Proc Natl Acad Sci USA 83:4650–4654
    [Google Scholar]
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