1887

Abstract

Summary: Anaerobic, but not aerobic, cultures of K-12 catalysed the rapid nitrosation of the model substrate 2,3-diaminonaphthalene when incubated with nitrite. Formate and lactate were effective electron donors for the nitrosation reaction, which was inhibited by nitrate. Optimal growth conditions for the expression of nitrosation activity by various strains and mutants were determined. Highest activities were found with bacteria that had been grown anaerobically in a minimal medium rather than in Lennox broth, with glycerol and fumarate rather than glucose as the main carbon and energy source, and in the presence of a low concentration of nitrate. Bacteria harvested in the early exponential phase were more active than those harvested in later stages of growth. Well-characterized mutants defective in the synthesis of one or more anaerobically induced electron transfer chains were screened for nitrosation activity under these optimal growth conditions: only the respiratory nitrate reductase encoded by the operon was implicated as a major contributor to nitrosation activity. Due to the limited sensitivity of the assays currently available, a minor contribution from the two alternative nitrate reductases or even other molybdoproteins could not be excluded. The role of formate in nitrosation was complex and was clearly not limited simply to that of an electron donor in the bacterial reduction of nitrite to nitric oxide: at least two further, chemical roles were inferred. This extensive study of more than 400 independent cultures of K-12 and its derivatives resolved some, but not all, of the apparently conflicting data in the literature concerning nitrosation catalysed by enteric bacteria.

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1997-08-01
2024-03-29
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References

  1. Berg B. L., Stewart V. 1990; Structural genes for nitrate-inducible formate dehydrogenase in Escherichia coli K-12. Genetics 125:691–702
    [Google Scholar]
  2. Berg B. L., Li J., Heider 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]
  3. Blasco F., Nunzi F., Pommier J., Brasseur R., Chippaux M., Giordano G. 1992; Formation of active heterologous nitrate reductases between nitrate reductases A and Z in Escherichia coli. . Mol Microbiol 6:209–219
    [Google Scholar]
  4. Bӧhm R., Sauter M., Bӧck A. 1990; Nucleotide sequence and expression of an operon in Escherichia coli coding for formate hydrogenlyase components. Mol Microbiol 4:231–243
    [Google Scholar]
  5. Calmels S., Ohshima H., Vincent P., Gounot A.-M., Bartsch H. 1985; Screening of microorganisms for nitrosation catalysis at pH 7 and kinetic studies on nitrosamine formation from secondary amines by E. coli strains. Carcinogensis 6:911–915
    [Google Scholar]
  6. Calmels S., Ohshima H., Rosenkranz H., McCoy E., Bartsch H. 1987; Biochemical studies on the catalysis of nitrosation by bacteria. Carcinogenesis 8:1085–1088
    [Google Scholar]
  7. Calmels S., Ohshima H., Bartsch H. 1988; Nitrosamine formation by denitrifying and non-denitrifying bacteria: implication of nitrite reductase and nitrate reductase in nitrosation catalysis. J Gen Microbiol 134:221–226
    [Google Scholar]
  8. Casadaban M. J., 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]
  9. Crooke H., Cole J. 1995; The biogenesis of c-type cytochromes in Escherichia coli requires a membrane-bound protein, DipZ, with a protein disulphide isomerase-like domain. Mol Microbiol 15:1139–1150
    [Google Scholar]
  10. 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]
  11. De Bernadis G., Guadagni S., Pistoria M. A., Amicucci G., Masci C., Herfath C., Agnifili A., Carboni M. 1983; Gastric juice, nitrite and bacteria in gastroduodenal disease and resected stomach. Tumori 96:231–237
    [Google Scholar]
  12. Enoch H. G., Lester R. L. 1975; The purification and properties of formate dehydrogenase and nitrate reductase from Escherichia coli. . J Biol Chem 250:6693–6705
    [Google Scholar]
  13. Forsythe S. J., Dolby J. M., Webster A. D. B., Cole J. A. 1988; Nitrate- and nitrite-reducing bacteria in the achlorhydric stomach. J Med Microbiol 25:253–259
    [Google Scholar]
  14. Gest H., Peck H. D. 1955; Mechanism of the hydrogenlyase system. J Bacteriol 70:326–334
    [Google Scholar]
  15. Gray C. T., Gest H. 1965; Biological formation of molecular hydrogen. Science 148:186–192
    [Google Scholar]
  16. Griffiths L., Cole J. A. 1987; Lack of redox control of the anaerobically-induced nirB gene of Escherichia coli K12. Arch Microbiol 147:364–369
    [Google Scholar]
  17. Grove J., Tanapongpipat S., Thomas G., Griffiths L., Crooke H., Cole J. 1996; Escherichia coli K-12 genes essential for the synthesis of c-type cytochromes and a third nitrate reductase located in the periplasm. Mol Microbiol 19:467–481
    [Google Scholar]
  18. Hill M. J., Hawksworth G., Tattersall U. 1973; Bacteria, nitrosamines and cancer of the stomach. Brit J Cancer 28:562–567
    [Google Scholar]
  19. Hussain H., Grove J., Griffiths L., Busby S., Cole J. 1994; A seven gene operon essential for formate-dependent nitrite reduction to ammonia by enteric bacteria. Mol Microbiol 12:153–163
    [Google Scholar]
  20. Ji X. B., Hollocher T. C. 1988; Mechanism for nitrosation of 2,3-diaminonaphthalene by Escherichia coli: enzymatic production of NO followed by O2-dependent chemical nitrosation. Appl Environ Microbiol 54:1791–1794
    [Google Scholar]
  21. Kunisaki N., Hayashi M. 1979; Formation of N-nitrosoamines from secondary amines and nitrite by resting cells of Escherichia coli B. Appl Environ Microbiol 37:279–282
    [Google Scholar]
  22. Leach S. A. 1995; N-nitroso compounds. . In Role of Gut Bacteria in Human Toxicology and Pharmacology pp. 69–78 . Edited by Hill M. J. London: Taylor & Francis;
    [Google Scholar]
  23. Leach S. A., Cook A. R., Challis B. C., Hill M., Thompson M. 1979; Bacterial mediated N-nitrosamine reactions and endogenous formation of N-nitroso compounds. In Relevance of N-Nitroso Compounds to Human Cancer: Exposure and Mechanisms. , pp. 396–399 . Edited by Bartsch H., O’Neill I. K., Schuite-Herman R. Lyon: International Agency for Research on Cancer;
    [Google Scholar]
  24. Leach S. A., Thompson M. H., Hill M. J. 1987; Bacterially catalysed N-nitrosation reactions and their relative importance in the human stomach. Carcinogenesis 8:1907–1912
    [Google Scholar]
  25. Lester R. L., DeMoss J. 1971; Effects of molybdenum and selenite on formate and nitrate metabolism in Escherichia coli. . J Bacteriol 105:1006–1014
    [Google Scholar]
  26. OʹDonnell C. M., Edwards C. 1992; Nitrosating activity in Escherichia coli. . FEMS Microbiol Lett 95:95–98
    [Google Scholar]
  27. Peck H. D. Jr, Gest H. 1957; Formic dehydrogenase and the hydrogenlyase enzyme complex in coli-aerogenes bacteria. J Bacteriol 73:706–721
    [Google Scholar]
  28. Pinsent J. 1954; The need for selenite and molybdate in the formation of formate dehydrogenase by members of the Coliaerogenese group of bacteria. Biochem J 57:10–16
    [Google Scholar]
  29. Rabin R. S., Stewart V. 1993; Dual response regulators (NarL and NarP) interact with dual sensors (NarX and NarQ) to control nitrate- and nitrite-regulated gene expression in Escherichia coli K-12. J Bacteriol 175:3259–3268
    [Google Scholar]
  30. Ralt D., Tannenbaum S. R. 1981; Role of bacteria in nitrosamine formation: N-nitroso compounds. Adv Chem Ser 174:159–164
    [Google Scholar]
  31. Ralt D„, Wishnok J. A., Fitts S., Tannenbaum S. R. 1988; Bacterial catalysis of nitrosation: involvement of the nar operon of Escherichia coli. . J Bacteriol 170:359–364
    [Google Scholar]
  32. Reed P. I., Haines K., Smith P. L. R., House F. R., Walters C. L. 1981; Gastric juice N-nitrosamines in health and gastroduodenal disease. Lancet 2:550–552
    [Google Scholar]
  33. Ruiz-Herrera J., DeMoss J. A. 1969; Nitrate reductase complex of Escherichia coli K-12: participation of specific formate dehydrogenase and cytochrome b 1 components in nitrate reduction. J Bacteriol 99:720–729
    [Google Scholar]
  34. Sauter M., Bӧhm R., Bȣck A. 1992; Mutational analysis of the operon (hyc) determining hydrogenase 3 formation in Escherichia coli. . Mol Microbiol 6:1523–1532
    [Google Scholar]
  35. Sawers G., Heider J., Zehelein E., Bӧck A. 1991; Expression and operon structure of the sel genes of Escherichia coli and identification of a third selenium-containing formate dehydrogenase isoenzyme. J Bacteriol 173:4983–4993
    [Google Scholar]
  36. Stewart V. 1993; Nitrate regulation of anaerobic respiratory gene expression in Escherichia coli. . Mol Microbiol 9:425–434
    [Google Scholar]
  37. Taverna P. & Sedgwick B. 1996; Generation of an endogenous DNA-methylating agent by nitrosation in Escherichia coli. . J Bacteriol 178:5105–5111
    [Google Scholar]
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