Physiology, Biochemistry and Genetics of Nitrate Dissimilation to Ammonia

  • J. A. Cole
Part of the Federation of European Microbiological Societies Symposium Series book series (FEMS, volume 56)

Abstract

Many textbooks, symposium publications and even edited papers in leading journals present denitrification as the only dissimilatory pathway for bacterial NO 3 reduction. In fact, the rapid, dissimilatory reduction to NH 4 + by fermentative bacteria was documented many years ago (see, for example, Woods, 1938). As the limited literature on NO 3 dissimilation to NH 4 + published before 1988 has recently been reviewed extensively (Cole, 1988; 1989), this article will focus on recent developments which confirm or conflict with the previous conclusions. Although the practical importance of denitrification by essentially respiratory bacteria is beyond doubt, Figure 1 presents it — possibly for the first time — in the context of the emerging diversity of enzymes which have evolved to dissimilate NO 3 and NO 2 in different bacterial groups.

Keywords

Nitrate Reductase Nitrite Reductase Anaerobic Growth Nitrite Reduction Fermentative Bacterium 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abou-Jaoude, A., Chippaux, M., and Pascal, M.-C., 1979a, Formate-nitrite reduction in Escherichia coli K12. 1. Physiological study of the system, Eur. J. Biochem., 95: 309.PubMedCrossRefGoogle Scholar
  2. Abou-Jaoude, A., Pascal, M.C. and Chippaux, M., 1979b, Formate-nitrite reduction in Escherichia Coli K12. 2. Identification of components involved in the electron transfer, Eur. J. Biochem.. 95: 315.Google Scholar
  3. Bell, A.I., Gaston, K.L., Cole, J.A. and Busby, S.J.W, 1989, Cloning of binding sequences for the Escherichia coli transcription activators, FNR and CRP; location of bases involved i discrimination between FNR and CRP. Nucl. Acids Res. 17: 3865.PubMedCrossRefGoogle Scholar
  4. Bielkie, A., and Ketchum, P.A., 1989, Purification of nitrate reductase from Xanthomonas maltophila. Abstract K-121. Abstracts of the Annual Meeting of the American Society for Microbiology. p. 265.Google Scholar
  5. Bonnefoy, V., Burini, J.F., Giordano, G., Pascal, M.-C. and Chippaux, M., 1987, Presence in the “silent” terminus region of Escherichia coli K12 chromosome of cryptic gene(s) encoding a new nitrate reductase, Mol. Microbiol., 1: 143.PubMedCrossRefGoogle Scholar
  6. Caskey, W.H., and Tiedje, J.M., 1979, Evidence for clostridia as agents of dissimilatory reduction of nitrate to ammonium in soil, Soil Sci. Soc. Am. J., 43: 931.CrossRefGoogle Scholar
  7. Cole, J.A., 1968. Cytochrome ç552 and nitrite reduction in Escherichia coli, Biochimica et Biophysica Acta., 162: 356.PubMedCrossRefGoogle Scholar
  8. Cole, J.A., 1988, Assimilatory and dissimilatory reduction of nitrate to ammonia. In: “The Nitrogen and Sulphur Cycles” Eds. Cole, J.A., and Ferguson, S.J., Symposium 42, The Society for General Microbiology, Cambridge University Press, U.K.Google Scholar
  9. Cole, J.A., 1989, Physiology, biochemistry and genetics of nitrite reduction by Escherichia coli, In: “Molecular and Genetic Aspects of Nitrate Assimilation” Eds. Wray, J.L., and Kinghorn, J.R., Oxford University Press, U.K.Google Scholar
  10. Cole, J.A., and Brown, C.M., 1980, Nitrite reduction to ammonium by fermentative bacteria: a short circuit in the biological nitrogen cycle, FEMS Microbiol. Lett., 7: 65.CrossRefGoogle Scholar
  11. Cole, J.A., and Ward, F.B., 1973, Nitrite reductase-deficient mutants of Escherichia coli K12, J. Gen. Microbiol., 76: 21.PubMedCrossRefGoogle Scholar
  12. Coleman, K.J., Cornish-Bowden, A., and COLE, J.A., 1978a, Purification and properties of nitrite reductase from Escherichia coli K12, Biochem. J. 175, 483.PubMedGoogle Scholar
  13. Coleman, K.J., Cornish-Bowden, A., and Cole J.A., 1978b, Activation of nitrite reductase from Escherichia coli K12 by oxidized nicotine-adenine dinucleotide, Biochem. J., 175: 495.PubMedGoogle Scholar
  14. Drummund, M.H., Whitty, P.W., and Wootton, J.C., 1986, Sequence and domain relationships of ntrC and nifA from Klebsiella pneumoniae; homologies to other regulatory proteins, EMBO J., 5: 441.Google Scholar
  15. Fazzolari Correa, E., Mariotti, A., and Germon, J.C., 1989, Dissimilatory nitrate reduction into ammonium by Enterobacter amnigenus: ability and competition with denitrification with Agrobacterium radiobacter, Abstract N-83, Abstracts of the Annual Meeting of the American Society for Microbiology, p. 299.Google Scholar
  16. Forsythe, S.J., Dolby, J.M., Webster, A.D.B., and Cole, J.A., 1988Google Scholar
  17. Nitrate-and nitrite-reducing bacteria in the achlorhydric stomach, J. Med. Microbiol., 25: 253.Google Scholar
  18. Fujita, T., and Sato, R., 1966a, Studies on soluble cytochromes in Enterobacteriaceae III. Localization of cytochrome ç552 in the surface layer of cells, J. Biochem., 60: 568.Google Scholar
  19. Fujita, T., and Sato, R., 1966b, Studies on soluble cytochromes in Enterobacteriaceae IV. Possible involvement of cytochrome _c552 in anaerobic nitrite metabolism, The Journal of Biochemistry, 60: 691.Google Scholar
  20. Fujita, T., and Sato, R., 1967, Studies on soluble cytochromes in Enterobacteriaceae V. Nitrite-dependent gas evolution in cells containing cytochrome ç552, J. Biochem., 62: 230.PubMedGoogle Scholar
  21. Gray, C.T., Wimpenny, J.W.T., Hughes, D.E., and Ranlett, M., 1963, A soluble c-type cytochrome from anaerobically grown Escherichia coli and various Enterobacteriaceae, Biochim. Biophys. Acta., 67: 157.PubMedCrossRefGoogle Scholar
  22. Griffiths, L., and Cole, J.A., 1987, Lack of redox control of the anaerobically-induced nirB+ gene of Escherichia coli K-12. Arch. Microbiol., 147: 364.PubMedCrossRefGoogle Scholar
  23. Haddock, B.A., and Jones, C.W., 1977, Bacterial respiration, Bacteriol. Rev., 41: 47.PubMedGoogle Scholar
  24. Hasan, S.M., and Hall, J.B., 1975, The physiological function of nitrate reduction in Clostridium perfringens, J. Gen. Microbiol., 87: 120.PubMedCrossRefGoogle Scholar
  25. Ingledew, W.J., and Poole, R.K., 1984, The respiratory chains of Escherichia coli. Microbiol. Rev., 48: 222.PubMedGoogle Scholar
  26. Jackson, R.H., Cornish-Bowden, A., and Cole, J.A., 1981a, Prosthetic groups of the NADH-dependent nitrite reductase from Escherichia coli K12, Bioch. J., 193: 861.Google Scholar
  27. Jackson, R.H., Cole, J.A., and Cornish-Bowden, A., 1981b, The steady-state kinetics of the NADH-dependent nitrite reductase from Escherichia coli K12: nitrite and hydroxylamine reduction, Biochem. J., 199: 171.PubMedGoogle Scholar
  28. Jackson, R.H., Cole, J.A., and Cornish-Bowden, A., 1982, The steady state kinetics of the NADH-dependent nitrite reductase from Escherichia coli: the reduction of single-electron acceptors, Biochem. J., 203: 505.PubMedGoogle Scholar
  29. Jayaraman, P.S., Peakman, T.C., Busby, S.J.W., Quincey, R.V., and Cole, J.A., 1987, Location and sequence of the promoter of the gene for the NADH-dependent nitrite reductase of Escherichia coli and its regulation by oxygen, the FNR protein and nitrite, J. Mol. Biol., 196: 781.PubMedCrossRefGoogle Scholar
  30. Jayaraman, P.-S., Gaston, K.L., Cole, J.A., and Busby, S.J.W., 1988, The nirB promoter of Escherichia coli: location of nucleotide sequences essential for regulation by oxygen, the FNR protein and nitrite, Mol. Microbiol., 2: 527.PubMedCrossRefGoogle Scholar
  31. Jayaraman, P.-S., Cole, J.A., and Busby, S.J.W., 1989, Mutational analysis of the sequence at the FNR-dependent nirB promoter in Escherichia coli, Nucl. Acids Res., 17: 135.PubMedCrossRefGoogle Scholar
  32. Jeter, R.M., Sias, S.R., and Ingraham, J.L., 1984, Chromosomal location and function of genes affecting Pseudomonas aeruginosa nitrite assimilation, J. Bacterol., 157, 673.Google Scholar
  33. Jones, G.A., 1972, Dissimilatory metabolism of nitrate by the rumen microbiota, Can. J. Microbiol., 18: 1783.PubMedCrossRefGoogle Scholar
  34. Kajie, S., and Anraku, Y., 1986, Purification of a hexaheme cytochrome c552 from Escherichia coli K12 and its properties as a nitrite reductase, Eur. J. Biochem., 154: 457.PubMedCrossRefGoogle Scholar
  35. Kaspar, H.F., and Tiedje, J.M., 1982, Dissimilatory reduction of nitrate and nitrite in the bovine rumen: nitrous oxide production and effect of acetylene, Appl. Environ. Microbiol., 41: 705.Google Scholar
  36. Kemp, J.D., and Atkinson, D.E., 1966, Nitrite reductase of Escherichia coli specific for reduced nicotinamide adenine dinucleotide, J. Bacteriol., 92: 628.PubMedGoogle Scholar
  37. Kemp, J.D., Atkinson, D.E., Ehret, A., and Lazzarimi, R.A., 1963, Evidence for the identity of the nicotinamide adenine dinucleotide phosphate-specific sulphite and nitrite reductases of Escherichia coli, J. Biol. Chem., 238: 3466.PubMedGoogle Scholar
  38. Koike, I., and Hattori, A., 1978a, Denitrification and ammonia formation in anaerobic coastal sediments. Appl. Environ. Microbiol., 35: 278.PubMedGoogle Scholar
  39. Koike, I., and Hattori, A., 1978b, Simultaneous determination of nitrification andnitrate reduction in coastal sediments by a 15N dilution technique, Appl. Environ. Microbiol., 35: 853.PubMedGoogle Scholar
  40. Lambden, P.R., and Guest, J.R., 1976, Mutants of Escherichia coli K12 unable to use fumarate as an electron acceptor, J. Gen. Microbiol., 97: 145.PubMedCrossRefGoogle Scholar
  41. Lang, F. and Hochstein, L.I., 1989, Purification and properties of a nitrate reductase from Halobacterium denitrificans. Abstract K-122. Abstracts of the Annual Meeting of the American Society for Microbiology, p. 265.Google Scholar
  42. Lazzarini, R.A., and Atkinson, D.E., 1961, A TPN specific nitrite reductase from E. coli, J. Biol. Chem., 236: 3330.Google Scholar
  43. Lewis, D., 1951, The metabolism of nitrate and nitrite in sheep.2. Hydrogen donators in nitrate reduction by rumen microorganisms in vitro Biochem.J., 49: 149.PubMedGoogle Scholar
  44. Liu, M.-C., Baker, B.W., Liu, M.-Y., and Dao, T.N., 1988, Purification of Vibrio fischeri nitrite reductase and its characterisation as a hexaheme c-type cytochrome, Arch. Biochem. Biophys., 262: 259.PubMedCrossRefGoogle Scholar
  45. Liu, M.-C., and Peck, H.D., 1981, The isolation of a hexaheme cytochrome from Desulfovibrio desulfuricans and its identification as a new type of nitrite reductase, J. Biol. Chem., 256: 13159.PubMedGoogle Scholar
  46. Macdonald, H., and Cole, J.A., 1985, Molecular cloning and functional analysis of the cysG and nirB genes of Escherichia coli K12, two closely-linked genes required for NADH-dependent nitrite reductase activity, Mol. Gen.Genet. 200: 328.PubMedCrossRefGoogle Scholar
  47. Massey, V., and Veeger, C., 1961, Studies on the reaction mechanisms of lipoyl dehydrogenase, Biochim. Biophys. Acta., 48: 33.PubMedCrossRefGoogle Scholar
  48. Motteram, P.A.S., Mc Carthy, J.E.G., Ferguson, S.J., Jackson, J.B., and Cole, J.A., 1981, Energy conservation during the formate-dependent reduction of nitrite by Escherichia coli, FEMS Microbiol. Letts., 12: 317.CrossRefGoogle Scholar
  49. Newman, B.M., and Cole, J.A., 1978, The chromosomal location and pleiotropic effects of mutations in the nirA+ gene of Escherichia coli K12: the essential role of nirA+ in nitrite reduction and in other anaerobic redox reactions, J. Gen. Microbiol., 106: 1.PubMedCrossRefGoogle Scholar
  50. Pabo, C.O., and Sauer, R.T., 1984, Protein-DNA recognition, Ann. Rev. Biochem., 53: 293.PubMedCrossRefGoogle Scholar
  51. Peck, H.D., and Gest, H., 1957, Formic dehydrogenase and the hydrogenlyase enzyme complex in Coli-Aerogenes bacteria, J. Bacteriol., 73: 706.PubMedGoogle Scholar
  52. Pope, N.R., and Cole, J.A., 1982, Generation of a membrane potential by one of two independent pathways for nitrite reduction by Escherichia coli. J. Gen. Microbiol., 128: 319.Google Scholar
  53. Pope, N.R., and Cole, J.A., 1984, Pyruvate and ethanol as electron donors for nitrite reduction by Escherichia coli K12, J. Gen. Microbiol., 130: 1279.PubMedGoogle Scholar
  54. Postgate, J.R., 1954, Presence of cytochrome in an obligate anaerobe, Biochem. J., 56: 11Google Scholar
  55. Rönner, V., and Sorensen, F., 1985, Denitrification rates in the low-oxygen waters of the stratified Baltic proper, Appl. Environ. Microbiol., 50: 801.PubMedGoogle Scholar
  56. Samuelsson, M.-O., and Rönner, V., 1982, Ammonium production by dissimilatory nitrate reducers isolated from Baltic sea water, as indicated by 15N study, Appl. Environ. Microbiol., 44: 1241.PubMedGoogle Scholar
  57. Schroder, I., Robertson, A.M., Bokranz, M., Unden, G., Bocher, R., and Kroger, A., 1985, The membranous nitrite reductase involved in the electron transport of Wolinella succinogenes, Arch. Microbiol., 140: 380.CrossRefGoogle Scholar
  58. Seki, S., Hattori, Y., Hasegawa, T., Haraguchi, H., and Ishimoto, M., 1987, Studies on nitrate reductase of Clostridium perfringens. IV. Identification of metals, molybdenum cofactor and iron-sulfur cluster, J. Biochem., 101: 503.PubMedGoogle Scholar
  59. Seki-Chiba, S., and Ishimoto, M., 1977, Studies on nitrate reductase of Clostridium perfringens: I. Purification, some properties, and effect of tungstate on its formation, J. Biochem., 82: 1663.PubMedGoogle Scholar
  60. Smith, M., 1983, Nitrous oxide production by Escherichia coli is correlated with nitrate reductase activity, Appl. Environ. Microbiol., 45: 1545.PubMedGoogle Scholar
  61. Sorensen, J., 1978, Capacity for denitrification and reduction of nitrate to ammonia in a coastal marine sediment, Appl. Environ. Microbiol., 35: 301.PubMedGoogle Scholar
  62. Spiro, S., and Guest, J.R., 1987a, Activation of the lac operon of Escherichia coli by a mutant FNR protein, Mol. Microbiol., 1: 53.PubMedCrossRefGoogle Scholar
  63. Spiro,S., and Guest, J.R., 1987b, Regulation and over-production of the fnr gene of Escherichia coli, J. Gen. Microbiol., 133: 3279.Google Scholar
  64. Steenkemp, D.J., and Peck, H.D., 1980, The association of hydrogenase and dithionite reductase of Desulfovibrio desulfuricans, Biochem. Biophys. Res. Commun., 94: 41.CrossRefGoogle Scholar
  65. Steenkemp, D.J., and Peck, H.D., 1981, Proton translocation associated with nitrite respiration in Desulfovibrio desulfuricans, J. Biol. Chem., 256: 5450.Google Scholar
  66. Stewart, V., 1982, Requirement of Fnr and Narl functions for nitrate reductase expression in Escherichia Coli K12, J. Bacteriol., 151: 1320.PubMedGoogle Scholar
  67. Stewart, V., Parales, J., and Merkel, S.M., 1989, Structure of genes narL and narX of the nar (Nitrate Reductase) locus in Escherichia coli K-12, J. Bacteriol., 171: 2229.PubMedGoogle Scholar
  68. Van’t Riet, J., and Planta, R.J., 1975, Purification, structure and properties of the respiratory nitrate reductase of Klebsiella aerogenes, Biochim. Biophys. Acta., 379: 81.CrossRefGoogle Scholar
  69. Wimpenny, J.W.T., and Cole, J.A., 1967, The regulation of metabolism of facultative bacteria.III. The effect of nitrate. Biochim. Biophys. Acta., 148: 233.PubMedCrossRefGoogle Scholar
  70. Wimpenny, J.W.T., and Warmsley, A.M.H., 1968, The effect of nitrate on Krebs cycle enzymes in various bacteria, Biochim. Biophys. Acta, 156: 297.PubMedCrossRefGoogle Scholar
  71. Woods, D.D., 1938, The reduction of nitrate to ammonia by Clostridium welchii, Biochem. J., 32: 2000.Google Scholar
  72. Yamamoto, I., Shimizu, H., Tsuji,T., and Ishimoto, M., 1986, Purification and properties of nitrate reductase from Mitsuokella multiacidus, J. Biochem, 99: 961.Google Scholar
  73. Zarowny, D.P., and Sanwal, B.D., 1963, Characterization of an NADH-specific nitrite reductase from E. coli K12, Can. J. Microbiol., 9: 531.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1990

Authors and Affiliations

  • J. A. Cole
    • 1
  1. 1.Department of BiochemistryUniversity of BirminghamBirminghamUK

Personalised recommendations