Advertisement

Activity of Chemolithotrophic Nitrifying Bacteria under Stress in Natural Soils

  • H. J. Laanbroek
  • J. W. Woldendorp
Part of the Advances in Microbial Ecology book series (AMIE, volume 14)

Abstract

Nitrification is an important process in the biogeochemical cycle of nitrogen, linking its reduced and oxidized parts. Since the conversion of ammonium to nitrate has a great impact on the environment, such as weathering of soils, production of greenhouse gases, and eutrophication of surface and ground waters (Van Breemen and Van Dijk, 1988), it is important to know the characteristics of the responsible organisms. Although many organotrophic microorganisms are able to produce oxidized nitrogenous compounds such as nitrite and nitrate (Focht and Verstraete, 1977; Killham, 1987; Kuenen and Robertson, 1987), chemolithotrophic nitrifying bacteria are considered to be the most important group producing these compounds from ammonia. A contribution to nitrate production by organotrophic microorganisms has only been observed in some acid coniferous forest soils (Schimel et al., 1984; Killham, 1986, 1990). According to Bergey’s Manual of Systematic Bacteriology (Watson et al., 1989), the family of nitrifying bacteria is a diverse group of rods, vibrios, cocci, and spirilla, all having the ability to utilize ammonia or nitrite as a major source of energy and carbon dioxide as the chief source of carbon. With the exception of Nitrobacter species, all others are obligate chemolithotrophs, but some can grow mixotrophically on a mixture of CO2 and small organic compounds. All strains are aerobic, but some may proliferate at low oxygen concentrations. Some Nitrobacter species might even grow at the expense of nitrate reduction in the absence of oxygen.

Keywords

Ammonia Oxidation Much Probable Number Grassland Soil Nitrify Bacterium Radial Oxygen Loss 
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. Abeliovich, A., 1987, Nitrifying bacteria in wastewater reservoirs, Appl. Environ. Microbiol. 53:754–760.PubMedGoogle Scholar
  2. Abeliovich, A., and Vonshak, A., 1992, Anaerobic growth of Nitrosomonas europaea, Arch. Microbiol. 158:267–270.Google Scholar
  3. Ahlers, B., König, W., and Bock, E., 1990, Nitrite reductase activity in Nitrobacter vulgaris, FEMS Microbiol. Lett. 67:121–126.Google Scholar
  4. Allison, S. M., and Prosser, J.I., 1991, Urease activity in neutrophilic autotrophic ammonia-oxidizing bacteria isolated from acid soils, Soil Biol. Biochem. 23:45–51.Google Scholar
  5. Allison, S. M., and Prosser, J. I., 1993, Ammonia oxidation at low pH by attached populations of nitrifying bacteria, Soil Biol. Biochem. 25:935–941.Google Scholar
  6. Anderson, I. C., and Joel, J. S., 1986, Relative rates of nitric oxide and nitrous oxide production by nitrifiers, denitrifiers and nitrate respirers, Appl. Environ. Microbiol. 51:938–945.PubMedGoogle Scholar
  7. Anderson, I. C., Poth, M., Homstead, J., and Burdige, D., 1993, A comparison of NO and N2O production by the autotrophic nitrifier Nitrosomonas europaea and the heterotrophic nitrifier Alcaligenes faecalis, Appl. Environ. Microbiol. 59:3525–3533.PubMedGoogle Scholar
  8. Armstrong, W., 1964, Oxygen diffusion from the roots of some British bog plants, Nature 204:511–519.Google Scholar
  9. Baumgärtner, M., Sameluck, F., Bock, E., and Conrad, R., 1991, Production of nitric oxide by amonium-oxidizing bacteria colonizing building stones, FEMS Microbiol. Ecol. 85:95–100.Google Scholar
  10. Berg, P., 1986, Nitrifier Populations and Nitrification Rates in Agricultural Soil, Swedish University of Agricultural Sciences, Uppsala, thesis.Google Scholar
  11. Berg, P., and Rosswall, T., 1986, Seasonal variation in abundance and activity of nitrifiers in four arable cropping systems, Microb. Ecol. 13:75–87.Google Scholar
  12. Blacquière, T., 1986, Nitrate reduction in the leaves and numbers of nitrifiers in the rhizosphere of Plantago lanceolata growing in two contrasting sites, Plant Soil 91:377–380.Google Scholar
  13. Bock, E., and Heinrich, G., 1969, Morphologische und physiologische Untersuchungen an Zellen von Nitrobacter winogradskyi Buch, Arch. Microbiol. 69:149–159.Google Scholar
  14. Bock, E., and Koops, H.-P., 1992, The genus Nitrobacter and related genera, in: The Prokaryotes. A Handbook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Applications, 2nd ed., Vol. III (A. Balows, H. G. Trüper, M. Dworkin, W. Harder, and K.-H. Schleifer, eds.), Springer-Verlag, New York, pp. 2302–2309.Google Scholar
  15. Bock, E., Wolderer, P. A., and Freitag, A., 1988, Growth of Nitrobacter in the absence of dissolved oxygen, Water Res. 22:245–250.Google Scholar
  16. Bock, E., Koops, H.-P., Ahlers, B., and Harms, H., 1992, Oxidation of inorganic nitrogen compounds as energy source, in: The Prokaryotes. A Handbook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Applications, 2nd ed., Vol. I (A. Balows, H. G. Trüper, M. Dworkin, W. Harder, and K.-H. Schleifer, eds.), Springer-Verlag, New York, pp. 414–430.Google Scholar
  17. Bohlool, B. B., and Schmidt, E. L., 1973, A fluorescent antibody approach to determination of growth rates in soil, Bull. Ecol. Res. Comm. 17:336–338.Google Scholar
  18. Bohlool, B. B., and Schmidt, E. L., 1980, The immunofluorescence approach in microbial ecology, Adv. Microb. Ecol. 4:203–241.Google Scholar
  19. Bohlool, B. B., Schmidt, E. L., and Beasly, C., 1977, Nitrification in the intertidal zone: Influence of effluent type and effect of tannin on nitrifiers, Appl. Environ. Microbiol. 34:523–528.PubMedGoogle Scholar
  20. Both, G. J., 1990, The Ecology of Nitrite-Oxidizing Bacteria in Grassland Soils, State University of Groningen, the Netherlands, PhD thesis.Google Scholar
  21. Both, G. J., and Laanbroek, H. J., 1991, The effect of the incubation period on the result of MPN enumerations of nitrite-oxidizing bacteria: Theoretical considerations, FEMS Microbiol. Ecol. 85:355–344.Google Scholar
  22. Both, G. J., Gerards, S., and Laanbroek, H. J., 1990, Enumeration of nitrite-oxidizing bacteria in grassland soils using a most probable number technique: Effect of nitrite concentration and sampling procedure, FEMS Microbiol. Ecol. 74:277–286.Google Scholar
  23. Both, G. J., Gerards, S., and Laanbroek, H. J., 1992a, The occurrence of chemolitho-autotrophic nitrifiers in water-saturated grassland soils, Microb. Ecol. 23:15–26.Google Scholar
  24. Both, G. J., Gerards, S., and Laanbroek, H. J., 1992b, Temporal and spatial variation in the nitrite-oxidizing bacterial community of a grassland soil, FEMS Microbiol. Ecol. 101:99–112.Google Scholar
  25. Both, G. J., Gerards, S., and Laanbroek, H.J., 1992c, Kinetics of nitrite oxidation in two Nitrobacter species grown in nitrite-limited chemostats, Arch. Microbiol. 157:436–441.Google Scholar
  26. Bramley, R. G. V., and White, R. E., 1989, The effect of pH, liming, moisture and temperature on the activity of nitrifiers in a soil under pasture, Aust. J. Soil Res. 27:711–724.Google Scholar
  27. Button, D. K., 1985, Kinetics of nutrient-limited transport and microbial growth, Microbiol. Rev. 49:270–297.PubMedGoogle Scholar
  28. Castignetti, D., and Gunner, H. B., 1982, Differential tolerance of hydroxylamine by an Alcaligenes sp., a heterotrophic nitrifier, and by Nitrobacter agilis, Can. J. Microbiol. 28:148–150.Google Scholar
  29. Christensen, P. B., and Sørensen, J., 1986, Temporal variation of denitrification activity in plant-covered, littoral sediment from Lake Hampen, Denmark, Appl. Environ. Microbiol. 51:1171–1179.Google Scholar
  30. Cooper, A. B., 1983, Population ecology of nitrifiers in a stream receiving geothermal inputs of ammonium, Appl. Environ. Microbiol. 45:1170–1177.PubMedGoogle Scholar
  31. De Boer, W., and Laanbroek, H. J., 1989, Ureolytic nitrification at low pH by Nitrosospira species, Arch. Microbiol. 152:178–181.Google Scholar
  32. De Boer, W., Duyts, H., and Laanbroek, H. J., 1988, Autotrophic nitrification in a fertilized acid heath soil, Soil Biol. Bioichem. 20:845–850.Google Scholar
  33. De Boer, W., Duyts, H., and Laanbroek, H. J., 1989a, Urea stimulated autotrophic nitrification in suspensions of fertilized, acid heath soil, Soil Biol. Biochem. 21:349–354.Google Scholar
  34. De Boer, W., Klein Gunnewiek, P. J. A., Troelstra, S. R., and Laanbroek, H. J., 1989b, Two types of chemolithotrophic nitrification in acid heathland humus, Plant Soil 119:229–235.Google Scholar
  35. De Boer, W., Klein Gunnewiek, P. J. A., and Troelstra, S. R., 1990, Nitrification in Dutch heathland soils. II. Characteristics of nitrate production, Plant Soil 127:193–200.Google Scholar
  36. De Boer, W., Klein Gunnewiek, P. J. A., Veenhuis, M., Bock, E., and Laanbroek, H. J., 1991, Nitrification at low pH by aggregated chemolithotrophic bacteria, Appl. Environ. Microbiol. 57:3600–3604.PubMedGoogle Scholar
  37. De Boer, W., Tietema, A., Klein Gunnewiek, P. J. A., and Laanbroek, H. J., 1992, The chemolithotrophic ammonium-oxidizing community in a nitrogen-saturated acid forest soil in relation to pH-dependent nitrifying activity, Soil Biol. Biochem. 24:229–234.Google Scholar
  38. De Boer, W., Hunscheid, M. P. J., Schotman, J. M. T., Troelstra, S. R., and Laanbroek, H. J., 1993, In situ net N transformations in pine, fir and oak stands of different ages on acid sandy soil, 3 years after liming, Biol. Fertil. Soils 15:120–126.Google Scholar
  39. De Boer, W., Klein Gunnewiek, P. J. A., and Laanbroek, H. J., 1995, Nitrification at low pH by a bacterium belonging to the genus Nitrosospira, Soil Biol. Biochem. 27:127–132.Google Scholar
  40. Diab, S., Kochba, M., and Avnimelech, Y., 1993, Nitrification pattern in a fluctuating anaerobic-aerobic pond environment, Water Res. 27:1469–1475.Google Scholar
  41. Eigener, U., 1975, Adenine nucleotide pool variations in intact Nitrobacter winogradskyi cells, Arch. Microbiol. 102:233–240.PubMedGoogle Scholar
  42. Eigener, U., and Bock, E., 1975, Study on the regulation of oxidation and CO2 assimilation in intact Nitrobacter winogradskyi cells, Arch. Microbiol. 102:241–246.PubMedGoogle Scholar
  43. Engelaar, W. M. H. G., Bodelier, P. L. E., Laanbroek, H. J., and Blom, C. W. P. M., 1991, Nitrification in the rhizosphere of a flooding-resistant and a flooding-non-resistant Rumex species under drained and waterlogged conditions, FEMS Microbiol. Ecol. 86:33–42.Google Scholar
  44. Engelaar, W. M. H. G., Symens, J. C., Laanbroek, H. J., and Blom, C. W. P. M., Preservation of nitrifying capacity and nitrate availability in waterlogged soils by radial oxygen loss from roots of wetland plants, Biol. Fertil. Soils, in press.Google Scholar
  45. Focht, D. D., and Verstraete, W., 1977, Biochemical ecology of nitrification and denitrification, Adv. Microb. Ecol. 1:135–214.Google Scholar
  46. Freitag, A., and Bock, E., 1990, Energy conservation in Nitrobacter, FEMS Microbiol. Lett. 66:157–162.Google Scholar
  47. Freitag, A., Rudert, M., and Bock, E., 1987, Growth of Nitrobacter by dissimilatory nitrate reduction, FEMS Microbiol. Lett. 48:105–109.Google Scholar
  48. Frijlink, M. J., Abee, T., Laanbroek, H. J., de Boer, W., and Konings, W. N., 1992a, The bio-energetics of ammonia and hydroxylamine oxidation in Nitrosomonas europaea at acid and alkaline pH, Arch. Microbiol. 157:194–199.Google Scholar
  49. Frijlink, M. J., Abee, T., Laanbroek, H. J., de Boer, W., and Konings, W. N., 1992b, Secondary transport of amino acids in Nitrosomonas europaea, Arch. Microbiol. 157:389–393.Google Scholar
  50. Gay, G., Josserand, A., and Bardin, R., 1983, Growth of two serotypes of Nitrobacter in mixotrophic and chemoorganotrophic conditions, Can. J. Microbiol. 29:394–397.Google Scholar
  51. Goreau, T. J., Kaplan, W. A., Wofsy, S. C., McElroy, M. B., Valois, F. W., and Watson, S. W., 1980, Production of NO2 and N2O by nitrifying bacteria at reduced concentrations of oxygen, Appl. Environ. Microbiol. 40:526–532.PubMedGoogle Scholar
  52. Griffiths, B. S., 1989, Enhanced nitrification in the presence of bacteriophagous protozoa, Soil Biol. Biochem. 21:1045–1051.Google Scholar
  53. Hankinson, T. R., and Schmidt, E. L., 1984, Examination of an acid forest soil for ammonia-and nitrite-oxidizing bacteria, Can. J. Microbiol. 30:1125–1132.Google Scholar
  54. Hankinson, T. R., and Schmidt, E. L., 1988, An acidophilic and a neutrophilic Nitrobacter strain isolated from the numerical predominant nitrite-oxidizing population of an acid forest soil, Appl. Environ. Microbiol. 54:1536–1540.PubMedGoogle Scholar
  55. Head, I. M., Hiorns, W. D., Embley, T. M., McCarthy, A. J., and Saunders, J. R., 1993, The phytogeny of autotrophic ammonia-oxidizing bacteria as determined by analysis of 16S ribosomal RNA gene sequences, J. Gen. Microbiol. 139:1147–1153.PubMedGoogle Scholar
  56. Hooper, A. B., and Terry, K. R., 1979, Hydroxylamine oxidoreductase of Nitrosomonas europaea production of nitric oxide from hydroxylamine, Biochim. Biophys. Acta 571:12–20.PubMedGoogle Scholar
  57. Jansson, S. L., 1958, Tracer studies on nitrogen transformations in soil with special attention to mineralization-immobilization relationships, Kungl. Lantbr. Ann. 24:101–361.Google Scholar
  58. Josserand, A., Gay, G., and Faurie, G., 1981, Ecological study of two Nitrobacter serotypes coexisting in the same soil, Microb. Ecol. 7:275–280.Google Scholar
  59. Killham, K., 1986, Heterotrophic nitrification, in: Nitrification (J. I. Prosser, ed.), IRL Press, Oxford, England, pp. 117–126.Google Scholar
  60. Killham, K., 1987, A new perfusion system for measurement and characterization of potential rates of soil nitrification, Plant Soil 97:267–272.Google Scholar
  61. Killham, K., 1990, Nitrification in coniferous forest soils, Plant Soil 128:31–44.Google Scholar
  62. Kleiner, D., 1985, Bacterial ammonium transport, FEMS Microbiol. Rev. 32:87–100.Google Scholar
  63. Koops, H.-P., and Möller, U. C., 1992, The lithotrophic ammonia-oxidizing bacteria, in: The Prokaryotes. A Handbook on the Biology of Bacteria: Ecophysiology, Isolation, Identification, Applications, 2nd ed., Vol. III (A. Balows, H. G. Trüper, M. Dworkin, W. Harder, and K.-H. Schleifer, eds.), Springer-Verlag, New York, pp. 2625–2637.Google Scholar
  64. Kuenen, J. G., and Robertson, L. A., 1987, Ecology of nitrification and denitrification, in: The Nitrogen and Sulphur Cycles (J. A. Cole and S. Ferguson, eds.), Cambridge University Press, Cambridge, England, pp. 162–218.Google Scholar
  65. Laan, P., Smolders, A., Blom, C. W. P. M., and Armstrong, W., 1989a, The relative roles of internal aeration, radial oxygen losses, iron exclusion and nutrient balances in flood-tolerance of Rumex species, Acta Bot. Neerl. 38:131–145.Google Scholar
  66. Laan, P., Beerevoets, M. J., Lythe, S., Armstrong, W., and Blom, C. W. P. M., 1989b, Root morphology and aerenchyma formation as indicators of flood-tolerance of Rumex species, J. Ecol. 77:693–703.Google Scholar
  67. Laanbroek, H. J., and Gerards, S., 1991, Effects of organic manure on nitrification in arable soils, Biol. Fert. Soils 12:147–153.Google Scholar
  68. Laanbroek, H. J., and Gerards, S., 1993, Competition for limiting amounts of oxygen between Nitrosomonas europaea and Nitrobacter winogradskyi grown in mixed continuous cultures, Arch. Microbiol. 159:453–459.Google Scholar
  69. Laanbroek, H. J., and Schotman, J. M. T, 1991, Effect of nitrite concentration and pH on most probable number enumerations of non-growing Nitrobacter species, FEMS Microbiol. Ecol. 85:269–278.Google Scholar
  70. Laanbroek, H. J., Bodelier, P. L. E., and Gerards, S., 1994, Oxygen consumption kinetics of Nitrosomonas europaea and Nitrobacter hamburgensis grown in mixed continuous cultures at different oxygen concentrations, Arch. Microbiol. 161:156–162.Google Scholar
  71. Lang, K., Lehtonen, M., and Martikainen, P. J., 1993, Nitrification potentials at different pH values in peat samples from various layers of a drained mire, Geomicrobiol. J. 11:141–147.Google Scholar
  72. Langelaan, J. G., and Troelstra, S. R., 1992, Growth, chemical composition and nitrate reductase activity of Rumex species in relation to form and level of N supply, Plant Soil 145:215–229.Google Scholar
  73. Macdonald, R. M., 1986, Nitrification in soil: An introductory history, in: Nitrification (J. I. Prosser, ed.), IRL Press, Oxford, England, pp. 1–16.Google Scholar
  74. Martikainen, P. J., and de Boer, W., 1993, Nitrous oxide production and nitrification in acidic soil from a Dutch coniferous forest, Soil Biol. Biochem. 25:343–347.Google Scholar
  75. Martikainen, P. J., and Nurmiaho-Lassila, E. L., 1985, Nitrosospira, an important ammonium-oxidizing bacterium in fertilized coniferous forest soil, Can. J. Microbiol. 31:190–197.Google Scholar
  76. Martikainen, P. J., Lehtonen, M., Lang, K., De Boer, W., Ferm, A., 1993, Nitrification and nitrous oxide production potentials in aerbic soil samples from the soil profile of a finnish coniferous site receiving high ammonium deposition, FEMS Microbiol. Ecol. 13:113–121.Google Scholar
  77. McCaig, A. E., Embley, T. M., and Prosser, J. I., 1994, Molecular analysis of enrichment cultures of marine ammonia oxidizers, FEMS Microbiol. Ecol. 120:363–368.Google Scholar
  78. Meiklejohn, J., 1968, Numbers of nitrifying bacteria in some Rhodesian soils under natural grass and improved pastures, J. Appl. Ecol. 5:291–300.Google Scholar
  79. Meincke, M., Krieg, E., and Bock, E., 1989, Nitrosovibrio spp., the dominant ammonia-oxidizing bacteria in building sandstone, Appl. Environ. Microbiol. 55:2108–2110.PubMedGoogle Scholar
  80. Moore, D. R. E., and Waid, J. S., 1971, The influence of washings of living plant roots on nitrification, Soil Biol. Biochem. 3:69–83.Google Scholar
  81. Munro, P. E., 1966, Inhibition of nitrifiers by grass root extracts, J. Appl. Ecol. 3:231–238.Google Scholar
  82. Olff, H., 1992, On the Mechanisms of Vegetation Succession, State University of Groningen, The Netherlands, Ph.D. thesis.Google Scholar
  83. Ponnamperuma, F. N., 1984, Effects of flooding on soils, in: Flooding and Plant Growth (T. T. Kozlowaki, ed.), Academic Press, New York, pp. 10–45.Google Scholar
  84. Poth, M., 1986, Dinitrogen production from nitrite by a Nitrosomonas isolate, Appl. Environ. Microbiol. 52:957–959.PubMedGoogle Scholar
  85. Poth, M., and Focht, D. D., 1985, 15N kinetic analysis of N2O production by Nitrosomonas europaea: An examination of nitrifier denitrification, Appl. Environ. Microbiol. 49:1134–1141.PubMedGoogle Scholar
  86. Prosser, J. I., 1989, Autotrophic nitrification in bacteria, Adv. Microb. Physiol. 30:125–181.PubMedGoogle Scholar
  87. Purchase, B. S., 1974, Evaluation of the claim that grass root exudates inhibit nitrification, Plant Soil 41:527–539.Google Scholar
  88. Rice, E. L., and Pancholy, S. K., 1972, Inhibition of nitrification by climax ecosystems, Am. J. Bot. 59:1033–1040.Google Scholar
  89. Rice, E. L., and Pancholy, S. K., 1973, Inhibition of nitrification by climax ecosystems. II. Additional evidence and possible role of tannins, Am. J. Bot. 60:691–702.Google Scholar
  90. Riha, S. J., Campbell, G. S., and Wolfe, J., 1986, A model of competition for ammonium among heterotrophs, nitrifiers and roots, Soil Sci. Soc. Am. J. 50:1463–1466.Google Scholar
  91. Robinson, J. B., 1963, Nitrification in a New Zealand grassland soil, Plant Soil 19:173–182.Google Scholar
  92. Rosswall, T., 1982, Microbiological regulation of the biogeochemical nitrogen cycle, Plant Soil 67:15–34.Google Scholar
  93. Sand-Jensen, K., Prahl, S., and Stockholm, H., 1982, Oxygen release from submerged aquatic macrophytes, Oikos 38:349–354.Google Scholar
  94. Sarathchandra, S. U., 1978, Nitrification activities of some New Zealand soils and the effect of some clay types on nitrification, N. Z. J. Agr. Res. 21:615–621.Google Scholar
  95. Schimel, J. P., Firestone, M. K., and Killham, K. S., 1984, Identification of heterotrophic nitrification in a Sierran forest soil, Appl. Environ. Microbiol. 48:802–806.PubMedGoogle Scholar
  96. Schmidt, E. L., 1973, Fluorescent antibody technique for the study of microbial ecology, Bull. Ecol. Res. Comm. 17:67–76.Google Scholar
  97. Schmidt, E. L., and Belser, L. W., 1982, Nitrifying bacteria, in: Methods of Soil Analysis, 2nd ed. (R. H. Miller and D. R. Keeney, eds.), American Society of Agronomy, Madison, Wis., pp. 1027–1042.Google Scholar
  98. Smit, A. J., and Woldendorp, J. W., 1981, Nitrate production in the rhizosphere of Plantago species, Plant Soil 61:43–52.Google Scholar
  99. Smith, A. J., and Hoare, D. S., 1968, Acetate assimilation by Nitrobacter agilis in relation to its “obligate autotrophy,” J. Bacteriol. 95:844–855.PubMedGoogle Scholar
  100. Spieck, E., Meincke, M., and Bock, E., 1992, Taxonomic diversity of Nitrosovibrio strains isolated from building sandstones, FEMS Microbiol. Ecol. 102:21–26.Google Scholar
  101. Stams, A. J. M., Flameling, E. M., and Marnette, E. C. L., 1990, The importance of autotrophic versus heterotrophic oxidation of atmospheric ammonium in forest ecosystems with acid soils, FEMS Microbiol. Ecol. 74:337–344.Google Scholar
  102. Stienstra, A. W., Both, G. J., Gerards, S., and Laanbroek, H. J., 1993, Numbers of nitrite-oxidizing bacteria in the root zone of grassland plants, FEMS Microbiol. Ecol. 12:207–214.Google Scholar
  103. Stienstra, A. W., Klein Gunnewiek, P. J. A., and Laanbroek, H. J., 1994, Repression of nitrification in soils under a climax grassland vegetation, FEMS Microbiol. Ecol. 12:207–214.Google Scholar
  104. Stüven, R., Vollmer, M., and Bock, E., 1992, The impact of organic matter on nitric oxide formation by Nitrosomonas europaea, Arch. Microbiol. 158:439–443.Google Scholar
  105. Suzuki, I., Dular, U., and Kwok, S. C., 1974, Ammonia or ammonium ion as substrate for oxidation by Nitrosomonas europaea cells and extracts, J. Bacteriol. 120:556–558.PubMedGoogle Scholar
  106. Terry, K. R., and Hooper, A. B., 1970, Polyphosphate and orthophosphate content of Nitrosomonas europaea as a function of growth, J. Bacteriol. 103:199–206.PubMedGoogle Scholar
  107. Theron, J. J., 1951, The influence of plants on the mineralization of nitrogen and the maintenance of organic matter in the soil, J. Agr. Sci. 41:289–296.Google Scholar
  108. Tietema, A., de Boer, W., Riemer, L., and Verstraten, J. M., 1992, Nitrate production in nitrogen-saturated acid forest soils: Vertical distribution and characteristics, Soil Biol. Biochem. 24:235–240.Google Scholar
  109. Troelstra, S. R., Wagenaar, R., and de Boer, W., 1990, Nitrification in Dutch heathland soils. I. General soil characteristics and nitrification in undisturbed soil cores, Plant Soil 127:179–192.Google Scholar
  110. Troelstra, S. R., Wagenaar, R., and Smant, W., 1992, Growth of actinorhizal plants as influenced by the form of N with special reference to Myrica gale and Alnus incarta, J. Exp. Botany 43:1349–1359.Google Scholar
  111. Uhel, C., Roumet, C., and Salsac, L., 1989, Inducible nitrate reductase of rice plants as a possible indicator for nitrification in water-logged paddy soils, Plant Soil 116:197–206.Google Scholar
  112. Van Breemen, N., and Van Dijk, H. F. G., 1988, Ecosystems effects of atmospheric deposition of nitrogen in the Netherlands, Environ. Poll. 54:249–274.Google Scholar
  113. Van Cleemput, O., and Baert, L., 1984, Nitrite: A key compound in N loss processes under acid conditions? Plant Soil 76:233–241.Google Scholar
  114. Van Gool, A. P., Tobback, P. P., and Fischer, I., 1971, Autotrophic growth and synthesis of reserve polymers in Nitrobacter winogradskyi, Arch. Microbiol. 76:252–264.Google Scholar
  115. Verhagen, F. J. M., and Laanbroek, H. J., 1991, Competition for ammonium between nitrifying and heterotrophic bacteria in dual energy-limited chemostats, Appl. Environ. Microbiol. 57:3255–3263.PubMedGoogle Scholar
  116. Verhagen, F. J. M., and Laanbroek, H. J., 1992, Effects of grazing by flagellates on competition for ammonium between nitrifying and heterotrophic bacteria in chemostats, Appl. Environ. Microbiol. 58:1962–1969.PubMedGoogle Scholar
  117. Verhagen, F. J. M., Duyts, H., and Laanbroek, H. J., 1992, Competition for ammonium between nitrifying and heterotrophic bacteria in continuously percolated soil columns, Appl. Environ. Microbiol. 58:3303–3311.PubMedGoogle Scholar
  118. Verhagen, F. J. M., Duyts, H., and Laanbroek, H. J., 1993, Effects of grazing by flagellates on competition for ammonium between nitrifying and heterotrophic bacteria in soil columns, Appl. Environ. Microbiol. 59:2099–2106.PubMedGoogle Scholar
  119. Verhagen, F. J. M., Hageman, P. E. J., Woldendorp, J. W., and Laanbroek, H. J., 1994a, Competition for ammonium between nitrifying bacteria and plant roots in soil in pots; effects of grazing by flagellates and fertilization, Soil Biol. Biochem. 26:89–96.Google Scholar
  120. Verhagen, F. J. M., Zölffel, M., Bruggerolle, G., and Patterson, D. J., 1994b, Adriamonas peritocrescens gen. no., sp. nov., a new free-living soil flagellate (Protista incertae sedis), Eur. J. Protozool. 30:295–308.Google Scholar
  121. Walker, N., and Wickramasinghe, K. N., 1979, Nitrification and autotrophic nitrifying bacteria in acid tea soils, Soil Biol. Biochem. 11:231–236.Google Scholar
  122. Ward, B. B., 1986, Nitrification in marine environments, in: Nitrification (J. I. Prosser, ed.), IRL Press, Oxford, England, pp. 157–184.Google Scholar
  123. Watson, S. W., Bock, E., Harms, H., Koops, H.-P., and Hooper, A. B., 1989, Nitrifying bacteria, in: Bergey’s Manual of Systematic Bacteriology, Vol. 3 (J. T. Staley, M. P. Bryant, N. Pfennig, and J. G. Holt, eds.), Williams & Wilkins, Baltimore, pp. 1808–1834.Google Scholar
  124. Woese, C. R., Weisburg, W. G., Hahn, C. M., Paster, B. J., Zahlen, L. B., Lewis, B. J., Macke, T. J., Ludwig, W., and Stackebrand, E., 1985, The phylogeny of purple bacteria: The gamma subdivision, Syst. Appl. Microbiol. 6:25–33.Google Scholar
  125. Woese, C. R., Weisburg, W. G., Paster, B. J., Hahn, C. M., Tanner, R. S., Krieg, N. R., Koops, H.-P., Harms, H., and Stackebrand, E., 1986, The phylogeny of purple bacteria: The beta subdivision, Syst. Appl. Microbiol. 5:327–336.Google Scholar
  126. Woldendorp, J. W., and Laanbroek, H. J., 1989, Activity of nitrifiers in relation to nitrogen nutrition of plants in natural ecosystems, Plant Soil 115:217–228.Google Scholar
  127. Wood, P. M., 1987, Monooxygenase and free radical mechanism for biological ammonia oxidation, in: The Nitrogen and Sulphur Cycles (J. A. Cole and S. Ferguson, eds.), Cambridge University Press, Cambridge, England, pp. 219–243.Google Scholar
  128. Zak, D. R., Groffman, P. M., Pregitzer, K. S., Christensen, S., and Tiedje, J. M., 1990, The vernal dam: Plant-microbe competition for nitrogen in northern hardwood forests, Ecology 71:651–656.Google Scholar

Copyright information

© Plenum Press, New York 1995

Authors and Affiliations

  • H. J. Laanbroek
    • 1
  • J. W. Woldendorp
    • 2
  1. 1.Centre for LimnologyNetherlands Institute of EcologyNieuwersluisThe Netherlands
  2. 2.Department of Soil Biology, Centre for Terrestrial EcologyNetherlands Institute of EcologyHeterenThe Netherlands

Personalised recommendations