Skip to main content
SpringerLink
Log in

Transformations of ammonia and the environmental impact of nitrifying bacteria

  • Published:
Biodegradation Aims and scope Submit manuscript

Abstract

In the sequence of events leading from ammonia to N2 during the process of biotransformation of inorganic nitrogen compounds, the weakest link, with respect to our knowledge and understanding of the organisms involved, is nitrification. In particular, this is true for the oxidation of ammonia to nitrite. The enzymes have not been thoroughly studied, and the enzymatic mechanisms have not been identified. Almost any biochemical and physiological aspect studied proved to be controversial, and major ecological questions still remain unanswered. Unless the structure and function of the various components of the process are worked out, progress in developing means for controlling nitrification will depend mainly on laborious trial and error and not on knowledgeable manipulation of this group of bacteria.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

AMO:

ammonia monooxygenase

HAO:

hydroxylamine oxidoreductase

MPN:

most probable number

TCE:

trichloroethylene

References

  • Abeliovich A & Azov Y (1976) Toxicity of ammonia to algae in sewage oxidation ponds. Appl. Environ. Microbiol. 31: 801–806

    Google Scholar 

  • Abeliovich A (1983) The effects of unbalanced ammonium and BOD concentrations on oxidation ponds. Wat. Res. 17: 299–301

    Google Scholar 

  • Abeliovich A (1985) Nitrification of ammonia in wastewater. Field observations and laboratory studies. Wat. Res. 19: 1097–1099

    Google Scholar 

  • Abeliovich A (1987) Nitrifying bacteria in wastewater reservoirs. Appl. Environ. Microbiol. 53: 754–760

    Google Scholar 

  • Abeliovich A & Vonshak A (1992) Anaerobic metabolism of Nitrosomonas europaea. Arch. Microbiol. 158: 267–270

    Google Scholar 

  • Aleem MIH, Hoch GE & Varner JE (1965) Water as the source of oxidant and reductant in bacterial chemosynthesis. Proc. Natl. Acad. Sci. USA 54: 869–873

    Google Scholar 

  • Andersson KK & Hooper AB (1983) O2 and H2O are each the source of one O in NO2 - produced from NH3 by Nitrosomonas: 15N N-NMR evidence. FEBS 164: 236–239

    Google Scholar 

  • Avron M & Shavit N (1965) Inhibitors and uncouplers of photophosphorylation. Biochim. Biophys. Acta 376: 97–104

    Google Scholar 

  • Bedard C & Knowles R (1989) Physiology, biochemistry and specific inhibitors of CH4, NH4 +, and CO oxidation by methanotrophs and nitrifiers. Microbiol. Rev. 53: 68–84

    Google Scholar 

  • Bennet E B (1986) The nitrifying of Lake Superior. Ambio. 15: 272–275

    Google Scholar 

  • Berg P & Rosswall T (1985) Ammonium oxidizer numbers, potential and actual oxidation rates in two Swedish arable soils. Biol. Fert. Soils 1: 31–140

    Google Scholar 

  • Blouin M, Bisaillon JG, Beaudet R & Ishaque M (1989) Nitrification of swine waste. Can. J. Microbiol. 36: 273–278

    Google Scholar 

  • Bock E, Koops HP & Harms H (1989) Nitrifying bacteria. In: Schlegel HG & Bowien B (Eds) Autotrophic Bacteria (pp 81–96). Science Tech. Publishers, Madison, WI, and Springer Verlag, Berlin.

    Google Scholar 

  • DeBoer W & Laanbroek HJ (1989) Ureolytic nitrification at low pH by Nitrospira sp. Arch. Microbiol. 152: 178–181

    Google Scholar 

  • DeBoer W, Duyts H & Laanbroek HJ (1988) Autotrophic nitrification in a fertilized acid heath soil. Soil Biol. Biochem. 20: 845–850

    Google Scholar 

  • DeGraff F (1964) Maintenance problems in large public aquaria. Arch. Neerl. Zool. 16: 142–143

    Google Scholar 

  • Downs MT (1988) Aquatic nitrogen transformations at low oxygen concentrations. Appl. Environ. Microbiol. 54: 172–175

    Google Scholar 

  • Drozd JW (1976) Energy coupling and respiration in Nitrosomonas europaea. Arch. Microbiol. 110: 257–262

    Google Scholar 

  • EEC Directive of 15.7.80 relating to the quality of water intended for human consumption, 80-778-EEC. (1980) Office J. Eur. Commun. 23, L229: 11–29

    Google Scholar 

  • Green LC, Tannenbaum SR & Goldman P (1981) Nitrate synthesis in the germfree and conventional rat. Science 212: 56–58

    Google Scholar 

  • Gresshoff PM, Roth LE, Stacey G, & Newton WE (1990) Nitrogen Fixation: Achievements and Objectives. Chapman and Hall, New York and London

    Google Scholar 

  • Hankinson TR & Schmidt TL (1988) An acidophilic and neutrophilic Nitrobacter strain isolated from the numerically predominant nitrite oxidizing population of an acid forest soil. Appl. Environ. Microbiol. 54: 1536–1540

    Google Scholar 

  • Hashimoto T & Hattori T (1987) Length of incubation for the estimation of the most probable number of nitrifying bacteria in soil. Soil Sci. Plant Nutr. 33: 507–509

    Google Scholar 

  • Hollocher TC, Tate ME & Nicholas DJD (1981) Oxidation of ammonia by Nitrosomonas europaea. Definitive 18O tracer evidence that hydroxylamine formation involves a monooxygenase. J. Biol. Chem. 256: 10834–10836

    Google Scholar 

  • Hooper AB (1968) A nitrite reducing enzyme from Nitrosomonas europaea. Preliminary characterization with hydroxylamine as electron donor. Biochim. Biophys. Acta 162: 49–65

    Google Scholar 

  • Hooper AB (1984) Ammonia oxidation and energy transduction in the nitrifying bacteria. In: Strohl WR & Tuovinen OH (Eds) Microbial Chemoautotrophy (pp 133–167). Ohio State University Press, Columbus, Ohio

    Google Scholar 

  • Hooper AB & Terry KR (1973) Specific inhibitors of ammonia oxidation in Nitrosomonas. J. Bacteriol. 115: 480–485

    Google Scholar 

  • Hooper AB & Terry KR (1974) Photoinactivation of ammonia oxidation in Nitrosomonas. J. Bacteriol. 119: 899–906

    Google Scholar 

  • Hooper AB, Maxwell PC & Terry KR (1978) Hydroxylamine oxidoreductase from Nitrosomonas: Absorption spectra and content of heme and metal. Biochem. 17: 2984–2989

    Google Scholar 

  • Hooper AB, DiSpirito AA, Olson KA, Anderson A, Cunningham W & Taaffee LR (1984) Genertation of the proton gradient by a periplasmic dehydrogenase. In: Crawford RL & Hanson RS (Eds) Microbial Growth on C1 Compounds. (pp 53–58). Society for Microbiology, Washington, DC

    Google Scholar 

  • Hooper AB, Arciero DM, DiSpirito AA, Fuchs J, Johnson M, Mundfrom G & McTavish H. (1990) Production of nitrite and N2O by the ammonia oxidizing nitrifiers. In: Gresshoff PM, Roth LE, Stacey G & Newton WE (Eds) Nitrogen Fixation: Achievement and Objectives (pp 387–392). Chapman and Hall, New York and London

    Google Scholar 

  • Horrigan SG & Springer AL (1990) Oceanic and estuarine ammonium oxidation: effects of light. Limnol. Oceanog. 35: 479–482

    Google Scholar 

  • Hutton WE & ZoBell CE (1953) Production of nitrite from ammonia by methane oxidizing bacteria. J. Bacteriol. 65: 216–219

    Google Scholar 

  • Hyman MR & Wood PM (1983) Methane oxidation by Nitrosomonas europaea. Biochem. J. 212: 31–37

    Google Scholar 

  • Hyman MR & Wood PM (1984) Ethylene oxidation by Nitrosomonas europaea. Arch. Microbiol. 137: 155–158

    Google Scholar 

  • Hyman MR & Wood PM (1985) Suicidal inactivation and labeling of ammonia monooxygenase by acetylene. Biochem. J. 227: 719–725

    Google Scholar 

  • Hyman MR & Arp DJ (1992) 14C2H2 and 14CO2 labeling studies of the de novo synthesis of polypeptides by Nitrosomonas europaea during recovery from acetylene and light inactivation of ammonia monooxygenase. J. Biol. Chem. 267: 1534–1545

    Google Scholar 

  • Hyman MR, Sansome-Smith AW, Shears JH & Wood PM (1985) A kinetic study of benzene oxidation to phenol by whole cells of Nitrosomonas europaea and evidence for the further oxidation of phenol to hydroquinone. Arch. Microbiol. 143: 302–306

    Google Scholar 

  • Hyman MR, Murton JB & Arp DJ (1988) Interaction of ammonia monooxygenase from Nitrosomonas europaea with alkanes, alkenes and alkynes. Appl. Environ. Microbiol. 54: 3187–3190

    Google Scholar 

  • Johnstone BH & Jones RD (1988) Effects of light and CO on the survival of a marine ammonium oxidizing bacterium during energy source deprivation. Appl. Environ. Microbiol. 54: 2890–2893

    Google Scholar 

  • Jones RD & Morita RY (1983) Methane oxidation by Nitrosomonas oceanus and Nitrosomonas europaea. Appl. Environ. Microbiol. 45: 401–410

    Google Scholar 

  • Killham K (1986) Heterotrophic nitrification. In: Prosser JI (Ed) Nitrification (pp 117–126). IRL Press, Oxford, Washington, DC

    Google Scholar 

  • Kim K & Craig H (1990) Two isotope characterization of N2O in the Pacific Ocean and constraints on its origin in deep water. Nature 347: 58–61

    Google Scholar 

  • King JM & Spotte SH (1974) Marine aquariums in the research laboratory. Aquarium Systems, Inc. East Lake, Ohio

    Google Scholar 

  • Kinne O (1976) Cultivation of marine organisms: water quality management and technology. In: Kinne O (Ed) Mar. Ecol. Vol 3 (pp 19–268). John Wiley & Sons, London, New York, Sydney, Toronto

    Google Scholar 

  • Klemendtsson L, Svensson BH & Rosswall T (1988) Relationship between soil moisture content and nitrous oxide production during nitrification and denitrification. Biol. Fertil. Soils 6: 106–111

    Google Scholar 

  • Knowles R & Lean DRS (1987) Nitrification: a significant case of oxygen depletion under winter ice. Can J. Fish. Aquat. Sci. 44: 743–749

    Google Scholar 

  • Matulewich VA, Storm PF & Finstein M (1975) Length of incubation for enumerating nitrifying bacteria present in various environments. Appl. Microbiol 29: 265–268

    Google Scholar 

  • McCarty GW, Bremmer JM & Schmidt EL (1991) Effects of phenolic acids on ammonia oxidation by terrestrial autotrophic nitrifying microorganisms. FEMS Microbiol. Ecol. 85: 345–349

    Google Scholar 

  • Miyazaki T, Wada E & Hattori A (1973) Capacities of shallow waters of Sagami Bay for oxidation and reduction of inorganic nitrogen. Deep Sea Res. 20: 571–577

    Google Scholar 

  • Nagano T & Fridovich I (1985) The co-oxidation of ammonia to nitrite during the aerobic xanthine oxidase reaction. Arch. Biochem. Biophys. 241: 596–601

    Google Scholar 

  • Ng AS & Stenstrom MK (1987) Nitrification in powdered activated sludge process. J. Environ. Engn. 113: 1285–1301

    Google Scholar 

  • Olson TC & Hooper AB (1983) Energy coupling in the bacterial oxidation of small molecules: an extra cytoplasmic dehydrogenase in Nitrosomonas. FEMS Microbiol. Lett. 19: 47–50

    Google Scholar 

  • Papen H, von Berg R, Hinkel I, Thoene B & Rennenberg H (1989) Heterotrophic nitrification by Alcaligenes faecalis: NO2 -, NO3 -, N2O and NO production in exponentially growing cultures. Appl. Environ. Microbiol. 55: 2068–2072

    Google Scholar 

  • Pontius FW (1991) Phase III organic and inorganic contaminant regulations. J. AWWA 83: 20–22, 77–79

    Google Scholar 

  • Poth M (1986) Dinitrogen production from nitrite by Nitrosomonas isolate. Appl. Environ. Microbiol. 52: 957–959

    Google Scholar 

  • Poth M & Focht DD (1985) 15N kinetic analysis of N2O production by Nitrosomonas europaea: an examination of nitrifier denitrification. Appl. Environ. Microbiol. 49: 1134–1141

    Google Scholar 

  • Priscu JC, Downes MT, Priscu LR, Palmisano C & Sullivan CW (1990) Dynamics of ammonium oxidizer activity and N2O within and beneath Antarctic sea ice. Mar. Ecol. Prog. Ser. 62: 37–46

    Google Scholar 

  • Rasche EM, Hicks RE, Hyman MR & Arp DJ (1990a) Oxidation of monohalogenated ethanes and n-chlorinated alkanes by whole cells of Nitrosomonas europaea. J. Bacteriol. 172: 5368–5373

    Google Scholar 

  • Rasche EM, Hyman MR & Arp DJ (1990b) Biodegradation of halogenated hydrocarbon fumigants by nitrifying bacteria. Appl. Environ. Microbiol. 56: 2568–2571

    Google Scholar 

  • Rasche EM, Hyman MR & Arp DJ (1991) Factors limiting aliphatic chlorocarbon degradation by Nitrosomonas europaea: cometabolic inactivation of ammonia monooxygenase and substrate specificity. Appl. Environ. Microbiol. 57: 2986–2994

    Google Scholar 

  • Ratnayake M & Audas LJ (1978) Studies on the effects of herbicides on soil nitrification. Pesticide Biochem. Physiol 8: 170–185

    Google Scholar 

  • Remde A & Conrad R (1990) Production of nitric oxide in Nitrosomonas europaea by reduction of nitrite. Arch. Microbiol. 154: 187–191

    Google Scholar 

  • Revsbech NP & Sorensen J (Eds) (1990) Denitrification in Soil and Sediment. Plenum Press, New York and London

    Google Scholar 

  • Rice EL & Pancholy SK (1972) Inhibition of nitrification by climax ecosystems. Am. J. Bot. 59: 1033–1040

    Google Scholar 

  • Ritchie GAF & Nicholas DJD (1972) Identification and characterization of nitrous oxide produced by oxidative and reductive processes in Nitrosomonas europaea. Biochem. J. 126: 1181–1191

    Google Scholar 

  • Robertson LA & Kuenen JG (1988) Heterotrophic nitrification in Thiosphaera pantotropha: oxygen uptake and enzyme studies. J. Gen. Microbiol. 134: 857–863

    Google Scholar 

  • Robertson LA & Luenen JG (1990) Physiological and ecological aspects of aerobic denitrification, a link with heterotrophic nitrification? In: Revsbech NP & Sorensen J (Eds) Denitrification in Soil and Sediment (pp 91–104). Plenum Press, New York and London

    Google Scholar 

  • Shears JH & Wood PM (1985) Spectroscopic evidence for a photosensitive oxygenated state of ammonia mono-oxygenase. Biochem. J. 266: 499–507

    Google Scholar 

  • Soares MIM, Belkin S & Abeliovich A (1989) Clogging of microbial denitrification in sand columns: gas bubbles or biomass accumulation. Was.-Abwas. Forsch. 22: 20–24

    Google Scholar 

  • Soares MIM, Braester C, Belkin S & Abeliovich A (1991) Denitrification in laboratory sand columns: carbon regime, gas accumulation and hydraulic properties. Wat. Res. 25: 325–332

    Google Scholar 

  • Tan KH & Lopez-Falcon RA (1987a) Effect of fulvic and humic acids on nitrification. Part I. In vitro production of nitrite and nitrate. Commun. Soil Sci. Plant Anal. 18: 835–853

    Google Scholar 

  • Tan KH & Lopez-Falcon RA (1987b) Effect of fulvic and humic acids on nitrification. Part II. The nitrifying potential of cecil and davidson soils. Commun. Soil Sci. Plant Anal. 18: 855–873

    Google Scholar 

  • Terry KR & Hooper AB (1981) Hydroxylamine oxidoreductase: a 20-heme, 200,000 molecular weight cytochrome c with unusual denaturation properties which forms a 63,000 molecular weight monomer after heme removal. Biochem. 20: 7026–7032

    Google Scholar 

  • Underhill SE & Prosser JI (1987) Surface attachment of nitrifying bacteria and their inhibition by potassium ethyl xanthate. Microb. Ecol. 14: 129–139

    Google Scholar 

  • US Environmental Protection Agency: Quality criteria for water. 1976. Publication No. 440-976-023. Cincinnati, OH, USA

  • Van Miegroet H & Cole DW (1984) The impact of nitrification on soil acidification and cation leaching in a red alder ecosystem. J. Environ. Qual. 13: 586–590

    Google Scholar 

  • Van Miegroet H & Cole DW (1985) Acidification sources in red alder and Douglas fir soils-importance of nitrification. Soil Sci. Soc. Amer. J. 49: 1274–1279

    Google Scholar 

  • Vannelli T, Logan M, Arciero DM & Hooper AB (1990) Degradation of halogenated aliphatic compounds by the ammonia oxidizing bacterium Nitrosomonas europaea. Appl. Environ. Microbiol. 56: 1169–1171

    Google Scholar 

  • Voysey PA & Wood PM (1987) Methanol and formaldehyde oxidation by an autotrophic nitrifying bacterium. J. Gen. Microbiol. 33: 283–290

    Google Scholar 

  • Ward BB (1984) Combined autoradiograph and immunofluorescence for estimation of single cell activity by ammonium oxidizing bacteria. Limnol. Oceanogr. 29: 402–410

    Google Scholar 

  • Wasserbauer R, Zadak Z & Novotny J (1988) Nitrifying bacteria on the asbestos cement roofs of stable buildings. Internat. Biodeterior. 24: 153–165

    Google Scholar 

  • White CS & Gosz JR (1987) Factors controlling nitrogen mineralization and nitrification in forest ecosystems in New Mexico. Biol. Fert. Soil. 5: 195–202

    Google Scholar 

  • Wittenbury RK, Phillips C & Wilkinson JF (1970) Enrichment, isolation and some properties of methane utilizing bacteria. J. Gen. Microbiol. 61: 205–218

    Google Scholar 

  • Witzel KP & Overbeck HJ (1979) Heterotrophic nitrification by Arthrobacter sp (strain 9006) as influenced by different cultural conditions, growth state and acetate metabolism. Arch. Microbiol. 122: 13–143

    Google Scholar 

  • Wolfe RL, Means EGIII, Davis MK & Barrett SE (1988) Biological nitrification in covered reservoirs containing chloraminated water. J. AWWA 80: 109–114

    Google Scholar 

  • Yamanaka T & Fukumori Y (1988) The nitrite oxidizing system of Nitrobacter winogradskyi. FEMS Microbiol. Revs. 54: 259–271

    Google Scholar 

  • Yamanaka T & Sakano Y (1980) Oxidation of hydroxylamine to nitrite catalyzed by hydroxylamine oxidoreductase purified from Nitrosomonas europaea. Curr. Microbiol. 4: 239–244

    Google Scholar 

  • Yamanaka T, Shimura M, Takahashi K & Shibasaka M (1979) Highly purified hydroxylamine oxidoreductase derived from Nitrosomonas europaea. J. Biochem. 86: 1101–1108

    Google Scholar 

  • Yoshida N (1988) 15N depleted N2O as product of nitrification. Nature 335: 528–529

    Google Scholar 

  • Yoshioka T & Saijo Y (1984) Photoinhibition and recovery of NH4 + oxidizing bacteria and NO2 - oxidizing bacteria. J. Gen. Appl. Microbiol. 30: 151–166

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Environmental Microbiology Unit, The Jacob Blaustein Institute for Desert Research, Ben-Gurion University, Israel

    Aharon Abeliovich

Authors
  1. Aharon Abeliovich
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Abeliovich, A. Transformations of ammonia and the environmental impact of nitrifying bacteria. Biodegradation 3, 255–264 (1992). https://doi.org/10.1007/BF00129087

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00129087

Key words

Search

Navigation