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NITROGEN IN SOILS/Nitrification 31 See also: Eutrophication; Greenhouse Gas Emis- Powlson DS (1993) Understanding the soil nitrogen cycle. sions; Isotopes in Soil and Plant Investigations; Soil Use and Management 9: 86–94. Nitrogen in Soils: Cycle; Nitrification; Plant Uptake; Powlson DS (1999) Fate of nitrogen from manufactured Symbiotic Fixation; Pollution: Groundwater fertilizers in agriculture. In: Wilson WS, Ball AS, and Hinton RH (eds) Managing Risks of Nitrates to Humans Further Reading and the Environment, pp. 42–57. Cambridge: Royal Society of Chemistry. Addiscott TM, Whitmore AP, and Powlson DS (1991) Powlson DS (1997) Integrating agricultural nutrient man- Farming, Fertilizers and the Nitrate Problem. Wallingford: agement with environmental objectives – current state CAB International. and future prospects. Proceedings No. 402. York: The Benjamin N (2000) Nitrates in the human diet – good or Fertiliser Society. bad? Annales de Zootechnologie 49: 207–216. Powlson DS, Hart PBS, Poulton PR, Johnston AE, and Catt JA et al. (1998) Strategies to decrease nitrate leaching Jenkinson DS (1986) Recovery of 15N-labelled fertilizer in the Brimstone Farm experiment, Oxfordshire, UK, applied in autumn to winter wheat at four sites in eastern 1988–1993: the effects of winter cover crops and England. Journal of Agricultural Science, Cambridge unfertilized grass leys. Plant and Soil 203: 57–69. 107: 611–620. Cheney K (1990) Effect of nitrogen fertilizer rate on soil Recous S, Fresnau C, Faurie G, and Mary B (1988) The fate nitrate nitrogen content after harvesting winter wheat. of labelled 15N urea and ammonium nitrate applied to a Journal of Agricultural Science, Cambridge 114: winter wheat crop. Plant and Soil 112: 205–214. 171–176. Wilson WS, Ball AS, and Hinton RH (eds) (1999) Managing Davidson EA (1991) Fluxes of nitrous oxide and nitric Risks of Nitrates to Humans and the Environment. oxide from terrestrial ecosystems. In: Rogers JE and Cambridge: Royal Society of Chemistry. Whitman WB (eds) Microbial Production and Con- sumption of Greenhouse Gases: Methane, Nitrogen Oxides, Halomethanes, pp. 219–235. Washington, DC: American Society for Microbiology. Dykhuizen RS, Fraser A, Duncan C, Golden M, Benjamin Nitrification N, and Leifert C (1999) Antimicrobial effect of acidified nitrite on gut pathogens: the importance of dietary ni- J I Prosser, University of Aberdeen, Aberdeen, UK trate in host defences. In: Wilson WS, Ball AS, and ß 2005, Elsevier Ltd. All Rights Reserved. Hinton RH (eds) Managing Risks of Nitrates to Humans and the Environment, pp. 295–316. Cambridge: Royal Society of Chemistry. Introduction Goss MJ, Howse KR, Christian DG, Catt JA, and Pepper TJ (1998) Nitrate leaching: modifying the loss from miner- Nitrification is the oxidation of reduced forms of alized organic matter. European Journal of Soil Science nitrogen, ultimately to nitrate. It is carried out by 49: 649–659. three microbial groups: (1) autotrophic ammonia Goulding K (2000) Nitrate leaching from arable and oxidizers, (2) autotrophic nitrite oxidizers, and (3) het- horticultural land. Soil Use and Management 16: erotrophic nitrifiers. Autotrophic ammonia and ni- 145–151. trite oxidizers are characterized by their ability to Goulding KWT, Poulton PR, Webster CP, and Howe MT oxidize ammonia sequentially to nitrate under aerobic (2000) Nitrate leaching from the Broadbalk wheat conditions, but these organisms possess a wider meta- experiment, Rothamsted, UK, as influenced by fertilizer and manure inputs and weather. Soil Use and Manage- bolic diversity. This has significant consequences for ment 16: 244–250. their ecology, for the occurrence and kinetics of nitri- Hatch D, Goulding K, and Murphy D (2002) Nitrogen. fication, and for interactions with other organisms. In: Haygarth PM and Jarvis SC (eds) Agriculture, The major sources of reduced forms of soil nitrogen Hydrology and Water Quality, pp. 7–27. Wallingford: are excretion and decomposition of organic nitrogen, CAB International. derived from animals and plants, and application Jarvis SC (2000) Progress in studies of nitrate leaching from of ammonia-based fertilizers. Many microorganisms grassland. Soil Use and Management 16: 152–156. and plants require ammonium for growth, while Macdonald AL, Powlson DS, Poulton PR, and Jenkinson others assimilate nitrate. For both groups, nitrifica- DS (1989) Unused fertilizer nitrogen in arable soils – its tion is important in regulating the supply or loss of contribution to nitrate leaching. Journal of the Science of nitrogen from the environment. While ammonia has a Food and Agriculture 46: 407–419. Macdonald AJ, Poulton PR, Powlson DS, and Jenkinson DS propensity to bind to soil particles, its conversion to (1997) Effects of season, soil type and cropping on re- nitrate leads to significant losses of soil nitrogen coveries, residues and losses of 15N-labelled fertilizer through leaching and conversion to gaseous forms applied to arable crops in spring. Journal of Agricultural through denitrification. Nitrification also contributes Science, Cambridge 129: 125–154. to soil acidification, with consequent increases in 32 NITROGEN IN SOILS/Nitrification mobilization of toxic metals, particularly in heavily In the first step, ammonia is oxidized to hydroxyl- fertilized and poorly buffered soils. In addition, nitri- amine by a membrane-bound ammonia monooxygen- fiers are involved in production and conversion of a ase. The reaction is endergonic and requires oxygen number of greenhouse gases. and a source of reducing equivalents. Hydroxylamine is then oxidized to nitrite by hydroxylamine oxido- Autotrophic Ammonia-Oxidizing Bacteria reductase, using oxygen from water in an exergonic reaction. Two electrons are required for ammonia oxi- Taxonomy dation, while the remainder pass down the electron transport chain. The NOÀ/NH redox potential is Autotrophic ammonia oxidizers are Gram-negative 2 3 À340 mV and reduced nicotinamide adenine dinucleo- bacteria, traditionally placed within the Nitrobacter- tide (NADH) is synthesized by reverse electron flow iaceae and characterized by their ability to oxidize using adenosine triphosphate (ATP). Hydrogen ions ammonia. Further classification is based on a limited generated by the second step lead to acidification of number of characteristics, including cell shape, unbuffered growth medium, limiting sustained growth. internal membrane structures, flagella, inclusion An alternative mechanism for the first step has bodies, salt tolerance, urease activity, and substrate recently been proposed, involving nitrogen dioxide affinity and inhibition. Confirmation of taxonomic and tetroxide, based on studies of N. eutropha: groupings and species descriptions is by DNA:DNA þ À hybridization of pure cultures. The type strain, Nitro- NH3 þ N2O4 þ 2H þ 2e ! NH2OH þ 2NO þ H2O somonas europaea, has been the subject of the 2NO þ O2 ! 2NO2ðN2O4Þ majority of biochemical, physiological, and genomic studies. This mechanism does not appear to involve ammonia More recently, analysis of sequences of 16S riboso- monooxygenase, and studies have also demonstrated mal ribonucleic acid (rRNA) and amo A genes (encod- reduction in lag phase and the stimulation of growth, ing the active subunit of ammonia monooxygenase) activity, and cell yield in cultures supplied with nitric has enabled phylogenetic classification of cultured oxide. Any reduction in lag phase will provide ammo- ammonia oxidizers. This places Nitrosococcus ocea- nia oxidizers with advantages in soil where ammonia nus in the -proteobacteria and other known auto- supply is intermittent. trophic ammonia oxidizers in seven lineages within a monophyletic group within the -proteobacteria: Carbon Metabolism Nitrosospira, Nitrosomonas europaea/Nitrosococcus Organic carbon is obtained by nitrifiers via carbon mobilis, Nitrosomonas communis, Nitrosomonas ma- dioxide fixation, and all strains studied as of 2003 rina, Nitrosomonas oligotropha, Nitrosomonas cryo- possess type I Rubisco genes, but with sequence vari- tolerans,andNitrosomonas sp. Nm143. Difficulties in ation between strains. Rubisco enzymes in some strains cultivating ammonia oxidizers limit available physio- are located in carboxysomes. Energy generated by am- logical data, but links exist between these phylogene- monia oxidation is only just sufficient for growth, par- tic groups, their physiological characteristics, and ticularly as carbon dioxide fixation requires significant their environmental origin. Analysis of 16S rRNA reducing equivalents, and generation of reducing gene sequences also indicates evolutionary relation- equivalents consumes ATP. ships with photosynthetic bacteria and other groups Ammonia monooxygenase has broad substrate possessing intracytoplasmic membrane structures, sug- specificity, and ammonia oxidizers can oxidize and gesting that ammonia oxidizers evolved from photo- assimilate, but not grow on, a number of organic com- synthetic organisms. 16S rRNA sequence analysis pounds, including methanol, bromoethane, ethylene, suggests only peripheral associations with methane propylene, cyclohexane, benzene, and phenol. Acet- oxidizers, but similarities exist between amoAgenes ate, formate, and pyruvate can increase biomass yield of -proteobacterial ammonia oxidizers (N. oceanus), by as much as 130%, but higher concentrations in- and pMMO (particulate methane monooxygenase), hibit growth. The ecological implications for this are suggesting a common ancestral origin. not clear, but assimilation of soil organic
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