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Combined heterotrophic nitrification and aerobic denitrification in Thiosphaera pantotropha and other bacteria

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Abstract

Reports of the simultaneous use of oxygen and denitrification by different species of bacteria have become more common over the past few years. Research with some strains (e.g. Thiosphaera pantotropha) has indicated that there might be a link between this ‘aerobic denitrification’ and a form of nitrification which requires rather than generates energy and is therefore known as heterotrophic nitrification. This paper reviews recent research into heterotrophic nitrification and aerobic denitrification, and presents a preliminary model which, if verified, will provide at least a partial explanation for the simultaneous occurrence of nitrification and denitrification in some bacteria.

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References

  • Abou Seada MNI & Ottow JCG (1985) Effect of increasing oxygen concentration on total denitrification and nitrous oxide release from soil by different bacteria. Biol. Fert. Soils 1: 31–38

    Google Scholar 

  • Alefounder PR & Ferguson SJ (1981) The location of dissimilatory nitrite reductase and the control of dissimilatory nitrate reductase by oxygen in Paracoccus denitrificans. Biochem. J. 192: 231–240

    Google Scholar 

  • Alefounder PR, Greenfield AJ, McCarthy JEG & Ferguson SJ (1983) Selection and organisation of denitrifying electrontransfer pathways in Paracoccus denitrificans. Biochim. Biophys. Acta 724: 20–39

    Google Scholar 

  • Alefounder PR, Greenfield AJ, McCarthy JEG & Ferguson SJ (1984) The basis for preferential electron flow to oxygen rather than nitrogen oxides in the denitrifying bacterium Paracoccus denitrificans. In: Poole RK & Dow CS (Eds) Microbial Gas Metabolism-Mechanistic, Metabolic and Biotechnological Aspects (pp 225–230) Academic Press

  • Anderson IC & Levine JS (1986) Relative rates of NO and N2O production by nitrifiers, denitrifiers and nitrate respirers. Appl. Env. Microbiol. 51: 938–945

    Google Scholar 

  • Beudeker RF, Gottschal JC & Kuenen JG (1982) Reactivity versus flexibility in Thiobacilli. Ant. van Leeuwenhoek 48: 39–51

    Google Scholar 

  • Boogerd FC (1984) Energetic aspects of denitrification in Paracoccus denitrification. PhD thesis. Free University of Amsterdam, the Netherlands

  • Castignetti D, Hollocher TC (1984) Heterotrophic nitrification among denitrifiers. Appl. Env. Microbiol. 47: 620–623

    Google Scholar 

  • Castignetti D & Hollocher TC (1982) Nitrogen redox metabolism of a heterotrophic, nitrifying-denitrifying Alcaligenes sp. from soil. Appl. Env. Microbiol. 44: 923–928

    Google Scholar 

  • Castignetti D (1988) An examination of protein translocation and energy conservation during heterotrophic nitrification. Abstracts of the International Workshop on Nitrification in Terrestial and Aquatic Ecosystems (Arnhem)

  • Chandra TS & Friedrich CG (1986) TnS-induced mutations affecting sulfure-oxidizing ability (Sox) of Thiosphaera pantotropha. J. Bact. 166: 446–452

    Google Scholar 

  • Dalton H (1977) Ammonia oxidation by the methane oxidizing bacterium Methylococcus capsulatus strain Bath. Arch. Microbiol. 114: 273–279

    Google Scholar 

  • Davies KJP, Lloyd D & Boddy L (1989) The effect of oxygen on denitrification in Paracoccus denitrificans and Pseudomonas aeruginosa. J. Gen. Microbiol. 136: 2945–2451

    Google Scholar 

  • Degn H, Cox RP & Lloyd D (1985) Continuous measurement of dissolved gases in biochemical systems with the quadrupole mass spectrometer. Methods Biochem. Anal. 31: 166–194

    Google Scholar 

  • Drozd JW, Godley A & Baley MI (1978) Ammonia oxidation by methane-oxidizing bacteria. Proc. Soc. Gen. Microbiol. 5: 66–67

    Google Scholar 

  • Dua RD, Bhandari B & Nicholas DJD (1979) Stable isotope studies on the oxidation of ammonia to hydroxylamine by Nitrosomonas europaea. FEMS Letts. 106: 401–404

    Google Scholar 

  • Gommers PJF, VanSchie BJ, VanDijken JP & Kuenen JG (1988) Biochemical limits to microbiological growth yields. Biotech. Bioeng. 32: 86–94

    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 (1981) Ammonium oxidation and energy transduction in the nitrifying bacteria. In: Strohl WR & Tuovinen OH (Ed) Microbial Chemoautotrophy (pp 133–167)

  • Iwasaki H & Matsubara T (1972) A nitrite reductase from Achromobacter cycloclastes. J. Biochem. 78: 355–361

    Google Scholar 

  • Iwasaki H, Shidara S, Suzuki H & Mori T (1963) Studies on denitrification. VIII. Further purification and properties of denitrifying enzyme. J. Biochem. 53: 299–303

    Google Scholar 

  • Iwasaki H, Noji S & Shidara S (1975) Achromobacter cycloclastes nitrite reductase. The function of copper, amino acid composition and ESR spectra. J. Biochem. 78: 355–361

    Google Scholar 

  • Kawakami Y, Pacaud B & Nishimura H (1985) Inhibition of denitrification by oxygen in Paracoccus denitrificans. J. Ferment. Technol. 63: 437–442

    Google Scholar 

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

  • Körner H & Zumft WG (1989) Expression of denitrification enzymes in response to the dissolved oxygen level and respiratory substrate in continuous culture of Pseudomonas stutzeri. Appl. Env. Microbiol. 55: 1670–1676

    Google Scholar 

  • Knowles R (1982) Denitrification. Microbiol. Rev. 46: 43–70

    Google Scholar 

  • Kučera I & Dadák V (1983) The effect of uncoupler on the distribution of the electron flow between the terminal acceptors oxygen and nitrite in the cells of Paracoccus denitrificans. Biochem. Biophys. Res. Comm. 117: 252–258

    Google Scholar 

  • Kučera I, Bourblikova P & Dadák V (1984) Function of terminal acceptors in the biosynthesis of denitrification pathway components in Paracoccus denitrificans Folia Microbiol. 29: 108–114

    Google Scholar 

  • Kuenen JG & Robertson LA (1987) Ecology of nitrification and denitrification. In: Cole JA & Ferguson S (Eds) The Nitrogen and Sulphur Cycles (pp 162–218) Cambridge University Press

  • Kurokawa M, Fukumori Y & Yamanaka T (1985) A hydroxylamine-cytochrome c reductase occurs in the heterotrophic nitrifier Arthrobacter globiformis. Plant Cell Physiol. 26: 1439–1442

    Google Scholar 

  • Lloyd D, Boddy L & Davies KJP (1987) Persistance of bacterial denitrification capacity under aerobic conditions: the rule rather than the exception. FEMS Microbiol. Ecol. 45: 185–190

    Google Scholar 

  • Lloyd D, Davies KJP & Boddy L (1986) Mass spectrometry as an ecological tool for in situ measurement of dissolved gases in sediment systems. FEMS Microbiol. Ecol. 38: 11–17

    Google Scholar 

  • Payne WJ (1981) Denitrification. John Wiley & Sons

  • Reuner ED & Becker GE (1970) Production of nitric oxide and nitrous oxide during denitrification by Corynebacterium nephridii. J. Bacteriol. 101: 821–826

    Google Scholar 

  • Robertson LA (1988) Aerobic denitrification and heterotrophic nitrification in Thiosphaera pantotropha and other bacteria. PhD thesis, Delft University of Technology, the Netherlands

  • Robertson LA & Kuenen JG (1983) Thiosphaera pantotropha gen. nov. sp. nov., a facultatively anaerobic, facultatively autotrophic sulphur bacterium. J. Gen. Microbiol. 129: 2847–2855

    Google Scholar 

  • Robertson LA & Kuenen JG (1984a) Aerobic denitrification-old wine in new bottles? Ant. van Leeuwenhoek 50: 525–544

    Google Scholar 

  • Robertson LA & Kuenen KG (1984b) Aerobic denitrification: a controversy revived. Arch. Microbiol. 139: 351–354

    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 Cornelisse R, De Vos P, Hadioetomo R & Kuenen JG (1989a) Aerobic denitrification in various heterotrophic nitrifiers. Antonie van Leeuwenhoek 56: 289–300

    Google Scholar 

  • Robertson LA, Cornelisse R, Zeng R & Kuenen JG (1989b) The effect of thiosulphate and other inhibitors of autotrophic nitrification on heterotrophic nitrifiers. Antonie van Leeuwenhoek 56: 301–310

    Google Scholar 

  • Robertson LA, Van Kleeff BHA & Kuenen JG (1986) A microcomputer-based method for semi-continuous monitoring of biological activities. J. Microbiol. Methods 5: 237–242

    Google Scholar 

  • Robertson LA, Van Niel EWJ, Torremans RAM & Kuenen JG (1988) Simultaneous nitrification and denitrification in aerobic chemostat cultures of Thiosphaera pantotropha. Appl. Env. Microbiol. 54: 2812–2818

    Google Scholar 

  • Sapshead LM & Wimpenny JWT (1972) The influence of oxygen and nitrate on the formation of the cytochrome pigments of the aerobic and anaerobic respiratory chain of Micrococcus denitrificans. Biochim. Biophys. Acta. 267: 388–397

    Google Scholar 

  • Sawada E, Satoh T & Kitamura H (1978) Purification and properties of a dissimilatory nitrate reductase of a denitrifying phototrophic bacterium. Plant Cell Physiol. 19: 1339–1351

    Google Scholar 

  • Shapleigh JP & Payne WJ (1985) Differentiation of c,d1 cytochrome and copper nitrite reductase production in denitrifiers. FEMS Microbiol Letts. 26: 275–279

    Google Scholar 

  • Stouthamer AH (1980) Bioenergetic studies on Paracoccus denitrificans. Trends Biochem. Sci. 5: 164–166

    Google Scholar 

  • Stouthamer AH (1988a) Dissimilatory reduction of oxidized nitrogen compounds. In: Zehnder AJB (Ed) Environmental Microbiology of Anaerobes (pp 245–303) John Wiley and Sons

  • Stouthamer AH (1988b) Bioenergetic and yields with electron acceptors other than oxygen. In: Yee-Chak Fung D & Erikson LE (Eds) Handbook on Anaerobic Fermentations (pp 345–440) Marcel Dekker Inc

  • Strand SE, McDonnell AJ & Unz RF (1988) Oxygen and nitrate reduction kinetics of a nonflocculating strain of Zooglea ramigera. Antonie van Leeuwenhoek 54: 245–255

    Google Scholar 

  • Suzuki I, Kwok S-C & Dular U (1976) Competitive inhibition of ammonia oxidation in Nitrosomonas europaea by methane, carbon monoxide or methanol. FEBS letts. 72: 117–120

    Google Scholar 

  • Verstraete W (1975) Heterotrophic nitrification in soils and aqueous media. Izvestija Akademii Nauk SSSR Ser. Biol. 4: 541–558

    Google Scholar 

  • Verstraete W & Alexander M (1972) Heterotrophic nitrification by Arthrobacter sp. J. Bacteriol. 110: 955–961

    Google Scholar 

  • Wood P (1986) Nitrification as a bacterial energy source. In: Prosser JI (Ed) Nitrification (pp 39–62) IRL Press

  • Zumft WG & Matsubara T (1982) A novel kind of multi-copper protein as terminal oxidoreductase of nitrous oxide respiration in Pseudomonas perfectomarinus. FEBS Letts. 148: 107–112

    Google Scholar 

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  1. Kluyver Laboratory for Biotechnology, Delft University of Technology, Delft, The Netherlands

    Lesley A. Robertson & J. Gijs Kuenen

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  1. Lesley A. Robertson
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  2. J. Gijs Kuenen
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Robertson, L.A., Kuenen, J.G. Combined heterotrophic nitrification and aerobic denitrification in Thiosphaera pantotropha and other bacteria. Antonie van Leeuwenhoek 57, 139–152 (1990). https://doi.org/10.1007/BF00403948

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  • DOI: https://doi.org/10.1007/BF00403948

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