Abstract
Autotrophic ammonia oxidizers depend on alkaline or neutral conditions for optimal activity. Below pH 7 growth and metabolic activity decrease dramatically. Actively oxidizing cells of Nitrosomonas europaea do not maintain a constant internal pH when the external pH is varied from 5 to 8. Studies of the kinetics and pH-dependency of ammonia and hydroxylamine oxidation by N. europaea revealed that hydroxylamine oxidation is moderately pH-sensitive, while ammonia oxidation decreases strongly with decreasing pH. Oxidation of these oxogenous substrates results in the generation of higher proton motive force which is mainly composed of a ΔΨ. Hydroxylamine, but not ammonia, is oxidized at pH 5, which leads to the generation of a high proton motive force which drives energy-dependent processes such as ATP-synthesis and secondary transport of amino acids.
Endogenoussubstrates can be oxidized between pH 5 to 8 and this results in the generation of a considerable proton motive force which is mainly composed of a ΔΨ. Inhibition of ammonia-mono-oxygenase or cytochrome aa3 does not influence the magnitude of this gradient or the oxygen consumption rate, indicating that endogenous respiration and ammonia oxidation are two distinct systems for energytransduction.
The results indicate that the first step in ammonia oxidation is acid sensitive while the subsequent steps can take place and generate a proton motive force at acid pH.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Bédard C, Knowles R (1989) Physiology, biochemistry, and specific inhibitors of CH4, NH +4 , and CO oxidation by methanotrophs and nitrifiers. FEMS Microbiol Rev 53: 68–84
Bhandari B, Nicholas DJD (1979) Ammonia and O2 uptake in relation to proton translocation in cells of Nitrosomonas europaea. Arch Microbiol 122: 249–255
Bhuiya ZH, Walker N (1977) Autotrophic nitrifying bacteria in acid tea soils from Bangladesh and Sri Lanka. J Appl Bacteriol 42: 253–257
Bock E, Koops HP, Harms H (1986) Cell biology of nitrifying bacteria. In: Prosser JI (ed) Nitrification Special publication 20. IRL Press, Oxford, pp 17–38
Clark C, Schmidt EL (1967a) Growth response of Nitrosomonas europaea to amino acids. J Bacteriol 93: 1302–1308
Clark C, Schmidt EL (1967b) Uptake and utilisation of amino acids by resting cells of Nitrosomonas europaea. J Bacteriol 93: 1309–1315
DeBoer W, Duyts H, Laanbroek HJ (1988) Autotrophic nitrification in a fertilized acid heath soil. Soil Biol Biochem 20: 845–850
DeBoer W, Duyts H, Laanbroek HJ (1989) Urea stimulated autotrophic nitrification in suspensions of fertilized, acid health soil. Soil Biol Biochem 21: 349–354
DeBoer W, Laanbroek HJ (1989) Ureolytic nitrification at low pH by Nitrosospira spec. Arch Microbiol 152: 178–181
Drozd JW (1976) Energy coupling and respiration in Nitrosomonas europaea. Arch Microbiol 110: 257–262
Focht DD, Verstraete W (1977) Biochemical ecology of nitrification and denitrification. Adv Microbiol Ecol 1: 135–214
Hankinson TR, Schmidt EL (1984) Examination of an acid forest soil for ammonia-and nitrite-oxidizing bacteria. Can J Microbiol 30: 1125–1132
Hyman MR, Wood PM (1983) Methane oxidation by Nitrosomonas europaea. Biochem J 212: 31–37
Kumar S, Nicholas DJD (1982) A protonmotive force-dependent adenosine-5′ triphosphate synthesis in spheroplasts of Nitrosomonas europaea. FEMS Microbiol Lett 14: 21–25
Kumar S, Nicholas DJD (1983) Proton electrochemical gradients in washed cells of Nitrosomonas europaea and Nicrobacter agilis. J Bacteriol 154: 65–71
Lolkema JS, Hellingwerf KJ, Konings WN (1982) The effect of “probe binding” on the quantitative determination of the proton motive force in bacteria. Biochem Biophys Acta 681: 85–94
Lowry OH, Rosenbrough NJ, Farr AL, Randal RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265–275
Lundin A, Thore A (1975) Analytical information obtainable by evaluation of the time course of firefly bioluminiscence in the assay of ATP. Anal Biochem 66: 47–63
Martikainen PJ, Nurmiaho-Lassila EL (1985) Nitrosopira, an important ammonium-oxidizing bacterium in fertilized coniferous forest soil. Can J Microbiol 31: 190–197
Miller DJ, Wood PM, (1983) The soluble cytochrome oxidase of Nitrosomonas europaea. J Gen Microbiol 129: 1645–1650
Shinbo T, Kama N, Kurihara K, Kobataka Y (1978) A PVC-based electrode sensitive to DDA+ as a device to monitor the membrane potential in biological systems. Arch Biochem Biophys 187: 414–422
Stams AJM, Flameling EM, Marnette ECL (1990) The importance of autotrophic versus heterotrophic nitrification of atmospheric ammonium in forest ecosystems with acid soil. FEMS Microbiol Ecol 74: 337–344
Suzuki L, Dular U, Kwok SC (1974) Ammonia or ammonium ion as substrate for oxidation by Nitrosomonas europaea cells and extracts. J Bacteriol 120: 556–558
Walker N, Wickramasinghe KN (1979) Nitrification and autotrophic nitrifying bacteria in acid tea soils. Soil Biol Biochem 11: 231–236
Wood PM (1986) Nitrification as a bacterial energy source. In: Prosser JI (ed), Nitrification Special publication 20. IRL Press, Oxford, pp 39–62
Wood PM (1988) Monooxygenase and free radical mechanisms for biological ammonia oxidation. Symp. 42, Soc. Gen. Microbiol., Cambridge University Press, Cambridge, pp 219–243
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Frijlink, M.J., Abee, T., Laanbroek, H.J. et al. The bioenergetics of ammonia and hydroxylamine oxidation in Nitrosomonas europaea at acid and alkaline pH. Arch. Microbiol. 157, 194–199 (1992). https://doi.org/10.1007/BF00245290
Published:
Issue Date:
DOI: https://doi.org/10.1007/BF00245290