1887

Abstract

Starved cells of and further ammonia oxidizers were able to rapidly accumulate ammonium and hydroxylamine to an internal concentration of about 1 and 0·8 M, respectively. In kinetic studies, the uptake/accumulation rates for ammonium [3·1 mmol (g protein) min] and hydroxylamine [4·39 mmol (g protein) min] were determined. The uptake and accumulation process of ammonium and hydroxylamine was not coupled to ammonia or hydroxylamine oxidation and nitrite was not produced. In the presence of uncouplers the ammonium accumulation was completely inhibited, indicating an active, membrane-potential-driven transport mechanism. When the external ammonium or hydroxylamine pool was depleted, the internal ammonium and hydroxylamine was consumed within 12 h or 20 min, respectively. The binding of ammonium/ammonia was correlated with an energized membrane system, and hydroxylamine may bind to the hydroxylamine oxidoredutase.

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2004-05-01
2020-08-07
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References

  1. Abeliovich A., Vonshak A.. 1992; Anaerobic metabolism of Nitrosomonas europaea. Arch Microbiol158:267–270[CrossRef]
    [Google Scholar]
  2. Anderson K. K., Hooper A. B.. 1983; O2 and H2O are each the source of one Oin [inline-graphic] produced from NH3 by Nitrosomonas; 15N-NMR evidence. FEBS Lett164:236–240 [/inline-graphic][CrossRef]
    [Google Scholar]
  3. Arciero D. M., Hooper A. B.. 1993; Hydroxylamine oxidoreductase from Nitrosomonas europaea is a multimer of an octa-heme subunit. J Biol Chem268:14645–14654
    [Google Scholar]
  4. Bergmann D. J., Arciero D. A., Hooper A. B.. 1994; Organization of the hao gene cluster of Nitrosomonas europaea: genes for two tetraheme c cytochromes. J Bacteriol176:3148–3153
    [Google Scholar]
  5. Bock E., Schmidt I., Stüven R., Zart D.. 1995; Nitrogen loss caused by denitrifying Nitrosomonas cells using ammonium or hydrogen as electron donors and nitrite as electron acceptor. Arch Microbiol163:16–20[CrossRef]
    [Google Scholar]
  6. Bodelier P. L., Frenzel P.. 1999; Contribution of methanotrophic and nitrifying bacteria to CH4 and [inline-graphic] oxidation in the rhizosphere of rice plants as determined by new methods of discrimination. Appl Environ Microbiol65:1826–1833 [/inline-graphic]
    [Google Scholar]
  7. Bollmann A., Bar-Gilissen M. J., Laanbroek H. J.. 2002; Growth at low ammonium concentrations and starvation response as potential factors involved in niche differentiation among ammonia-oxidizing bacteria. Appl Environ Microbiol68:4751–4757[CrossRef]
    [Google Scholar]
  8. Bradford M.. 1976; Rapid and sensitive methods for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal Biochem72:248–254[CrossRef]
    [Google Scholar]
  9. Chain P., Lamerdin J., Larimer F..12 other authors 2003; Complete genome sequence of the ammonia-oxidizing bacterium and obligate chemolithoautotroph Nitrosomonas europaea. J Bacteriol185:2759–2773[CrossRef]
    [Google Scholar]
  10. Drozd J. W.. 1976; Energy coupling and respiration in Nitrosomonas europaea. Arch Microbiol110:257–262[CrossRef]
    [Google Scholar]
  11. Dua R. D., Bhandari B., Nicholas D. J. D.. 1979; Stable isotope studies on the oxidation of ammonia to hydroxylamine by Nitrosomonas europaea. FEBS Lett106:401–404[CrossRef]
    [Google Scholar]
  12. Hollocher T. C., Kumar S., Nicholas D. J. D.. 1982; Respiration-dependent proton translocation in Nitrosomonas europaea and its apparent absence in Nitrobacter agilis during inorganic oxidations. J Bacteriol149:1013–1020
    [Google Scholar]
  13. Hooper A. B.. 1969a; Biochemical basis of obligate autotrophy in Nitrosomonas europaea. J Bacteriol97:776–779
    [Google Scholar]
  14. Hooper A. B.. 1969b; Lag phase of ammonia oxidation by resting cells of Nitrosomonas europaea. J Bacteriol97:968–969
    [Google Scholar]
  15. Hooper A. B., DiSpirito A. A.. 1985; In bacteria which grow on simple reductants generation of a proton gradient involves extracytoplasmic oxidation of substrate. Microbiol Rev49:140–157
    [Google Scholar]
  16. Hyman M. R., Arp D. J.. 1993; An electrophoretic study of the thermal-dependent and reductant-dependent aggregation of the 28 kDa component of ammonia monooxygenase from Nitrosomonas europaea. Electrophoresis14:619–627[CrossRef]
    [Google Scholar]
  17. Hyman M. R., Wood P. M.. 1985; Suicidal inactivation and labeling of ammonia monooxygenase by acetylene. Biochem J227:719–725
    [Google Scholar]
  18. Igarashi N., Moriyama H., Fujiwara T., Fukumori Y., Tanaka N.. 1997; The 2·8 Å structure of hydroxylamine oxidoreductase from nitrifying chemoautotrophic bacterium Nitrosomonas europaea. Nat Struct Biol4:276–284[CrossRef]
    [Google Scholar]
  19. Kleiner D.. 1981; The transport of NH3 and [inline-graphic] across biological membranes. Biochim Biophys Acta639:41–52 [/inline-graphic][CrossRef]
    [Google Scholar]
  20. Kleiner D.. 1985; Bacterial ammonia transport. FEMS Microbiol Rev32:87–100[CrossRef]
    [Google Scholar]
  21. Krämer R., Lambert C.. 1990; Uptake of glutamate in Corynebacterium glutamicum. 2. Evidence for a primary active transport system. Eur J Biochem194:937–944[CrossRef]
    [Google Scholar]
  22. Kumar S., Nicholas D. J. D.. 1983; Proton electrochemical gradients in washed cells of Nitrosomonas europaea and Nitrobacter agilis. J Bacteriol154:65–71
    [Google Scholar]
  23. Laanbroek H. J., Gerards S.. 1993; Competition for limiting amounts of oxygen between Nitrosomonas europaea and Nitrobacter winogradskyi grown in continuous mixed cultures. Arch Microbiol159:453–459[CrossRef]
    [Google Scholar]
  24. Masson P., Arciero D. M., Hooper A. B., Balny C.. 1990; Electrophoresis at elevated hydrostatic pressure of the multiheme hydroxylamine oxidoreductase. Electrophoresis11:128–133[CrossRef]
    [Google Scholar]
  25. Meier-Wagner J., Nolden L., Jakoby M., Siewe R., Krämer R., Burkovski A.. 2001; Multiplicity of ammonium uptake systems in Corynebacterium glutamicum: role of Amt and AmtB. Microbiology147:135–143
    [Google Scholar]
  26. Nejidat A., Shmuely H., Abeliovich A.. 1997; Effect of ammonia starvation on hydroxylamine oxidoreductase activity of Nitrosomonas europaea. J Biochem121:957–960[CrossRef]
    [Google Scholar]
  27. Painter H. A.. 1988; Nitrification in the treatment of sewage and waste-waters. In Nitrification pp.185–211Edited by Prosser J. I.. Oxford: IRL Press;
    [Google Scholar]
  28. Prosser J. I.. 1989; Autotrophic nitrification in bacteria. Adv Microb Physiol30:125–181
    [Google Scholar]
  29. Rees M., Nason A.. 1966; Incorporation of atmospheric oxygen into nitrite formed during ammonia oxidation by Nitrosomonas europaea. Biochim Biophys Acta113:398–401[CrossRef]
    [Google Scholar]
  30. Risgaard-Petersen N., Rysgaard S., Revsbech N. P.. 1995; A combined microdiffusion–hypobromite oxidation method for determination of 15N isotope in [inline-graphic]. Soil Sci Soc Am J59:1077–1080 [/inline-graphic][CrossRef]
    [Google Scholar]
  31. Sayavedra-Soto L. A., Hommes N. G., Arp D. J.. 1994; Characterization of the gene encoding hydroxylamine oxidoreductase in Nitrosomonas europaea. J Bacteriol176:504–510
    [Google Scholar]
  32. Schalk J., Devries S., Kuenen J. G., Jetten M. S. M.. 2000; A novel hydroxylamine oxidoreductase involved in the Anammox process. Biochemistry39:5405–5412[CrossRef]
    [Google Scholar]
  33. Schmidt I., Bock E.. 1997; Anaerobic ammonia oxidation with nitrogen dioxide by Nitrosomonas eutropha. Arch Microbiol167:106–111[CrossRef]
    [Google Scholar]
  34. Schmidt I., Bock E.. 1998; Anaerobic ammonia oxidation by cell-free extracts of Nitrosomonas eutropha. Antonie van Leeuwenhoek73:271–278[CrossRef]
    [Google Scholar]
  35. Schmidt I., Zart D., Bock E.. 2001a; Gaseous NO2 as a regulator for ammonia oxidation ofNitrosomonas eutropha. Antonie van Leeuwenhoek79:311–318[CrossRef]
    [Google Scholar]
  36. Schmidt I., Zart D., Bock E.. 2001b; Effects of gaseous NO2 on cells of Nitrosomonas eutropha previously incapable of using ammonia as an energy source. Antonie van Leeuwenhoek79:39–47[CrossRef]
    [Google Scholar]
  37. Schmidt I., Bock E., Jetten M. S. M.. 2001c; Ammonia oxidation by Nitrosomonas eutropha with NO2 as oxidant is not inhibited by acetylene. Microbiology147:2247–2253
    [Google Scholar]
  38. Schmidt I., Sliekers O., Schmid M., Cirpus I., Strous M., Bock E., Kuenen J. G., Jetten M. S. M.. 2002; Aerobic and anaerobic ammonia oxidizing bacteria – competitors or natural partners?. FEMS Microbiol Ecol39:175–181
    [Google Scholar]
  39. Strehler B. L. J., Trotter J. B.. 1952; Firefly luminescence in the study of energy transfer mechanism. I. Substrate and enzyme determination. Arch Biochim Biophys40:28–41[CrossRef]
    [Google Scholar]
  40. Suzuki I., Dular U., Kwok S.-C.. 1974; Ammonia or ammonium ion as substrate for oxidation by Nitrosomonas europaea cells and extracts. J Bacteriol120:556–558
    [Google Scholar]
  41. Van de Graaf A. A., de Bruijn P., Robertson L. A., Kuenen J. G.. 1996; Autotrophic growth of anaerobic ammonium-oxidizing micro-organisms in a fluidized bed reactor. Microbiology142:2187–2196[CrossRef]
    [Google Scholar]
  42. Verstraete W., Alexander M.. 1972; Heterotrophic nitrification by Arthrobacter sp. J Bacteriol110:955–961
    [Google Scholar]
  43. Watson S. W., Bock E., Harms H., Koops H.-P., Hooper A. B.. 1989; Genera of ammonia-oxidizing bacteria. In Bergey's Manual of Systematic Bacteriology pp.1822–1834Edited by Staley J. T.. Bryant M. P., Pfennig N., Holt J. G.. Baltimore: Williams & Wilkins;
    [Google Scholar]
  44. Wiesmann U.. 1994; Biological nitrogen removal from wastewater. Adv Biochem Eng Biotechnol51:113–154
    [Google Scholar]
  45. Wood P. M.. 1986; Nitrification as a bacterial energy source. In Nitrification pp.39–62Edited by Prosser J. I.. Oxford: IRL Press;
    [Google Scholar]
  46. Zart D., Schmidt I., Bock E.. 2000; Significance of gaseous NO for ammonia oxidation by Nitrosomonas eutropha. Antonie van Leeuwenhoek77:49–55[CrossRef]
    [Google Scholar]
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