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.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.26719-0
2004-05-01
2024-12-13
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/5/mic1501405.html?itemId=/content/journal/micro/10.1099/mic.0.26719-0&mimeType=html&fmt=ahah

References

  1. Abeliovich A., Vonshak A. 1992; Anaerobic metabolism of Nitrosomonas europaea. Arch Microbiol 158:267–270 [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 Lett 164:236–240 [/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 Chem 268:14645–14654
    [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 Bacteriol 176:3148–3153
    [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 Microbiol 163:16–20 [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 Microbiol 65:1826–1833 [/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 Microbiol 68:4751–4757 [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 Biochem 72:248–254 [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 Bacteriol 185:2759–2773 [CrossRef]
    [Google Scholar]
  10. Drozd J. W. 1976; Energy coupling and respiration in Nitrosomonas europaea. Arch Microbiol 110:257–262 [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 Lett 106:401–404 [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 Bacteriol 149:1013–1020
    [Google Scholar]
  13. Hooper A. B. 1969a; Biochemical basis of obligate autotrophy in Nitrosomonas europaea. J Bacteriol 97:776–779
    [Google Scholar]
  14. Hooper A. B. 1969b; Lag phase of ammonia oxidation by resting cells of Nitrosomonas europaea. J Bacteriol 97:968–969
    [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 Rev 49:140–157
    [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. Electrophoresis 14:619–627 [CrossRef]
    [Google Scholar]
  17. Hyman M. R., Wood P. M. 1985; Suicidal inactivation and labeling of ammonia monooxygenase by acetylene. Biochem J 227:719–725
    [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 Biol 4:276–284 [CrossRef]
    [Google Scholar]
  19. Kleiner D. 1981; The transport of NH3 and [inline-graphic] across biological membranes. Biochim Biophys Acta 639:41–52 [/inline-graphic] [CrossRef]
    [Google Scholar]
  20. Kleiner D. 1985; Bacterial ammonia transport. FEMS Microbiol Rev 32:87–100 [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 Biochem 194:937–944 [CrossRef]
    [Google Scholar]
  22. Kumar S., Nicholas D. J. D. 1983; Proton electrochemical gradients in washed cells of Nitrosomonas europaea and Nitrobacter agilis. J Bacteriol 154:65–71
    [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 Microbiol 159:453–459 [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. Electrophoresis 11:128–133 [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. Microbiology 147:135–143
    [Google Scholar]
  26. Nejidat A., Shmuely H., Abeliovich A. 1997; Effect of ammonia starvation on hydroxylamine oxidoreductase activity of Nitrosomonas europaea. J Biochem 121:957–960 [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 Physiol 30:125–181
    [Google Scholar]
  29. Rees M., Nason A. 1966; Incorporation of atmospheric oxygen into nitrite formed during ammonia oxidation by Nitrosomonas europaea. Biochim Biophys Acta 113:398–401 [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 J 59:1077–1080 [/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 Bacteriol 176:504–510
    [Google Scholar]
  32. Schalk J., Devries S., Kuenen J. G., Jetten M. S. M. 2000; A novel hydroxylamine oxidoreductase involved in the Anammox process. Biochemistry 39:5405–5412 [CrossRef]
    [Google Scholar]
  33. Schmidt I., Bock E. 1997; Anaerobic ammonia oxidation with nitrogen dioxide by Nitrosomonas eutropha. Arch Microbiol 167:106–111 [CrossRef]
    [Google Scholar]
  34. Schmidt I., Bock E. 1998; Anaerobic ammonia oxidation by cell-free extracts of Nitrosomonas eutropha. Antonie van Leeuwenhoek 73:271–278 [CrossRef]
    [Google Scholar]
  35. Schmidt I., Zart D., Bock E. 2001a; Gaseous NO2 as a regulator for ammonia oxidation ofNitrosomonas eutropha. Antonie van Leeuwenhoek 79:311–318 [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 Leeuwenhoek 79:39–47 [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. Microbiology 147:2247–2253
    [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 Ecol 39:175–181
    [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 Biophys 40:28–41 [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 Bacteriol 120:556–558
    [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. Microbiology 142:2187–2196 [CrossRef]
    [Google Scholar]
  42. Verstraete W., Alexander M. 1972; Heterotrophic nitrification by Arthrobacter sp. J Bacteriol 110:955–961
    [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 Biotechnol 51:113–154
    [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 Leeuwenhoek 77:49–55 [CrossRef]
    [Google Scholar]
/content/journal/micro/10.1099/mic.0.26719-0
Loading
/content/journal/micro/10.1099/mic.0.26719-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error