1887

Abstract

The ammonia monooxygenase (AMO) of is a metalloenzyme that catalyses the oxidation of ammonia to hydroxylamine. We have identified histidine 191 of AmoA as the binding site for the oxidized mechanism-based inactivator acetylene. Binding of acetylene changed the molecular mass of His-191 from 155.15 to 197.2 Da (+42.05), providing evidence that acetylene was oxidized to ketene (CHCO; 42.04 Da) which binds specifically to His-191. It must be assumed that His-191 is part of the acetylene-activating site in AMO or at least directly neighbours this site.

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2009-01-01
2020-08-14
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References

  1. Anderson K. K., Hooper A. B.. 1983; O2 and H2O are each the source of one O in produced from NH3 by Nitrosomonas; 15N-NMR evidence. FEBS Lett164:236–240
    [Google Scholar]
  2. Bedard C., Knowles R.. 1989; Physiology, biochemistry, and specific inhibitors of CH4, , and CO oxidation by methanotrophs and nitrifiers. Microbiol Rev53:68–84
    [Google Scholar]
  3. Bonner W. M., Laskey R. A.. 1974; A film detection method for tritium-labelled proteins and nucleic acids in polyacrylamide gels. Eur J Biochem46:83–88
    [Google Scholar]
  4. Chain P., Lamerdin J., Larimer F., Regala W., Lao V., Land M., Hauser L., Hooper A., Klotz M.. other authors 2003; Complete genome sequence of the ammonia-oxidizing bacterium and obligate chemolithoautotroph Nitrosomonas europaea. J Bacteriol185:2759–2773
    [Google Scholar]
  5. Chan S. I., Yu S. S.. 2008; Controlled oxidation of hydrocarbons by the membrane-bound methane monooxygenase: the case for a tricopper cluster. Acc Chem Res41:969–979
    [Google Scholar]
  6. Chan S. I., Chen K. H.-C., Yu S. S.-F., Chen C.-L., Kuo S. S.-J.. 2004; Toward delineating the structure and function of the particulate methane monooxygenase from methanotrophic bacteria. Biochemistry43:4421–4430
    [Google Scholar]
  7. Chen P. P., Chan S. I.. 2006; Theoretical modeling of the hydroxylation of methane as mediated by the particulate methane monooxygenase. J Inorg Biochem100:801–809
    [Google Scholar]
  8. Chen P. P., Yang R. B., Lee J. C., Chan S. I.. 2007; Facile O-atom insertion into C–C and C–H bonds by a trinuclear copper complex designed to harness a singlet oxene. Proc Natl Acad Sci U S A104:14570–14575
    [Google Scholar]
  9. Covey T. R., Bronner R. F., Shushan B. I., Henion J.. 1988; The determination of proteins, oligonucleotide and peptide molecular weights by ionspray mass spectrometry. Rapid Commun Mass Spectrom2:249–256
    [Google Scholar]
  10. Dalton H., Wilkins P. C., Jiang Y.. 1993; Mechanistic pathways in soluble methane mono-oxygenase. Biochem Soc Trans21:749–752
    [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
    [Google Scholar]
  12. Eckerskorn C., Strupat K., Kellermann J., Lottspeich F., Hillenkamp F.. 1997; High-sensitivity peptide mapping by micro-LC with on-line membrane blotting and subsequent detection by scanning-IR-MALDI mass spectrometry. J Protein Chem16:349–362
    [Google Scholar]
  13. Ensign S. A., Hyman M. R., Arp D. J.. 1993; In vitro activation of ammonia monooxygenase from Nitrosomonas europaea by copper. J Bacteriol175:1971–1980
    [Google Scholar]
  14. Fomina L., Vazquez B., Tkatchouk E., Fomine S.. 2002; The Glaser reaction mechanism. A DFT study. Tetrahedron58:6741–6747
    [Google Scholar]
  15. Hooper A. B., Terry K. R.. 1973; Specific inhibitor of ammonia oxidation in Nitrosomonas. J Bacteriol115:480–485
    [Google Scholar]
  16. Hooper A. B., Vannelli T., Bergmann D. J., Arciero D. M.. 1997; Enzymology of the oxidation of ammonia to nitrite by bacteria. Antonie Van Leeuwenhoek71:59–67
    [Google Scholar]
  17. Hyman M. R., Arp D. J.. 1990; The small-scale production of [U-14C]acetylene from Ba14CO3: application to labeling of ammonia monooxygenase in autotrophic nitrifying bacteria. Anal Biochem190:348–353
    [Google Scholar]
  18. Hyman M. R., Arp D. J.. 1992; 14C2H2- and 14CO2-labeling studies of the de novo synthesis of polypeptides by Nitrosomonas europaea during recovery from acetylene and light inactivation of ammonia monooxygenase. J Biol Chem267:1534–1545
    [Google Scholar]
  19. 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
    [Google Scholar]
  20. Hyman M. R., Wood P. M.. 1985; Suicidal inactivation and labelling of ammonia monooxygenase by acetylene. Biochem J227:719–725
    [Google Scholar]
  21. Hynes R. K., Knowles R.. 1978; Inhibition by acetylene of ammonia oxidation in Nitrosomonas europaea. FEMS Microbiol Lett4:319–321
    [Google Scholar]
  22. Laemmli U. K.. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature227:680–685
    [Google Scholar]
  23. Lieberman R. L., Rosenzweig A. C.. 2005a; Crystal structure of a membrane-bound metalloenzyme that catalyses the biological oxidation of methane. Nature434:177–182
    [Google Scholar]
  24. Lieberman R. L., Rosenzweig A. C.. 2005b; The quest for the particulate methane monooxygenase active site. Dalton Trans3390–3396
    [Google Scholar]
  25. Lieberman R. L., Kondapalli K. C., Shrestha D. B., Hakemian A. S., Smith S. M., Telser J., Kuzelka J., Gupta R., Borovik A. S.. other authors 2006; Characterization of the particulate methane monooxygenase metal centers in multiple redox states by X-ray absorption spectroscopy. Inorg Chem45:8372–8378
    [Google Scholar]
  26. Lipscomb J. D.. 1994; Biochemistry of the soluble methane monooxygenase. Annu Rev Microbiol48:371–399
    [Google Scholar]
  27. Martinho M., Choi D. W., Dispirito A. A., Antholine W. E., Semrau J. D., Münck E.. 2007; Mössbauer studies of the membrane-associated methane monooxygenase from Methylococcus capsulatus Bath: evidence for a diiron center. J Am Chem Soc129:15783–15785
    [Google Scholar]
  28. McTavish H., Fuchs J. A., Hooper A. B.. 1993; Sequence of the gene coding for ammonia monooxygenase in Nitrosomonas europaea. J Bacteriol175:2436–2444
    [Google Scholar]
  29. Nesheim J. C., Lipscomb J. D.. 1996; Large kinetic isotope effects in methane oxidation catalyzed by methane monooxygenase: evidence for C–H bond cleavage in a reaction cycle intermediate. Biochemistry35:10240–10247
    [Google Scholar]
  30. Prior S. D., Dalton H.. 1985a; Acetylene as a suicide substrate and active site probe for methane monooxygenase from Methylococcus capsulatus (Bath): inhibitor of methane-oxidising activity. FEMS Microbiol Lett29:105–109
    [Google Scholar]
  31. Prior S. D., Dalton H.. 1985b; The effect of copper ions on membrane content and methane monooxygenase activity in methanol-grown cells of Methylococcus capsulatus (Bath. J Gen Microbiol131:155–163
    [Google Scholar]
  32. Rees M., Nason A.. 1966; Incorporation of atmospheric oxygen into nitrite formed during ammonia oxidation by Nitrosomonas europaea. Biochim Biophys Acta113:398–401
    [Google Scholar]
  33. Schägger H., von Jagow G.. 1987; Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem166:368–379
    [Google Scholar]
  34. Schmidt I., Bock E.. 1997; Anaerobic ammonia oxidation with nitrogen dioxide by Nitrosomonas eutropha. Arch Microbiol167:106–111
    [Google Scholar]
  35. Schmidt I., Bock E., Jetten M. S. M.. 2001; Ammonia oxidation by Nitrosomonas eutropha with NO2 as oxidant is not inhibited by acetylene. Microbiology147:2247–2253
    [Google Scholar]
  36. Schmidt I., Steenbakkers P. J. M., op den Camp H. J. M., Schmidt K., Jetten M. S. M.. 2004; Physiologic and proteomic evidence for a role of nitric oxide in biofilm formation by Nitrosomonas europaea and other ammonia oxidizers. J Bacteriol186:2781–2788
    [Google Scholar]
  37. Shears J. H., Wood P. M.. 1985; Spectroscopic evidence for a photosensitive oxygenated state of ammonia monoxygenase. Biochem J226:499–507
    [Google Scholar]
  38. Smith B. J.. 1994; Chemical cleavage of proteins. In Basic Protein and Peptide Protocols. Methods in Molecular Biology vol. 32 pp297–309 Edited by Walker J. M. Totowa, NJ: Humana Press;
    [Google Scholar]
  39. Stirling D. I., Dalton H.. 1977; Effect of metal-binding agents and other compounds on methane oxidation by two strains of Methylococcus capsulatus. Arch Microbiol114:71–76
    [Google Scholar]
  40. Yeager C. M., Bottomley P. J., Arp D. J., Hyman M. R.. 1999; Inactivation of toluene 2-monooxygenase in Burkholderia cepacia G4 by alkynes. Appl Environ Microbiol65:632–639
    [Google Scholar]
  41. Zahn J. A., DiSpirito A. A.. 1996; Membrane-associated methane monooxygenase from Methylococcus capsulatus (Bath. J Bacteriol178:1018–1029
    [Google Scholar]
  42. Zahn J. A., Arciero D. M., Hooper A. B., DiSpirito A. A.. 1996; Evidence for an iron center in the ammonia monooxygenase from Nitrosomonas europaea. FEBS Lett397:35–38
    [Google Scholar]
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