Response of anaerobic ammonium-oxidizing bacteria to hydroxylamine

Applied and Environmental Microbiology

Volumn 74, Issue 14, 2008, Pages 4417-4426

  Van Der Star, Wouter R L ^a,c   Van De Graaf, Maarten J ^a   Kartal, Boran ^b   Picioreanu, Cristian ^a   Jetten, Mike S M ^a,b   Van Loosdrecht, Mark C M ^a  

^a DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^b RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^c DELTARES   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; BACTERIOLOGY; BIOCHEMISTRY; HYDRAZINE; NITRIC OXIDE; NITROGEN; NITROGEN REMOVAL; NONMETALS;

ANAEROBIC (UASB); ANAEROBIC AMMONIUM OXIDATION (ANAMMOX); ANAMMOX; DINITROGEN GAS; HYDROXYLAMINE (HA); MATHEMATICAL MODELLING; MECHANISTIC MODELING; METABOLIC PATHWAYS; NITROGEN CYCLING; OXIDIZING BACTERIA;

AMMONIUM COMPOUNDS;

AMMONIA; HYDRAZINE; HYDROXYLAMINE; NITRIC OXIDE; NITRITE;

AMMONIUM; BACTERIUM; CHEMICAL COMPOUND; ELECTRON; EXPERIMENTAL STUDY; METABOLISM; MICROBIAL COMMUNITY; NITRITE; NITROGEN CYCLE; NUMERICAL MODEL; OXIDATION; REDUCTION;

ANAEROBIC BACTERIUM; ARTICLE; BACTERIAL METABOLISM; MATHEMATICAL MODEL; NONHUMAN; OXIDATION;

BACTERIA, ANAEROBIC; BIOMASS; HYDRAZINES; HYDROXYLAMINE; KINETICS; MODELS, CHEMICAL; NITRIC OXIDE; NITROGEN; NITROUS OXIDE; OXIDATION-REDUCTION; QUATERNARY AMMONIUM COMPOUNDS; THERMODYNAMICS; TIME FACTORS;

EID: 47749095642     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.00042-08     Document Type: Article

References (40)

1. Bamford, V. A., H. C. Angove, H. E. Seward, A. J. Thomson, J. A. Cole, J. N. Butt, A. M. Hemmings, and D. J. Richardson. 2002. Structure and spectroscopy of the periplasmic cytochrome c nitrite reductase from Escherichia coli. Biochemistry 41:2921-2931.
2. Cabello, P., C. Pino, M. F. Olmo-Mira, F. Castillo, M. D. Roldan, and C. Moreno-Vivian. 2004. Hydroxylamine assimilation by Rhodobacter capsulatus E1F1. Requirement of the hep gene (hybrid cluster protein) located in the nitrate assimilation nas gene region for hydroxylamine reduction. J. Biol. Chem. 279:45485-45494.
3. Cirpus, I. E. Y., M. De Been, H. J. M. Op den Camp, M. Strous, D. Le Paslier, G. J. Kuenen, and M. S. M. Jetten. 2005. A new soluble 10 kDa monoheme cytochrome c-552 from the anammox bacterium Candidatus "Kuenenia stuttgartiensis." FEMS Microbiol. Lett. 252:273-278.
4. 2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica. Nature (London) 422:606-608.
5. Egli, K., U. Fanger, P. J. J. Alvarez, H. Siegrist, J. R. Van der Meer, and A. J. B. Zehnder. 2001. Enrichment and characterization of an anammox bacterium from a rotating biological contactor treating ammonium-rich leachate. Arch. Microbiol. 175:198-207.
6. Frear, D. S., and R. C. Burrell. 1955. Spectrophotometric method for determining hydroxylamine reductase activity in higher plants. Anal. Chem. 27:1664-1665.
7. Huston, W. M., H. R. Harhangi, A. P. Leech, C. S. Butler, M. S. M. Jetten, H. J. M. Op den Camp, and J. W. B. Moir. 2007. Expression and characterisation of a major c-type cytochrome encoded by gene kustc0563 from Kuenenia stuttgartiensis as a recombinant protein in Escherichia coli. Protein Expr. Purif. 51:28-33.
8. Jardin, N., A. Hippen, C. F. Seyfried, K.-H. Rosenwinkel, and F. Greulich. 2001. Deammonification of sludge liquor at wastewater treatment plant Hattingen with moving bed system. GWF, Wasser/Abwasser 142:479-484.
9. Jetten, M., M. Schmid, K. Van de Pas-Schoonen, J. Sinninghe Damsté, and M. Strous. 2005. Anammox organisms: enrichment, cultivation, and environmental analysis. Methods Enzymol. 397:34-57.
10. Kartal, B., M. M. M. Kuypers, G. Lavik, J. Schalk, H. J. M. Op den Camp, M. S. M. Jetten, and M. Strous. 2007. Anammox bacteria disguised as denitrifiers: nitrate reduction to dinitrogen gas via nitrite and ammonium. Environ. Microbiol. 9:635-642.
11. Kartal, B., J. Rattray, L. Van Niftrik, J. L. Van de Vossenberg, M. C. Schmid, J. A. Fuerst, J. Sinninghe Damsté, M. S. M. Jetten, and M. Strous. 2007. Candidatus "Anammoxoglobus propionicus" gen. nov., sp. nov., a new propionate oxidizing species of anaerobic ammonium oxidizing bacteria. Syst. Appl. Microbiol. 30:39-49.
12. Kartal, B., L. van Niftrik, J. Rattray, J. L. C. M. van de Vossenberg, M. C. Schmid, J. Sinninghe Damsté, M. S. M. Jetten, and M. Strous. 2008. Candidatus 'Brocadia fulgida': an autofluorescent anaerobic ammonium oxidizing bacterium. FEMS Microbiol. Ecol. 63:46-55.
13. Kartal, B., L. A. Van Niftrik, A. O. Sliekers, M. Schmid, I. Schmidt, K. Van de Pas-Schoonen, I. Cirpus, W. R. L. Van der Star, M. C. M. Van Loosdrecht, W. Abma, J. G. Kuenen, J. W. Mulder, M. S. M. Jetten, H. Op den Camp, M. Strous, and J. Van de Vossenberg. 2004. Application, eco-physiology and biodiversity of anaerobic ammonium-oxidizing bacteria. Rev. Environ. Sci. Bio/Technol. 3:255-264.
14. Kuypers, M. M. M., G. Lavik, D. Woebken, M. Schmid, B. M. Fuchs, R. Amann, B. B. Jorgensen, and M. S. M. Jetten. 2005. Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc. Natl. Acad. Sci. USA 102:6478-6483.
15. Kuypers, M. M. M., A. O. Sliekers, G. Lavik, M. Schmid, B. B. Jorgensen, J. G. Kuenen, J. S. Sinninghe Damsté, M. Strous, and M. S. M. Jetten. 2003. Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature (London) 422:608-611.
16. Latimer, W. 1952. The oxidation states of the elements and their potentials in aqueous solutions, 2nd ed. Prentice Hall, New York, NY.
17. Lide, D. R. (ed.) 2006. CRC handbook of chemistry and physics, 87th ed., p. 5.85-5.88. CRC Press, Boca Raton, FL.
18. Pynaert, K., B. F. Smets, S. Wyffels, D. Beheydt, S. D. Siciliano, and W. Verstraete. 2003. Characterization of an autotrophic nitrogen-removing biofilm from a highly loaded lab-scale rotating biological contactor. Appl. Environ. Microbiol. 69:3626-3635.
19. Rysgaard, S., R. N. Glud, N. Risgaard-Petersen, and T. Dalsgaard. 2004. Denitrification and anammox activity in Arctic marine sediments. Limnol. Oceanogr. 49:1493-1502.
20. Schalk, J., S. De Vries, J. G. Kuenen, and M. S. M. Jetten. 2000. Involvement of a novel hydroxylamine oxidoreductase in anaerobic ammonium oxidation. Biochemistry 39:5405-5412.
21. Schalk, J., H. Oustad, J. G. Kuenen, and M. S. M. Jetten. 1998. The anaerobic oxidation of hydrazine: a novel reaction in microbial nitrogen metabolism. FEMS Microbiol. Lett. 158:61-67.
22. Schmid, M., K. Walsh, R. Webb, W. Irene, C. Rijpstra, K. van de Pas-Schoonen, M. J. Verbruggen, T. Hill, B. Moffett, J. Fuerst, S. Schouten, J. S. Sinninghe Damsté, J. Harris, P. Shaw, M. Jetten, and M. Strous. 2003. Candidatus "Scalindua brodae," sp. nov., Candidatus "Scalindua wagneri," sp. nov., two new species of anaerobic ammonium oxidizing bacteria. Syst. Appl. Microbiol. 26:529-538.
23. Schmid, M. C., N. Risgaard-Petersen, J. van de Vossenberg, M. M. M. Kuypers, G. Lavik, J. Petersen, S. Hulth, B. Thamdrup, D. Canfield, T. Dalsgaard, S. Rysgaard, M. K. Sejr, M. Strous, H. J. M. Op den Camp, and M. S. M. Jetten. 2007. Anaerobic ammonium-oxidizing bacteria in marine environments: widespread occurrence but low diversity. Environ. Microbiol. 9:1476-1484.
24. x) by two different lithotrophs. Appl. Environ. Microbiol. 68:5351-5357.
25. Schubert, C. J., E. Durisch-Kaiser, B. Wehrli, B. Thamdrup, P. Lam, and M. M. M. Kuypers. 2006. Anaerobic ammonium oxidation in a tropical freshwater system (Lake Tanganyika). Environ. Microbiol. 8:1857-1863.
26. Shimamura, M., T. Nishiyama, H. Shigetomo, T. Toyomoto, Y. Kawahara, K. Furukawa, and T. Fujii. 2007. Isolation of a multiheme protein with features of a hydrazine-oxidizing enzyme from an anaerobic ammonium-oxidizing enrichment culture. Appl. Environ. Microbiol. 73:1065-1072.
27. Singh, J. 1974. Cytochrome oxidase from Pseudomonas aeruginosa. III. Reduction of hydroxylamine. Biochim. Biophys. Acta 333:28-36.
28. Sliekers, A. O., N. Derwort, J. L. C. Gomez, M. Strous, J. G. Kuenen, and M. S. M. Jetten. 2002. Completely autotrophic nitrogen removal over nitrite in one single reactor. Water Res. 36:2475-2482.
29. Strous, M., J. J. Heijnen, J. G. Kuenen, and M. S. M. Jetten. 1998. The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Appl. Microbiol. Biotechnol. 50:589-596.
30. Strous, M., J. G. Kuenen, and M. S. M. Jetten. 1999. Key physiology of anaerobic ammonium oxidation. Appl. Environ. Microbiol. 65:3248-3250.
31. Strous, M., E. Pelletier, S. Mangenot, T. Rattei, A. Lehner, M. W. Taylor, M. Horn, H. Daims, D. Bartol-Mavel, P. Wincker, V. Barbe, N. Fonknechten, D. Vallenet, B. Segurens, C. Schenowitz-Truong, C. Medigue, A. Collingro, B. Snel, B. E. Dutilh, H. J. M. Op den Camp, C. Van der Drift, I. Cirpus, K. T. Van de Pas-Schoonen, H. R. Harhangi, L. Van Niftrik, M. Schmid, J. Keltjens, J. Van de Vossenberg, B. Kartal, H. Meier, D. Frishman, M. A. Huynen, H.-W. Mewes, J. Weissenbach, M. S. M. Jetten, M. Wagner, and D. Le Paslier. 2006. Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature (London) 440:790-794.
32. Strous, M., E. Van Gerven, P. Zheng, J. G. Kuenen, and M. S. M. Jetten. 1997. Ammonium removal from concentrated waste streams with the anaerobic ammonium oxidation (anammox) process in different reactor configurations. Water Res. 31:1955-1962.
33. Van de Graaf, A. A., P. De Bruijn, L. A. Robertson, M. S. M. Jetten, and J. G. Kuenen. 1996. Autotrophic growth of anaerobic ammonium-oxidizing microorganisms in a fluidized bed reactor. Microbiology 142:2187-2196.
34. 15N studies in a fluidized bed reactor. Microbiology 143:2415-2421.
35. Van der Star, W. R. L., W. R. Abma, D. Blommers, J. W. Mulder, T. Tokutomi, M. Strous, C. Picioreanu, and M. C. M. Van Loosdrecht. 2007. Startup of reactors for anoxic ammonium oxidation: experiences from the first full-scale anammox reactor in Rotterdam. Water Res. 41:4149-4163.
36. Van Dongen, L. G. J. M., M. S. M. Jetten, and M. C. M. Van Loosdrecht. 2001. The combined SHARON/anammox process. IWA Publishing, London, United Kingdom.
37. Van Dongen, U., M. S. M. Jetten, and M. C. M. Van Loosdrecht. 2001. The SHARON-Anammox process for treatment of ammonium rich wastewater. Water Sci. Technol. 44(1):153-160.
38. Watt, G. W., and J. D. Chrisp. 1952. A spectrophotometric method for the determination of hydrazine. Anal. Chem. 24:2006-2008.
39. Wett, B. 2006. Solved upscaling problems for implementing deammonification of rejection water. Water Sci. Technol. 53(12):121-128.
40. Zheng, P., X. Feng, M. S. M. Jetten, and J. G. Kuenen. 1997. Study on substrate conversion characteristics of mixed microbial culture for anaerobic ammonium oxidation. Zhejiang Nongye Daxue Xuebao 23:409-413.