Anammox bacteria disguised as denitrifiers: Nitrate reduction to dinitrogen gas via nitrite and ammonium

Environmental Microbiology

Volumn 9, Issue 3, 2007, Pages 635-642

  Kartal, Boran ^a   Kuypers, Marcel M M ^b   Lavik, Gaute ^b   Schalk, Jos ^c,d   Op Den Camp, Huub J M ^a   Jetten, Mike S M ^a,c   Strous, Marc ^a  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b MAX PLANCK INSTITUTE FOR MARINE MICROBIOLOGY   (Germany)

^c DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

^d UNILEVER RESEARCH VLAARDINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; NITRATE; NITRITE; NITRITE REDUCTASE; NITROGEN; QUATERNARY AMMONIUM DERIVATIVE; SEA WATER;

ANAEROBIC GROWTH; ARTICLE; BACTERIUM; CLASSIFICATION; ENZYMOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION;

ANAEROBIOSIS; BACTERIA; CALCIUM; NITRATES; NITRITE REDUCTASES; NITRITES; NITROGEN; OXIDATION-REDUCTION; QUATERNARY AMMONIUM COMPOUNDS; SEAWATER;

BACTERIA (MICROORGANISMS); CANDIDATUS KUENENIA STUTTGARTIENSIS;

EID: 33846976146     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2006.01183.x     Document Type: Article

References (35)

1. Amann, R.I., Binder, B.J., Olson, R.J., Chisholm, S.W., Devereux, R., and Stahl, D.A. (1990) Combination of 16S ribosomal-RNA-targeted oligonucleotide probes with flow-cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56: 1919-1925.
2. Arrigo, K.R. (2005) Marine microorganisms and global nutrient cycles. Nature 437: 349-355.
3. Codispoti, L.A., Brandes, J.A., Christensen, J.P., Devol, A.H., Naqvi, S.W.A., Paerl, H.W., and Yoshinari, T. (2001) The oceanic fixed nitrogen and nitrous oxide budgets: moving targets as we enter the anthropocene? Sci Mar 65: 85-105.
4. Cole, J. (1996) Nitrate reduction to ammonia by enteric bacteria: redundancy, or a strategy for survival during oxygen starvation? FEMS Microbiol Lett 136: 1-11.
5. Daims, H., Bruehl, A., Amann, R., Schleifer, K.H., and Wagner, M. (1999) The domain-specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22: 434-444.
6. 2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica. Nature 422: 606-608.
7. Einsle, O., Messerschmidt, A., Stach, P., Bourenkov, G.P., Bartunik, H.D., Huber, R., and Kroneck, P.M.H. (1999) Structure of cytochrome c nitrite reductase. Nature 400: 476-480.
8. van de Graaf, A.A.V., De Bruijn, P., Robertson, L.A., Jetten, M.S.M., and Kuenen, J.G. (1996) Autotrophic growth of anaerobic ammonium-oxidizing microorganisms in a fluidized bed reactor. Microbiol UK 142: 2187-2196.
9. Güven, D., Dapena, A., Kartal, B., Schmid, M.C., Maas, B., van de Pas-Schoonen, K., et al. (2005) Propionate oxidation by and methanol inhibition of anaerobic ammonium-oxidizing bacteria. Appl Environ Microbiol 71: 1066-1071.
10. Hooper, A.B., and Terry, K.R. (1979) Hydroxylamine oxidoreductase of nitrosomonas production of nitric-oxide from hydroxylamine. Biochim Biophys Acta 571: 12-20.
11. Jaffe, D.A. (2000) The nitrogen cycle. In Earth System Science. Jacobson, M.C., Charlson, R.J., Rohde, H., and Orians, G.H. (eds). San Diego, CA, USA: Academic Press, pp. 322-342.
12. Kartal, B., Rattray, J., van Niftrik, L., van de Vossenberg, J., Schmid, M., Webb, R.I., et al. (2006a) Candidatus 'Anammoxoglobus propionicus' gen. nov., sp. nov., a new propionate oxidizing species of anaerobic ammonium oxidizing bacteria. Syst Appl Microbiol doi: 10.1016/j.syapm.2006.03.004.
13. Kartal, B., Koleva, M., Arsov, R., van der star, W., Jetten, M.S.M., and Strous, M. (2006b) Adaptation of a freshwater anammox population to high salinity wastewater. J Biotechnol 126: 546-553.
14. Knowles, R. (1982) Denitrification. Microbiol Rev 46: 43-70.
15. Kuypers, M.M.M., Sliekers, A.O., Lavik, G., Schmid, M., Jorgensen, B.B., Kuenen, J.G., et al. (2003) Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422: 608-611.
16. Kuypers, M.M.M., Lavik, G., Woebken, D., Schmid, M., Fuchs, B.M., Amann, R., et al. (2005) Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc Natl Acad Sci USA 102: 6478-6483.
17. Kuypers, M.M.M., Lavik, G., and Thamdrup, B. (2006) Anaerobic ammonium oxidation in the marine environment. In Past and Present Water Column Anoxia. Neretin, L.N. (ed.). Dordrecht, the Netherlands: Springer, pp. 311-335.
18. Meyer, R.L., Risgaard-Petersen, N., and Allen, D.E. (2005) Correlation between anammox activity and microscale distribution of nitrite in a subtropical mangrove sediment. Appl Environ Microbiol 71: 6142-6149.
19. Mulder, A., Vandegraaf, A.A., Robertson, L.A., and Kuenen, J.G. (1995) Anaerobic ammonium oxidation discovered in a denitrifying fluidized-bed reactor. FEMS Microbiol Ecol 16: 177-183.
20. Richards, F.A. (1965) Anoxic basins and fjords. In Chemical Oceanography. Ripley, J.P., and Skirrow, G. (eds). London, UK: Academic Press, pp. 611-645.
21. Risgaard-Petersen, N., Rysgaard, S., and Revsbech, N.P. (1995) Combined microdiffusion-hypobromite oxidation method for determining nitrogen-15 isotope in ammonium. Soil Sci Soc Am J 59: 1077-1080.
22. Risgaard-Petersen, N., Nielsen, L.P., Rysgaard, S., Dalsgaard, T., and Meyer, R.L. (2003) Application of the isotope pairing technique in sediments where anammox and denitrification coexist. Limnol Oceanogr Methods 1: 63-73.
23. Risgaard-Petersen, N., Meyer, R.L., Schmid, M., Jetten, M.S. M., Enrich-Prast, A., Rysgaard, S., and Revsbech, N.P. (2004) Anaerobic ammonium oxidation in an estuarine sediment. Aquat Microb Ecol 36: 293-304.
24. Rysgaard, S., Glud, R.N., Risgaard-Petersen, N., and Dalsgaard, T. (2004) Denitrification and anammox activity in Arctic marine sediments. Limnol Oceanogr 49: 1493-1502.
25. Schmid, M., Twachtmann, U., Klein, M., Strous, M., Juretschko, S., Jetten, M., et al. (2000) Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Syst Appl Microbiol 23: 93-106.
26. Schmid, M., Walsh, K., Webb, R., Rijpstra, W.I.C., van de Pas-Schoonen, K., Verbruggen, M.J., et al. (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.
27. Schmid, M.C., Maas, B., Dapena, A., de Pas-Schoonen, K.V., de Vossenberg, J.V., Kartal, B., et al. (2005) Biomarkers for in situ detection of anaerobic ammonium-oxidizing (anammox) bacteria. Appl Environ Microbiol 71: 1677-1684.
28. Schouten, S., Strous, M., Kuypers, M.M.M., Rijpstra, W.I.C., Baas, M., Schubert, C.J., et al. (2004) Stable carbon isotopic Fractionations associated with inorganic carbon fixation by anaerobic ammonium-oxidizing bacteria. Appl Environ Microbiol 70: 3785-3788.
29. Simon, J. (2002) Enzymology and bioenergetics of respiratory nitrite ammonification. FEMS Microbiol Rev 26: 285-309.
30. Strous, M., Fuerst, J.A., Kramer, E.H.M., Logemann, S., Muyzer, G., van de Pas-Schoonen, K.T., et al. (1999) Missing lithotroph identified as new planctomycete. Nature 400: 446-449.
31. Strous, M., Pelletier, E., Mangenot, S., Rattei, T., Lehner, A., Taylor, M.W., et al. (2006) Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440: 790-794.
32. Thamdrup, B., and Dalsgaard, T. (2002) Production of N-2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl Environ Microbiol 68: 1312-1318.
33. Trimmer, M., Nicholls, J.C., and Deflandre, B. (2003) Anaerobic ammonium oxidation measured in sediments along the Thames estuary, United Kingdom. Appl Environ Microbiol 69: 6447-6454.
34. Wu, G.H., Wainwright, L.M., and Poole, R.K. (2003) Microbial globins. Adv Microbial Physiol 47: 255-310.
35. Zumft, W.G. (2005) Nitric oxide reductases of prokaryotes with emphasis on the respiratory, heme-copper oxidase type. J Inorg Biochem 99: 194-215.