Proteins and protein complexes involved in the biochemical reactions of anaerobic ammonium-oxidizing bacteria

Biochemical Society Transactions

Volumn 39, Issue 1, 2011, Pages 303-308

  De Almeida, Naomi M ^a   Maalcke, Wouter J ^a   Keltjens, Jan T ^a   Jetten, Mike S M ^a,b   Kartal, Boran ^a  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

Anaerobic ammonium oxidation (anammox); Hydrazine; Hydroxylamine oxidoreductase (HAO); Nitrate reductase (nar); Protonmotive force

Indexed keywords

AMMONIA; BACTERIAL PROTEIN; NITRITE; NITROGEN;

ANAEROBIC METABOLISM; BACTERIAL METABOLISM; BACTERIUM; CHEMICAL REACTION; CONFERENCE PAPER; NITROGEN FIXATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION;

ADENOSINE TRIPHOSPHATE; BACTERIA, ANAEROBIC; BACTERIAL PROTEINS; ELECTRON TRANSPORT; GENOME, BACTERIAL; MULTIGENE FAMILY; NITRATES; NITRITES; NITROGEN; OXIDATION-REDUCTION; QUATERNARY AMMONIUM COMPOUNDS;

EID: 79551491148     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0390303     Document Type: Conference Paper

References (45)

1. Broda, E. (1977) Two kinds of lithotrophs missing in nature. Z. Allg. Mikrobiol. 17, 491-493
2. Strous, M., Fuerst, J.A., Kramer, E.H.M., Logemann, S., Muyzer, G., van de Pas-Schoonen, K.T., Webb, R., Kuenen, J.G. and Jetten, M.S.M. (1999) Missing lithotroph identified as new planctomycete. Nature 400, 446-449
3. Jetten, M.S.M., Op den Camp, H.J.M., Kuenen, G.J. and Strous, M. (2010) Family I. 'Candidatus Brocadiaceae' fam. nov. In Bergey's Manual of Systematic Bacteriology (Krieg, N.R., Staley, J.T., Brown, D.R., Hedlund, B., Paster, B.J., Ward, N., Ludwig, W. and Whitman, W.B., eds), pp. 596-602, Springer, New York
4. Jetten, M.S.M., Horn, S.J. and van Loosdrecht, M.C.M. (1997) Towards a more sustainable municipal wastewater treatment system. Water Sci. Technol. 35, 171-180
5. Kartal, B., van Niftrik, L., Sliekers, O., Schmid, M.C., Schmidt, I., van de Pas-Schoonen, K., Cirpus, I., van der Star, W., van Loosdrecht, M., Abma, W. et al. (2004) Application, eco-physiology and biodiversity of anaerobic ammonium-oxidizing bacteria. Rev. Environ. Sci. Bio/Technol. 3, 255-264
6. Kuypers, M.M.M., Lavik, G., Woebken, D., Schmid, M., Fuchs, B.M., Amann, R., Jorgensen, B.B. and Jetten, M.S.M. (2005) Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc. Natl. Acad. Sci. U.S.A. 102, 6478-6483
7. 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.), pp. 311-335, Springer, Dordrecht
8. Penton, C.R., Devol, A.H. and Tiedje, J.M. (2006) Molecular evidence for the broad distribution of anaerobic ammonium-oxidizing bacteria in freshwater and marine sediments. Appl. Environ. Microbiol. 72, 6829-6832
9. Abma, W., Schultz, C., Mulder, J.W., Van Loosdrecht, M.C.M., van der Star, W., Strous, M. and Tokutomi, T. (2007) The advance of anammox. Water 21, 36-37
10. Schmid, M.C., Risgaard-Petersen, N., van de Vossenberg, J., Kuypers, M.M.M., Lavik, G., Petersen, J., Hulth, S., Thamdrup, B., Canfield, D., Dalsgaard, T. et al. (2007) Anaerobic ammonium-oxidizing bacteria in marine environments: widespread occurrence but low diversity. Environ. Microbiol. 9, 1476-1484
11. Abma, W.R., Driessen, W., Haarhuis, R. and van Loosdrecht, M.C.M. (2010) Upgrading of sewage treatment plant by sustainable and cost-effective separate treatment of industrial wastewater. Water Sci. Technol. 61, 1715-1722
12. Kartal, B., Kuenen, J.G. and van Loosdrecht, M.C.M. (2010) Sewage treatment with anammox. Science 328, 702-703
13. Rysgaard, S. and Glud, R.N. (2004) Anaerobic N2 production in Arctic sea ice. Limnol. Oceanogr. 49, 86-94
14. 2 production in coastal marine sediments. Geochim. Cosmochim. Acta 69, 2057-2065
15. 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
16. Schubert, C.J., Durisch-Kaiser, E., Wehrli, B., Thamdrup, B., Lam, P. and Kuypers, M.M.M. (2006) Anaerobic ammonium oxidation in a tropical freshwater system (Lake Tanganyika). Environ. Microbiol. 8, 1857-1863
17. Arrigo, K.R. (2005) Marine microorganisms and global nutrient cycles. Nature 437, 349-355
18. Brandes, J.A., Devol, A.H. and Deutsch, C. (2007) New developments in the marine nitrogen cycle. Chem. Rev. 107, 577-589
19. Francis, C.A., Beman, J.M. and Kuypers, M.M.M. (2007) New processes and players in the nitrogen cycle: the microbial ecology of anaerobic and archaeal ammonia oxidation. ISME J. 1, 19-27
20. Cirpus, I.E.Y., Geerts, W., Hermans, J.H.M., den Camp, H., Strous, M., Kuenen, J.G. and Jetten, M.S.M. (2006) Challenging protein purification from anammox bacteria. Int. J. Biol. Macromol. 39, 88-94
21. Strous, M., Kuenen, J.G. and Jetten, M.S.M. (1999) Key physiology of anaerobic ammonium oxidation. Appl. Environ. Microbiol. 65, 3248-3250
22. Sinninghe Damsté, J.S., Strous, M., Rijpstra, W.I.C., Hopmans, E.C., Geenevasen, J.A.J., van Duin, A.C.T., van Niftrik, L.A. and Jetten, M.S.M. (2002) Linearly concatenated cyclobutane lipids form a dense bacterial membrane. Nature 419, 708-712
23. Strous, M., Pelletier, E., Mangenot, S., Rattei, T., Lehner, A., Taylor, M.W., Horn, M., Daims, H., Bartol-Mavel, D., Wincker, P. et al. (2006) Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440, 790-794
24. Kartal, B., Kuypers, M.M.M., Lavik, G., Schalk, J., Op den Camp, H.J.M., Jetten, M.S.M. and Strous, M. (2007) Anammox bacteria disguised as denitrifiers: nitrate reduction to dinitrogen gas via nitrite and ammonium. Environ. Microbiol. 9, 635-642
25. Kartal, B., Rattray, J., van Niftrik, L.A., van de Vossenberg, J., Schmid, M.C., Webb, R.I., Schouten, S., Fuerst, J.A., Damste, J.S.S., Jetten, M.S.M. and Strous, M. (2007) Candidatus 'Anammoxoglobus propionicus' a new propionate oxidizing species of anaerobic ammonium oxidizing bacteria. Syst. Appl. Microbiol. 30, 39-49
26. Kartal, B., van Niftrik, L., Rattray, J., de Vossenberg, J., Schmid, M.C., Damste, J.S.S., Jetten, M.S.M. and Strous, M. (2008) Candidatus 'Brocadia fulgida': an autofluorescent anaerobic ammonium oxidizing bacterium. FEMS Microbiol. Ecol. 63, 46-55
27. Van de Graaf, A.A., deBruijn, P., Robertson, L.A., Jetten, M.S.M. and Kuenen, J.G. (1997) Metabolic pathway of anaerobic ammonium oxidation on the basis of 15N studies in a fluidized bed reactor. Microbiology 143, 2415-2421
28. Van der Star, W.R.L., van de Graaf, M.J., Kartal, B., Picioreanu, C., Jetten, M.S.M. and van Loosdrecht, M.C.M. (2008) Response of anaerobic ammonium-oxidizing bacteria to hydroxylamine. Appl. Environ. Microbiol. 74, 4417-4426
29. Van Niftrik, L., Geerts, W.J.C., Van Donselaar, E.G., Humbel, B.M., Webb, R.I., Fuerst, J.A., Verkleij, A.J., Jetten, M.S.M. and Strous, M. (2008) Linking ultrastructure and function in four genera of anaerobic ammonium-oxidizing bacteria: cell plan, glycogen storage, and localization of cytochrome c proteins. J. Bacteriol. 190, 708-717
30. Van de Graaf, A.A., deBruijn, P., Robertson, L.A., Jetten, M.S.M. and Kuenen, J.G. (1996) Autotrophic growth of anaerobic ammonium-oxidizing micro-organisms in a fluidized bed reactor. Microbiology 142, 2187-2196
31. Van de Graaf, A.A., Mulder, A., Debruijn, P., Jetten, M.S.M., Robertson, L.A. and Kuenen, J.G. (1995) Anaerobic oxidation of ammonium is a biologically mediated process. Appl. Environ. Microbiol. 61, 1246-1251
32. Guven, D., Dapena, A., Kartal, B., Schmid, M.C., Maas, B., van de Pas-Schoonen, K., Sozen, S., Mendez, R., Op den Camp, H.J.M., Jetten, M.S.M. et al. (2005) Propionate oxidation by and methanol inhibition of anaerobic ammonium-oxidizing bacteria. Appl. Environ. Microbiol. 71, 1066-1071
33. Anderson, J.H. (1964) The metabolism of hydroxylamine to nitrite by Nitrosomonas. Biochem. J. 91, 8-17
34. Hooper, A.B., Vannelli, T., Bergmann, D.J. and Arciero, D.M. (1997) Enzymology of the oxidation of ammonia to nitrite by bacteria. Antonie Van Leeuwenhoek 71, 59-67
35. Klotz, M.G., Schmid, M.C., Strous, M., Op den Camp, H., Jetten, M.S.M. and Hooper, A.B. (2008) Evolution of an octahaem cytochrome c protein family that is key to aerobic and anaerobic ammonia oxidation by bacteria. Environ. Microbiol. 10, 3150-3163
36. Shimamura, M., Nishiyama, T., Shigetomo, H., Toyomoto, T., Kawahara, Y., Furukawa, K. and Fujii, T. (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
37. Van Niftrik, L., Geerts, W.J.C., van Donselaar, E.G., Humbel, B.M., Yakushevska, A., Verkleij, A.J., Jetten, M.S.M. and Strous, M. (2008) Combined structural and chemical analysis of the anammoxosome: a membrane-bounded intracytoplasmic compartment in anammox bacteria. J. Struct. Biol. 161, 401-410
38. Van Niftrik, L., van Helden, M., Kirchen, S., van Donselaar, E.G., Harhangi, H.R., Webb, R.I., Fuerst, J.A., Op den Camp, H.J., Jetten, M.S. and Strous, M. (2010) Intracellular localization of membrane-bound ATPases in the compartmentalized anammox bacterium 'Candidatus Kuenenia stuttgartiensis'. Mol. Microbiol. 77, 701-715
39. Shimamura, M., Nishiyama, T., Shinya, K., Kawahara, Y., Furukawa, K. and Fujii, T. (2008) Another multiheme protein, hydroxylamine oxidoreductase, abundantly produced in an anammox bacterium besides the hydrazine-oxidizing enzyme. J. Biosci. Bioeng. 105, 243-248
40. Schalk, J., de Vries, S., Kuenen, J.G. and Jetten, M.S.M. (2000) Involvement of a novel hydroxylamine oxidoreductase in anaerobic ammonium oxidation. Biochemistry 39, 5405-5412 (Pubitemid 30257081)
41. 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
42. Simon, J. (2002) Enzymology and bioenergetics of respiratory nitrite ammonification. FEMS Microbiol. Rev. 26, 285-309
43. Methe, B.A., Nelson, K.E., Eisen, J.A., Paulsen, I.T., Nelson, W., Heidelberg, J.F., Wu, D., Wu, M., Ward, N., Beanan, M.J. et al. (2003) Genome of Geobacter sulfurreducens: metal reduction in subsurface environments. Science 302, 1967-1969
44. Heidelberg, J.F., Paulsen, I.T., Nelson, K.E., Gaidos, E.J., Nelson, W.C., Read, T.D., Eisen, J.A., Seshadri, R., Ward, N., Methe, B. et al. (2002) Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nat. Biotechnol. 20, 1118-1123
45. Van Niftrik, L.A., Fuerst, J.A., Sinninghe Damsté, J.S., Kuenen, J.G., Jetten, M.S.M. and Strous, M. (2004) The anammoxosome: an intracytoplasmic compartment in anammox bacteria. FEMS Microbiol. Lett. 233, 7-13