Abstract
Anaerobic ammonium oxidation (anammox) and anaerobic methane oxidation (ANME coupled to denitrification) with nitrite as electron acceptor are two of the most recent discoveries in the microbial nitrogen cycle. Currently the anammox process has been relatively well investigated in a number of natural and man-made ecosystems, while ANME coupled to denitrification has only been observed in a limited number of freshwater ecosystems. The ubiquitous presence of anammox bacteria in marine ecosystems has changed our knowledge of the global nitrogen cycle. Up to 50% of N2 production in marine sediments and oxygen-depleted zones may be attributed to anammox bacteria. However, there are only few indications of anammox in natural and constructed freshwater wetlands. In this paper, the potential role of anammox and denitrifying methanotrophic bacteria in natural and artificial wetlands is discussed in relation to global warming. The focus of the review is to explore and analyze if suitable environmental conditions exist for anammox and denitrifying methanotrophic bacteria in nitrogen-rich freshwater wetlands.
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References
Alawi M, Lipski A, Sanders T, Pfeiffer EM, Spieck E (2007) Cultivation of a novel cold-adapted nitrite oxidizing betaproteobacterium from the Siberian Arctic. ISME J 1:256–264
Amano T, Yoshinaga I, Okada K, Yamagishi T, Ueda S, Obuchi A, Sako Y, Suwa Y (2007) Detection of anammox activity and diversity of anammox bacteria-related 16S rRNA genes in coastal marine sediment in Japan. Microbes Environ 22:232–242
Bezbaruah AN, Zhang TC (2004) pH, redox, and oxygen microprofiles in rhizosphere of Bulrush (Scirpus validus) in a constructed wetland treating municipal wastewater. Biotechnol Bioeng 88(1):60–69
Birol E, Karousakis K, Koundouri P (2006) Using a choice experiment to account for preference heterogeneity in wetland attributes: the case of Cheimaditida wetland in Greece. Ecol Econ 60(1):145–156
Boumann HA, Hopmans EC, van de Leemput I, Op den Camp HJM, van de Vossenberg J, Strous M, Jetten MSM, Sinninghe Damsté JS, Schouten S (2006) Ladderane phospholipids in anammox bacteria comprise phosphocholine and phosphoethanolamine headgroups. FEMS Microbiol Lett 258:297–304
Brandes JA, Devol AH, Deutsch C (2007) New developments in the marine nitrogen cycle. Chem Rev 107(2):577–589
Brune A, Frenzel P, Cypionka H (2000) Life at the oxic-anoxic interface: microbial activities and adaptations. FEMS Microbiol Rev 24:691–710
Byrne N, Strous M, Crépeau V, Kartal B, Birrien JL, Schmid M, Lesongeur F, Godfroy A (2009) Presence and activity of anaerobic ammonium-oxidizing bacteria at deep-sea hydrothermal vents. ISME J 3(1):117–123
Christensen PB, Revsbech NP, Sand-Jensen K (1994) Microsensor Analysis of Oxygen in the Rhizosphere of the Aquatic Macrophyte Littorella uniflora (L.) Ascherson. Plant Physiol 105:847–852
Dale OR, Tobias CR, Song B (2009) Biogeographical distribution of diverse anaerobic ammonium oxidizing (anammox) bacteria in Cape Fear River Estuary. Environ Microbiol 11:1194–1207
Dalsgaard T, Thamdrup B (2002) Factors controlling anaerobic ammonium oxidation with nitrite in marine sediments. Appl Environ Microbiol 68:3802–3808
Dalsgaard T, Canfield DE, Petersen J, Thamdrup B, Acuna-Gonzalez J (2003) N2 production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica. Nature 422(6932):606–608
Devol AH (2003) Solution to a marine mystery. Nature 422:575–576
Douglas GC, Angela NK (2007) A marine nitrogen cycle fix? Nature 445:159–160
Engström P, Penton CR, Devol AH (2009) Anaerobic ammonium oxidation in deep-sea sediments off the Washington margin. Limnol Oceanogr 54(5):1643–1652
Erler DV, Eyre BD, Davison L (2008) The contribution of Anammox and denitrification to sediment N2 production in a surface flow constructed wetland. Environ Sci Technol 42(24):9144–9150
Ettwig KF, Shima S, van de Pas-Schoonen KT, Kahnt J, Medema MH, Op den Camp HJM, Jetten MSM, Strous M (2008) Denitrifying bacteria anaerobically oxidize methane in the absence of Archaea. Environ Microbiol 10(11):3164–3173
Ettwig KF, van Alen T, van de Pas-Schoonen KT, Jetten MSM, Strous M (2009) Enrichment and molecular detection of denitrifying methanotrophic bacteria of the NC10 phylum. Appl Environ Microbiol 75(11):3656–3662
Francis CA, Roberts KJ, Beman JM, Santoro AE, Oakley BB (2005) Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc Natl Acad Sci USA 102(41):14683–14688
Galán A, Molina V, Bo T, Woebken D, Lavik G, Kuypers MMM, Ulloa O (2009) Anammox bacteria and the anaerobic oxidation of ammonium in the oxygen minimum zone off northern Chile. Deep-sea Res, Part 2, Top Stud Oceanogr 56(16):1021–1031
Hamersley MR, Lavik G, Woebken D, Rattray JE, Lam P, Hopmans EC, Sinninghe Damsté JS, Krüger S, Graco M, Gutiérrez D, Kuypers MMM (2007) Anaerobic ammonium oxidation in the Peruvian oxygen minimum zone. Limnol Oceanogr 52:923–933
Hamersley MR, Woebken D, Boehrer B, Schultze M, Lavik G, Kuypers MMM (2009) Water column anammox and denitrification in a temperate permanently stratified lake (Lake Rassnitzer, Germany). Systematic and Applied Microbiology 32(8):571–582
Hietanen S, Kuparinen J (2008) Seasonal and short-term variation in denitrification and anammox at a coastal station on the Gulf of Finland, Baltic Sea. Hydrobiologia 596:67–77
Hopmans EC, Kienhuis MVM, Rattray JE, Jaeschke A, Schouten S, Sinninghe Damsté JS (2006) Improved analysis of ladderane lipids in biomass and sediments using high-performance liquid chromatography/atmospheric pressure chemical ionization tandem mass spectrometry. Rapid Commun Mass Spectrom 20(14):2099–2103
Hu S, Zeng RJ, Burow LC, Lant P, Keller J, Yuan Z (2009) Enrichment of denitrifying anaerobic methane-oxidizing microorganisms. Environ Microbiol Rep 1(5):377–384
IPCC-Intergovernmental panel on climate change. Climate change 2001: the scientific basis. Summary for policy makers. Cambridge University Press, Cambridge, UK 2001a
Itokawa H, Hanaki K, Matsuo T (2001) Nitrous oxide production in high loading biological nitrogen removal process under low cod/n ratio condition. Water Res 35(3):657–664
Jaeschke A, Op den Camp HJM, Harhangi H, Klimiuk A, Hopmans EC, Jetten MSM, Schouten S, Sinninghe DJS (2009a) 16S rRNA gene and lipid biomarker evidence for anaerobic ammonium-oxidizing bacteria (anammox) in California and Nevada hot springs. FEMS Microbiol Ecol 67:343–350
Jaeschke A, Rooks C, Trimmer M, Nicholls JC, Hopmans EC, Schouten S, Sinninghe DJS (2009b) Comparison of ladderane phospholipid and core lipids as indicators for anaerobic ammonium oxidation (anammox) in marine sediments. Geochim Cosmochim Acta 73(7):2077–2088
Jensen MM, Thamdrup B, Dalsgaard T (2007) Effects of specific inhibitors on anammox and denitrification in marine sediments. Appl Environ Microbiol 73:3151–3158
Jensen MM, Petersen J, Dalsgaard T, Thamdrup B (2009) Pathways, rates, and regulation of N2 production in the chemocline of an anoxic basin, Mariager Fjord, Denmark. Mar Chem 113:102–113
Jetten MSM, Strous M, van de Pas-Schoonen KT, Schalk J, Udo van Dongen GJM, van de Graaf AA, Logemann S, Muyzer G, van Loosdrecht MCM, Kuenen JG (1999) The anaerobic oxidation of ammonium. FEMS Microbiol Rev 22:421–437
Jetten MSM, Wagner M, Fuerst J, van Loosdrecht MCM, Kuenen JG, Strous M (2001) Microbiology and application of the anaerobic ammonium oxidation (anammox) process. Curr Opin Biotechnol 12:283–288
Jetten MSM, Op den Camp HJM, Keltjens JT, Strous M (2008) Two impossible microbes with global implications: the nitrite-dependent anaerobic oxidation of methane and ammonium. In: Liu S-J, Drake HL (eds) Microbes and the Environment: Perspective And Challenges Science Press, Beijing 100717, China pp 15–22
Joye SB, Hollibaugh JT (1995) Influence of sulfide inhibition of nitrification on nitrogen regeneration in sediments. Science 270:623–625
Kampschreur MJ, Tan NCG, Picioreanu C, Jetten MSM, Schmidt I, van Loosdrecht MCM (2006) Role of nitrogen oxides in the metabolism of ammonia-oxidizing bacteria. Biochem Soc Trans 34:179–181
Kampschreur MJ, van der Star WRL, Wielders HA, Mulder JW, Jetten MSM, van Loosdrecht MCM (2008) Dynamics of nitric oxide and nitrous oxide emission during full-scale reject water treatment. Water Res 42:812–826
Kartal B, Rattray J, van Niftrik L, van de Vossenberg J, Schmid MC, Webb RI, Schouten S, Fuerst JA, Sinninghe Damsté JS, Jetten MSM, Strous M (2007) Candidatus 'Anammoxoglobus propionicus' a new propionate oxidizing species of anaerobic ammonium oxidizing bacteria. Syst Appl Microbiol 30:39–49
Kartal B, van Niftrik L, Rattray J, van de Vossenberg JL, Schmid MC, Sinninghe Damsté JS, Jetten MS, Strous M (2008) Candidatus 'Brocadia fulgida': an autofluorescent anaerobic ammonium oxidizing bacterium. FEMS Microbiol Ecol 63(1):46–55
Konnecke M, Berhnard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546
Koops HP, Pommerening-Röser A (2001) Distribution and ecophysiology of the nitrifying bacteria emphasizing cultured species. FEMS Microbiol Ecol 37:1–9
Koops HP, Böttcher B, Möller UC, Pommerening-Röser A, Stehr G (1991) Classification of eight new species of ammonia- oxidizing bacteria, Nitrosomonas communis sp. nov., Nitrosomonas ureae sp. nov., Nitrosomonas aestuarii sp. nov., Nitrosomonas marina sp. nov., Nitrosomonas nitrosa sp. nov., Nitrosomonas eutropha sp. nov., Nitrosomonas oligotropha sp. nov. and Nitrosomonas halophila sp. nov. J Gen Microbiol 137:1689–1699
Kuenen JG, Jetten MSM (2001) Extraordinary anaerobic ammonium oxidizing bacteria. ASM News 67:456
Kuypers MMM, Sliekers AO, Lavik G, Schmid M, Jørgensen BB, Kuenen JG, Sinninghe Damsté JS, Strous M, Jetten MSM (2003) Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422(10):608–611
Kuypers MMM, Lavik G, Wöbken D, Schmid M, Fuchs BM, Amann R (2005) Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc Natl Acad Sci USA 102:6478–6483
Lam P, Jensen MM, Lavik G, McGinnis DF, Müller B, Schubert CJ, Amann R, Thamdrup B, Kuypers MMM (2007) Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. Proc Natl Acad Sci USA 102:6478–6483
Lam P, Lavik G, Jensen MM, van de Vossenberg J, Schmid M, Woebken D, Gutiérrez D, Amann R, Jetten MSM, Kuypers MMM (2009) Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc Natl Acad Sci USA 106(12):4575–4756
Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809
Lindsay MR, Webb RI, Strous M, Jetten MS, Butler MK, Forde RJ, Fuerst JA (2001) Cell compartmentalisation in planctomycetes: novel types of structural organization for the bacterial cell. Arch Microbiol 175:413–429
Meyer RL, Risgaard-Petersen N, Allen DE (2005) Correlation between Anammox activity and microscale distribution of nitrite in a subtropical mangrove sediment. Appl Environ Microbiol 71:6142–6149
Mitsch WJ, Gosselink JG (2007) Wetlands, 4th edn. Wiley, New York
Morris J (1991) Effects of nitrogen loading on wetland ecosystems with particular reference to atmospheric deposition. Annu Rev Ecol Syst 22(1):257–279
Mulder A, Graaf AA, Robertson LA, Kuenen JG (1995) Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor. FEMS Microbiology Ecology 16(3):177–184
Murray JW, Jannash HW, Honjo S, Anderson RF, Reeburgh WS, Top Z, Friederich GE, Lodispoti LA, Izdar E (1989) Unexpected changes in the oxic/anoxic interface in the Black Sea. Nature 338:411–413
Paredes D, Kuschk P, Stange F, Müller RA, Köser H (2007) Model experiments on improving nitrogen removal in laboratory scale subsurface constructed wetlands by enhancing the anaerobic ammonia oxidation. Water Sci Technol 56(3):145–150
Peng Y, Zhu G (2006) Biological nitrogen removal with nitrification and denitrification via nitrite pathway. Appl Microbiol Biotechnol 73(1):15–26
Pynaert K, Smets BF, Wyffels S, Beheydt D, Siciliano SD, Verstraete W (2003) Characterization of an autotrophic nitrogen-removing biofilm from a highly loaded lab-scale rotating biological contactor. Appl Environ Microbiol 69(6):3626–3635
Quan ZX, Rhee SK, Zuo JE, Yang Y, Bae JW, Park JR, Lee ST, Park YH (2008) Diversity of ammonium-oxidizing bacteria in a granular sludge anaerobic ammonium-oxidizing (anammox) reactor. Environ Microbiol 10(11):3130–3139
Raghoebarsing AA, Pol A, van de Pas-Schoonen KT, Smolders AJ, Ettwig KF, Rijpstra WI, Schouten S, Damsté JS, Op den Camp HJ, Jetten MS, Strous M (2006) A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440(7086):918–921
Rattray JE, van de Vossenberg J, Hopmans EC, Kartal B, van Niftrik L, Rijpstra WI, Strous M, Jetten MSM, Schouten S, Sinninghe Damsté JS (2008) Ladderane lipid distribution in four genera of anammox bacteria. Arch Microbiol 190(1):51–66
Rich JJ, Dale OR, Song B, Ward BB (2008) Anaerobic Ammonium Oxidation (Anammox) in Chesapeake Bay sediments. Microb Ecol 55:311–320
Risgaard-Petersen N, Meyer RL, Schmid M, Jetten MSM, Enrich-Prast A, Rysgaard S, Revsbech NP (2004) Anaerobic ammonia oxidation in an estuarine sediment. Aquat Microb Ecol 36:293–304
Rysgaard S, Glud RN, Risgaard-Petersen N, Dalsgaard T (2004) Denitrification and anammox activity in arctic marine sediments. Limnol Oceanogr 49:1493–1502
Schmid M, Twachtmann U, Klein M, Strous M, Juretschko S, Jetten MSM, Metzger JW, Schleifer KH, Wagner M (2000) Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Systamatic Applied Microbiology 23:93–106
Schmid M, Walsh K, Webb R, Rijpstra WIC, van de Pas-Schoonen K, Verbruggen MJ, Hill T, Moffett B, Fuerst J, Schouten S, Sinninghe DJS, Harris J, Shaw P, Jetten M, Strous M (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
Schmid MC, Maas B, Dapena A, van de Pas-Schoonen K, van de Vossenberg J, Kartal B, van Niftrik L, Schmidt I, Cirpus I, Kuenen JG, Wagner M, Sinninghe Damsté JS, Kuypers M, Revsbech NP, Mendez R, Jetten MSM, Strous M (2005) Biomarkers for in situ detection of anaerobic ammonium-oxidizing (anammox) bacteria. Appl Environ Microbiol 71(4):1677–1684
Schmid MC, Risgaard-Petersen N, van de Vossenberg J, Kuypers MMM, Lavik G, Petersen J, Hulth S, Thamdrup B, Canfield D, Dalsgaard T, Rysgaard S, Sejr MK, Strous M, Op den Camp HJM, Jetten MSM (2007) Anaerobic ammonium-oxidizing bacteria in marine environments: widespread occurrence but low diversity. Environ Microbiol 9(6):1476–1484
Schubert CJ, Durisch-Kaiser E, Wehrli B, Thamdrup B, Lam P, Kuypers MMM (2006) Anaerobic ammonium oxidation in a tropical freshwater system (Lake Tanganyika). Environ Microbiol 8:1857–1863
Shipin O, Koottatep T, Khanh NTT, Polprasert C (2005) Integrated natural treatment systems for developing communities: low-tech N-removal through the fluctuating microbial pathways. Water Sci Technol 51(12):299–306
Sinninghe DJS, Strous M, Rijpstra WIC, Hopmans EC, Geenevasen JAJ, van Duin ACT, van Niftrik LA, Jetten MSM (2002) Linearly concatenated cyclobutane lipids form a dense bacterial membrane. Nature 419:708–712
Sinninghe DJS, Rijpstra WIC, Geenevasen JAJ, Strous M, Jetten MSM (2005) Structural identification of ladderane and other membrane lipids of planctomycetes capable of anaerobic ammonium oxidation (anammox). FEBS J 272(16):4270–4283
Søvik AK, Augustin J, Heikkinen K, Huttunen JT, Necki JM, Karjalainen SM, Kløve B, Liikanen A, Mander U, Puustinen M, Teiter S, Wachniew P (2006) Emission of the greenhouse gases nitrous oxide and methane from constructed wetlands in Europe. J Environ Qual 35(6):2360–2373
Stottmeister U, Wießner A, Kuschk P, Kappelmeyer U, Kästner M, Bederski O, Muller RA, Moormann H (2003) Effects of plants and microorganisms in constructed wetlands for wastewater treatment. Biotechnol Adv 22:93–117
Strous M, Jetten MSM (2004) Anaerobic oxidation of methane and ammonium. Annu Rev Microbiol 58:99–117
Strous M, Van Gerven E, Kuenen JG, Jetten M (1997) Effects of Aerobic and Microaerobic Conditions on Anaerobic Ammonium-Oxidizing (Anammox) Sludge. Appl Environ Microbiol 63(6):2446–2448
Strous M, Fuerst JA, Evelien HMK, Logemann S, Muyzer G, van de Pas-Schoonen KT, Webb R, Kuenen JG, Jetten MSM (1999) Missing lithotroph identified as new planctomycete. Nature 400(6743):446–449
Strous M, Pelletier E, Mangenot S, Rattei T, Lehner A, Taylor MW, Horn M, Daims H, Bartol-Mavel D, Wincker P, Barbe V, Fonknechten N, Vallenet D, Segurens B, Schenowitz-Truong C, Medigue C, Collingro A, Snel B, Dutilh BE, Op den Camp HJ, van der Drift C, Cirpus I, van de Pas-Schoonen KT, Harhangi HR, van Niftrik L, Schmid M, Keltjens J, van de Vossenberg J, Kartal B, Meier H, Frishman D, Huynen MA, Mewes HW, Weissenbach J, Jetten MS, Wagner M, Le Paslier D (2006) Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440:790–794
Tal Y, Watts JE, Schreier HJ (2005) Anaerobic ammonia-oxidizing bacteria and related activity in Baltimore inner harbor sediment. Appl Environ Microbiol 71:1816–1821
Thamdrup B, Dalsgaard T (2002) Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl Environ Microbiol 68:1312–1318
Third KA, Sliekers AO, Kuenen JG, Jetten MSM (2001) The CANON system (Completely Autotrophic Nitrogen-removal Over Nitrite) under ammonium limitation: interaction and competition between three groups of bacteria. Syst Appl Microbiol 24(4):588–596
Trimmer M, Nicholls JC (2009) Production of nitrogen gas via anammox and denitrification in intact sediment cores along a continental shelf to slope transect in the North Atlantic. Limnol Oceanogr 54(2):577–589
van de Graaf AA, Mulder A, de Bruijn P, Jetten MS, Robertson LA, Kuenen JG (1995) Anaerobic oxidation of ammonium is a biologically mediated process. Appl Environ Microbiol 61(4):1246–1251
van de Vossenberg J, Rattray JE, Geerts W, Kartal B, van Niftrik L, van Donselaar EG, Sinninghe Damsté JS, Strous M, Jetten MS (2008) Enrichment and characterization of marine anammox bacteria associated with global nitrogen gas production. Environ Microbiol 10(11):3120–3129
van Dongen U, Jetten MSM, van Loosdrecht MCM (2001) The SHARON®-Anammox® process for treatment of ammonium rich wastewater. Water Science & Technology 44(1):153–160
van Niftrik LA, Fuerst JA, Damsté JSS, Kuenen JG, Jetten MSM, Strous M (2004) The anammoxosome: an intracytoplasmic compartment in anammox bacteria. FEMS Microbiol Lett 233(1):7–13
van Niftrik L, Geerts WJC, van Donselaar EG, Humbel BM, Webb RI, Fuerst JA, Verkleij AJ, Jetten MSM, Strous M (2008a) 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(2):708–717
van Niftrik L, Geerts WJC, van Donselaar EG, Humbel BM, Yakushevska A, Verkleij AJ, Jetten MSM, Strous M (2008b) Combined structural and chemical analysis of the anammoxosome: a membrane-bounded intracytoplasmic compartment in anammox bacteria. J Struct Biol 161(3):401–410
Wang H, Wang W, Yin C, Wang Y, Lu J (2006a) Littoral zones as the ‘‘hotspots’’ of nitrous oxide (N2O) emission in a hyper-eutrophic lake in China. Atmos Environ 40:5522–5527
Wang HJ, Lu JW, Wang WD, Yang LY, Yin CQ (2006b) Methane fluxes from the littoral zone of hypereutrophic Taihu Lake, China. J Geophys Res-Atmos 111:D17109. doi:10.1029/2005JD006864
Wang H, Yang L, Wang W, Lu J, Yin C (2007a) Nitrous oxide (N2O) fluxes and their relationship with water-sediment parameters in a hyper-eutrophic shallow Lake, China. J Geophys Res-Biogeosci 112:G01005. doi:10.1029/2005JG000129
Wang HJ, Lu JW, Wang WD, Huang PH, Yin CQ (2007b) Spatio-temporal distribution of nitrogen in the undulating littoral zone of Lake Taihu, China. Hydrobiologia 581:97–108
Ward BB (2003) Significance of anaerobic ammonium oxidation in the ocean. Trend Microbiol 11(9):408–410
Woebken D, Fuchs BM, Kuypers MMM, Amann R (2007) Potential interactions of particle-associated anammox bacteria with bacterial and archaeal partners in the Namibian upwelling system. Appl Environ Microbiol 73:4648–4657
Woebken D, Lam P, Kuypers MM, Naqvi SW, Kartal B, Strous M, Jetten MSM, Fuchs BM, Amann R (2008) A microdiversity study of anammox bacteria reveals a novel Candidatus Scalindua phylotype in marine oxygen minimum zones. Environ Microbiol 10(11):3106–3119
Zhu G, Peng Y, Li B, Guo J, Yang Q, Wang S (2008) Biological nitrogen removal from wastewater. Rev Environ Contam Toxicol 192:159–195
Acknowledgements
This research is financially jointly supported by the National Natural Science Foundation of China (No. 20877086), National Basic Research Program of China (No. 2009CB421103), Knowledge Innovation Program of the Chinese Academy of Sciences (RCEES-QN-200706; KZCXI-YW-06-02), and special fund of the State Key Laboratory of Environmental Aquatic Chemistry (08Y04ESPCR). The anammox research of MJ is support by ERC Advanced grant 232937. Moreover, the Guibing Zhu wants to give special appreciation to German Academic Exchange Service (DAAD) for their financially supporting the opportunity to visit the Helmholtz-Centre for Environmental Research–UFZ Leipzig-Halle, Germany and the Department of Microbiology, IWWR, Nijmegen, The Netherlands.
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Zhu, G., Jetten, M.S.M., Kuschk, P. et al. Potential roles of anaerobic ammonium and methane oxidation in the nitrogen cycle of wetland ecosystems. Appl Microbiol Biotechnol 86, 1043–1055 (2010). https://doi.org/10.1007/s00253-010-2451-4
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DOI: https://doi.org/10.1007/s00253-010-2451-4