Anaerobic ammonia oxidizing bacteria: ecological distribution, metabolism, and microbial interactions

Highlights

The unique characteristics of anammox bacteria were reviewed.

Ecological distribution and nitrogen loss contributions were well documented.

Ecological interactions between anammox bacteria and other organisms were discussed.

Abstract

Anammox (ANaerobic AMMonia OXidation) is a newly discovered pathway in the nitrogen cycle. This discovery has increased our knowledge of the global nitrogen cycle and triggered intense interest for anammox-based applications. Anammox bacteria are almost ubiquitous in the suboxic zones of almost all types of natural ecosystems and contribute significant to the global total nitrogen loss. In this paper, their ecological distributions and contributions to the nitrogen loss in marine, wetland, terrestrial ecosystems, and even extreme environments were reviewed. The unique metabolic mechanism of anammox bacteria was well described, including the particular cellular structures and genome compositions, which indicate the special evolutionary status of anammox bacteria. Finally, the ecological interactions among anammox bacteria and other organisms were discussed based on substrate availability and spatial organizations. This review attempts to summarize the fundamental understanding of anammox, provide an up-to-date summary of the knowledge of the overall anammox status, and propose future prospects for anammox. Based on novel findings, the metagenome has become a powerful tool for the genomic analysis of communities containing anammox bacteria; the metabolic diversity and biogeochemistry in the global nitrogen budget require more comprehensive studies.

Graphical abstract

Keywords

Anammox / Metabolism / Metagenome / Ecological distribution / Microbial interactions

References

[1] Dalsgaard T, Thamdrup B, Canfield D E. Anaerobic ammonium oxidation (anammox) in the marine environment. Research in Microbiology, 2005, 156(4): 457–464

[2] Broda E. Two kinds of lithotrophs missing in nature. Zeitschrift fur allgemeine Mikrobiologie, 1977, 17(6): 491–493

[3] Mulder A, Graaf A, Robertson L, Kuenen J. Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor. FEMS Microbiology Ecology, 1995, 16(3): 177–184

[4] van de Graaf A A, Mulder A, de Bruijn P, Jetten M S, Robertson L A, Kuenen J G. Anaerobic oxidation of ammonium is a biologically mediated process. Applied and Environmental Microbiology, 1995, 61(4): 1246–1251

[5] Liu S, Yang F, Gong Z, Meng F, Chen H, Xue Y, Furukawa K. Application of anaerobic ammonium-oxidizing consortium to achieve completely autotrophic ammonium and sulfate removal. Bioresource Technology, 2008, 99(15): 6817–6825

[6] Kuypers M M, Sliekers A O, Lavik G, Schmid M, Jørgensen B B, Kuenen J G, Sinninghe Damsté J S, Strous M, Jetten M S. Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature, 2003, 422(6932): 608–611

[7] Woebken D, Lam P, Kuypers M M, Naqvi S W, Kartal B, Strous M, Jetten M S, Fuchs B M, Amann R. A microdiversity study of anammox bacteria reveals a novel Candidatus Scalindua phylotype in marine oxygen minimum zones. Environmental Microbiology, 2008, 10(11): 3106–3119

[8] Li H, Chen S, Mu B Z, Gu J D. Molecular detection of anaerobic ammonium-oxidizing (anammox) bacteria in high-temperature petroleum reservoirs. Microbial Ecology, 2010, 60(4): 771–783

[9] Hong Y G, Li M, Cao H, Gu J D. Residence of habitat-specific anammox bacteria in the deep-sea subsurface sediments of the South China Sea: Analyses of marker gene abundance with physical chemical parameters. Microbial Ecology, 2011, 62(1): 36–47

[10] van de Vossenberg J, Woebken D, Maalcke W J, Wessels H J, Dutilh B E, Kartal B, Janssen-Megens E M, Roeselers G, Yan J, Speth D, Gloerich J, Geerts W, van der Biezen E, Pluk W, Francoijs K J, Russ L, Lam P, Malfatti S A, Tringe S G, Haaijer S C, Op den Camp H J, Stunnenberg H G, Amann R, Kuypers M M, Jetten M S. The metagenome of the marine anammox bacterium ‘Candidatus Scalindua profunda’ illustrates the versatility of this globally important nitrogen cycle bacterium. Environmental Microbiology, 2013, 15(5): 1275–1289

[11] Fuchsman C A, Staley J T, Oakley B B, Kirkpatrick J B, Murray J W. Free-living and aggregate-associated Planctomycetes in the Black Sea. FEMS Microbiology Ecology, 2012, 80(2): 402–416

[12] Dalsgaard T, Canfield D E, Petersen J, Thamdrup B, Acuña-González J. N₂ production by the anammox reaction in the anoxic water column of Golfo Dulce, Costa Rica. Nature, 2003, 422(6932): 606–608

[13] Lam P, Lavik G, Jensen M M, van de Vossenberg J, Schmid M, Woebken D, Gutiérrez D, Amann R, Jetten M S M, Kuypers M M M. Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proceedings of the National Academy of Sciences of the United States of America, 2009, 106(12): 4752–4757

[14] Rush D, Wakeham S G, Hopmans E C, Schouten S, Sinninghe Damsté J S. Biomarker evidence for anammox in the oxygen minimum zone of the Eastern Tropical North Pacific. Organic Geochemistry, 2012, 53: 80–87

[15] Nicholls J C, Davies C A, Trimmer M. High-resolution profiles and nitrogen isotope tracing reveal a dominant source of nitrous oxide and multiple pathways of nitrogen gas formation in the central Arabian Sea. Limnology and Oceanography, 2007, 52(1): 156–168

[16] Jensen M M, Lam P, Revsbech N P, Nagel B, Gaye B, Jetten M S, Kuypers M M. Intensive nitrogen loss over the Omani Shelf due to anammox coupled with dissimilatory nitrite reduction to ammonium. The ISME Journal, 2011, 5(10): 1660–1670

[17] Kuypers M M, Lavik G, Woebken D, Schmid M, Fuchs B M, Amann R, Jørgensen B B, Jetten M S. Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proceedings of the National Academy of Sciences of the United States of America, 2005, 102(18): 6478–6483

[18] Schneider B, Nausch G, Pohl C. Mineralization of organic matter and nitrogen transformations in the Gotland Sea deep water. Marine Chemistry, 2010, 119(1–4): 153–161

[19] Schmid M C, Risgaard-Petersen N, van de Vossenberg J, Kuypers M M, Lavik G, Petersen J, Hulth S, Thamdrup B, Canfield D, Dalsgaard T, Rysgaard S, Sejr M K, Strous M, den Camp H J, Jetten M S. Anaerobic ammonium-oxidizing bacteria in marine environments: Widespread occurrence but low diversity. Environmental Microbiology, 2007, 9(6): 1476–1484

[20] Thamdrup B, Dalsgaard T. Production of N₂ through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Applied and Environmental Microbiology, 2002, 68(3): 1312–1318

[21] Shu Q, Jiao N. Profiling Planctomycetales diversity with reference to anammox-related bacteria in a South China Sea, deep-sea sediment. Marine Ecology (Berlin), 2008, 29(4): 413–420

[22] Trimmer M, Nicholls J C. Production of nitrogen gas via anammox and denitrification in intact sediment cores along a continental shelf to slope transect in the North Atlantic. Limnology and Oceanography, 2009, 54(2): 577–589

[23] Shehzad A, Liu J, Yu M, Qismat S, Liu J, Zhang X H. Diversity, community composition and abundance of anammox bacteria in sediments of the North Marginal Seas of China. Microbes and Environments, 2016, 31(2): 111–120

[24] Kartal B, Kuypers M M, Lavik G, Schalk J, Op den Camp H J, Jetten M S, Strous M. Anammox bacteria disguised as denitrifiers: Nitrate reduction to dinitrogen gas via nitrite and ammonium. Environmental Microbiology, 2007, 9(3): 635–642

[25] Schubert C J, Durisch-Kaiser E, Wehrli B, Thamdrup B, Lam P, Kuypers M M. Anaerobic ammonium oxidation in a tropical freshwater system (Lake Tanganyika). Environmental Microbiology, 2006, 8(10): 1857–1863

[26] Penton C R, Devol A H, Tiedje J M. Molecular evidence for the broad distribution of anaerobic ammonium-oxidizing bacteria in freshwater and marine sediments. Applied and Environmental Microbiology, 2006, 72(10): 6829–6832

[27] Wang S, Zhu G, Peng Y, Jetten M S, Yin C. Anammox bacterial abundance, activity, and contribution in riparian sediments of the Pearl River estuary. Environmental Science & Technology, 2012, 46(16): 8834–8842

[28] Han P, Gu J D. Further analysis of anammox bacterial community structures along an anthropogenic nitrogen-input gradient from the riparian sediments of the Pearl River Delta to the deep-ocean sediments of the South China Sea. Geomicrobiology Journal, 2015, 32(9): 789–798

[29] Hou L J, Zheng Y L, Liu M, Gong J, Zhang X L, Yin G Y, You L. Anaerobic ammonium oxidation (anammox) bacterial diversity, abundance, and activity in marsh sediments of the Yangtze Estuary. Journal of Geophysical Research. Biogeosciences, 2013, 118(3): 1237–1246

[30] Nicholls J C, Trimmer M. Widespread occurrence of the anammox reaction in estuarine sediments. Aquatic Microbial Ecology, 2009, 55(2): 105–113

[31] Fernandes S O, Michotey V D, Guasco S, Bonin P C, Bharathi P A. Denitrification prevails over anammox in tropical mangrove sediments (Goa, India). Marine Environmental Research, 2012, 74: 9–19

[32] Koop-Jakobsen K, Giblin A E. Anammox in tidal marsh sediments: The role of salinity, nitrogen loading, and marsh vegetation. Estuaries and Coasts, 2009, 32(2): 238–245

[33] Sato Y, Ohta H, Yamagishi T, Guo Y, Nishizawa T, Rahman M H, Kuroda H, Kato T, Saito M, Yoshinaga I, Inubushi K, Suwa Y. Detection of anammox activity and 16S rRNA genes in ravine paddy field soil. Microbes and Environments, 2012, 27(3): 316–319

[34] .Hamersley M R, Woebken D, Boehrer B, Schultze M, Lavik G, Kuypers M M. Water column anammox and denitrification in a temperate permanently stratified lake (Lake Rassnitzer, Germany). Systematic and Applied Microbiology, 2009, 32(8): 571–582

[35] Dale O R, Tobias C R, Song B. Biogeographical distribution of diverse anaerobic ammonium oxidizing (anammox) bacteria in Cape Fear River Estuary. Environmental Microbiology, 2009, 11(5): 1194–1207

[36] Fu B, Liu J, Yang H, Hsu T C, He B, Dai M, Kao S J, Zhao M, Zhang X H. Shift of anammox bacterial community structure along the Pearl Estuary and the impact of environmental factors. Journal of Geophysical Research. Oceans, 2015, 120(4): 2869–2883

[37] Wang J, Gu J D. Dominance of Candidatus Scalindua species in anammox community revealed in soils with different duration of rice paddy cultivation in Northeast China. Applied Microbiology and Biotechnology, 2013, 97(4): 1785–1798

[38] Rich J J, Dale O R, Song B, Ward B B. Anaerobic ammonium oxidation (anammox) in Chesapeake Bay sediments. Microbial Ecology, 2008, 55(2): 311–320

[39] Zhu G, Wang S, Wang Y, Wang C, Risgaard-Petersen N, Jetten M S, Yin C. Anaerobic ammonia oxidation in a fertilized paddy soil. The ISME Journal, 2011, 5(12): 1905–1912

[40] Li M, Cao H, Hong Y G, Gu J D. Seasonal dynamics of anammox bacteria in estuarial sediment of the Mai Po Nature Reserve revealed by analyzing the 16S rRNA and hydrazine oxidoreductase (hzo) genes. Microbes and Environments, 2011, 26(1): 15–22

[41] Sun W, Xu M Y, Wu W M, Guo J, Xia C Y, Sun G P, Wang A J. Molecular diversity and distribution of anammox community in sediments of the Dongjiang River, a drinking water source of Hong Kong. Journal of Applied Microbiology, 2014, 116(2): 464–476

[42] Moore T A. Detection of Anammox Bacteria in Ammonium-Contaminated Groundwater. Waterloo, Canada: University of Waterloo, 2011

[43] Zhao Y, Xia Y, Kana T M, Wu Y, Li X, Yan X. Seasonal variation and controlling factors of anaerobic ammonium oxidation in freshwater river sediments in the Taihu Lake region of China. Chemosphere, 2013, 93(9): 2124–2131

[44] Lee K H, Wang Y F, Zhang G X, Gu J D. Distribution patterns of ammonia-oxidizing bacteria and anammox bacteria in the freshwater marsh of Honghe wetland in Northeast China. Ecotoxicology (London, England), 2014, 23(10): 1930–1942

[45] Naeher S, Huguet A, Roose-Amsaleg C L, Laverman A M, Fosse C, Lehmann M F, Derenne S, Zopfi J. Molecular and geochemical constraints on anaerobic ammonium oxidation (anammox) in a riparian zone of the Seine Estuary (France). Biogeochemistry, 2015, 123(1–2): 237–250

[46] Bernard R J, Mortazavi B, Kleinhuizen A A. Dissimilatory nitrate reduction to ammonium (DNRA) seasonally dominates NO₃⁻ reduction pathways in an anthropogenically impacted sub-tropical coastal lagoon. Biogeochemistry, 2015, 125(1): 47–64

[47] Deng F, Hou L, Liu M, Zheng Y, Yin G, Li X, Lin X, Chen F, Gao J, Jiang X. Dissimilatory nitrate reduction processes and associated contribution to nitrogen removal in sediments of the Yangtze Estuary. Journal of Geophysical Research. Biogeosciences, 2015, 120(8): 1521–1531

[48] Long A, Heitman J, Tobias C, Philips R, Song B. Co-occurring anammox, denitrification, and codenitrification in agricultural soils. Applied and Environmental Microbiology, 2013, 79(1): 168–176

[49] Humbert S, Tarnawski S, Fromin N, Mallet M P, Aragno M, Zopfi J. Molecular detection of anammox bacteria in terrestrial ecosystems: Distribution and diversity. The ISME Journal, 2010, 4(3): 450–454

[50] Hu B L, Rush D, van der Biezen E, Zheng P, van Mullekom M, Schouten S, Sinninghe Damsté J S, Smolders A J, Jetten M S, Kartal B. New anaerobic, ammonium-oxidizing community enriched from peat soil. Applied and Environmental Microbiology, 2011, 77(3): 966–971

[51] Rysgaard S, Glud R N, Sejr M K, Blicher M E, Stahl H J. Denitrification activity and oxygen dynamics in Arctic sea ice. Polar Biology, 2008, 31(5): 527–537

[52] Byrne N, Strous M, Crépeau V, Kartal B, Birrien J L, Schmid M, Lesongeur F, Schouten S, Jaeschke A, Jetten M, Prieur D, Godfroy A. Presence and activity of anaerobic ammonium-oxidizing bacteria at deep-sea hydrothermal vents. The ISME Journal, 2009, 3(1): 117–123

[53] Jaeschke A, Op den Camp H J, Harhangi H, Klimiuk A, Hopmans E C, Jetten M S, Schouten S, Sinninghe Damsté J S. 16S rRNA gene and lipid biomarker evidence for anaerobic ammonium-oxidizing bacteria (anammox) in California and Nevada hot springs. FEMS Microbiology Ecology, 2009, 67(3): 343–350

[54] Hong Y G, Yin B, Zheng T L. Diversity and abundance of anammox bacterial community in the deep-ocean surface sediment from equatorial Pacific. Applied Microbiology and Biotechnology, 2011, 89(4): 1233–1241

[55] Thamdrup B, Dalsgaard T, Jensen M M, Ulloa O, Farias L, Escribano R. Anaerobic ammonium oxidation in the oxygen-deficient waters off northern Chile. Limnology and Oceanography, 2006, 51(5): 2145–2156

[56] Bulow S E, Rich J J, Naik H S, Pratihary A K, Ward B B. Denitrification exceeds anammox as a nitrogen loss pathway in the Arabian Sea oxygen minimum zone. Deep-sea Research. Part I, Oceanographic Research Papers, 2010, 57(3): 384–393

[57] Pitcher A, Villanueva L, Hopmans E C, Schouten S, Reichart G J, Sinninghe Damsté J S. Niche segregation of ammonia-oxidizing archaea and anammox bacteria in the Arabian Sea oxygen minimum zone. The ISME Journal, 2011, 5(12): 1896–1904

[58] Hamersley M R, Lavik G, Woebken D, Rattray J E, Lam P, Hopmans E C, Damste J S S, Kruger S, Graco M, Gutierrez D, Kuypers M M M. Anaerobic ammonium oxidation in the Peruvian oxygen minimum zone. Limnology and Oceanography, 2007, 52(3): 923–933

[59] Rysgaard S, Glud R N, Risgaard Petersen N, Dalsgaard T. Denitrification and anammox activity in Arctic marine sediments. Limnology and Oceanography, 2004, 49(5): 1493–1502

[60] Gihring T M, Lavik G, Kuypers M M M, Kostka J E. Direct determination of nitrogen cycling rates and pathways in Arctic fjord sediments (Svalbard, Norway). Limnology and Oceanography, 2010, 55(2): 740–752

[61] Bale N J, Villanueva L, Fan H, Stal L J, Hopmans E C, Schouten S, Sinninghe Damsté J S. Occurrence and activity of anammox bacteria in surface sediments of the southern North Sea. FEMS Microbiology Ecology, 2014, 89(1): 99–110

[62] Brandsma J, van de Vossenberg J, Risgaard-Petersen N, Schmid M C, Engström P, Eurenius K, Hulth S, Jaeschke A, Abbas B, Hopmans E C, Strous M, Schouten S, Jetten M S, Damsté J S. A multi-proxy study of anaerobic ammonium oxidation in marine sediments of the Gullmar Fjord, Sweden. Environmental Microbiology Reports, 2011, 3(3): 360–366

[63] Yang X R, Li H, Nie S A, Su J Q, Weng B S, Zhu G B, Yao H Y, Gilbert J A, Zhu Y G. Potential contribution of anammox to nitrogen loss from paddy soils in Southern China. Applied and Environmental Microbiology, 2015, 81(3): 938–947

[64] Nie S, Li H, Yang X, Zhang Z, Weng B, Huang F, Zhu G B, Zhu Y G. Nitrogen loss by anaerobic oxidation of ammonium in rice rhizosphere. The ISME Journal, 2015, 9(9): 2059–2067

[65] Shen L d, Zheng P h, Ma S j. Nitrogen loss through anaerobic ammonium oxidation in agricultural drainage ditches. Biology and Fertility of Soils, 2015, 52(2): 1–10

[66] Boog J, Nivala J, Aubron T, Wallace S, van Afferden M, Müller R A. Hydraulic characterization and optimization of total nitrogen removal in an aerated vertical subsurface flow treatment wetland. Bioresource Technology, 2014, 162(0): 166–174

[67] 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, Strous M. Linking ultrastructure and function in four genera of anaerobic ammonium-oxidizing bacteria: cell plan, glycogen storage, and localization of cytochrome C proteins. Journal of Bacteriology, 2008, 190(2): 708–717

[68] Rattray J E, van de Vossenberg J, Hopmans E C, Kartal B, van Niftrik L, Rijpstra W I C, Strous M, Jetten M S, Schouten S, Sinninghe Damsté J S. Ladderane lipid distribution in four genera of anammox bacteria. Archives of Microbiology, 2008, 190(1): 51–66

[69] 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, Jetten M S M. Linearly concatenated cyclobutane lipids form a dense bacterial membrane. Nature, 2002, 419(6908): 708–712

[70] 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, Strous M. Intracellular localization of membrane-bound ATPases in the compartmentalized anammox bacterium “Candidatus Kuenenia stuttgartiensis”. Molecular Microbiology, 2010, 77(3): 701–715

[71] van Teeseling M C F, Mesman R J, Kuru E, Espaillat A, Cava F, Brun Y V, VanNieuwenhze M S, Kartal B, van Niftrik L. Anammox Planctomycetes have a peptidoglycan cell wall. Nature Communications, 2015, 6(1): 1–6

[72] Schalk J, Oustad H, Kuenen J G, Jetten M S. The anaerobic oxidation of hydrazine: A novel reaction in microbial nitrogen metabolism. FEMS Microbiology Letters, 1998, 158(1): 61–67

[73] Jetten M S, Wagner M, Fuerst J, van Loosdrecht M, Kuenen G, Strous M. Microbiology and application of the anaerobic ammonium oxidation (“anammox”) process. Current Opinion in Biotechnology, 2001, 12(3): 283–288

[74] Oshiki M, Ali M, Shinyako-Hata K, Satoh H, Okabe S. Hydroxylamine-dependent anaerobic ammonium oxidation (anammox) by “Candidatus Brocadia sinica”. Environmental Microbiology, 2016, 18(9): 3133–3143

[75] Dietl A, Ferousi C, Maalcke W J, Menzel A, de Vries S, Keltjens J T, Jetten M S, Kartal B, Barends T R. The inner workings of the hydrazine synthase multiprotein complex. Nature, 2015, 527(7578): 394–397

[76] Jetten M S, Niftrik L, Strous M, Kartal B, Keltjens J T, Op den Camp H J. Biochemistry and molecular biology of anammox bacteria. Critical Reviews in Biochemistry and Molecular Biology, 2009, 44(2–3): 65–84

[77] van der Star W R, Dijkema C, de Waard P, Picioreanu C, Strous M, van Loosdrecht M C. An intracellular pH gradient in the anammox bacterium Kuenenia stuttgartiensis as evaluated by 31P NMR. Applied Microbiology and Biotechnology, 2010, 86(1): 311–317

[78] Strous M, Pelletier E, Mangenot S, Rattei T, Lehner A, Taylor M W, Horn M, Daims H, Bartol-Mavel D, Wincker P, Barbe V, Fonknechten N, Vallenet D, Segurens B, Schenowitz-Truong C, Médigue C, Collingro A, Snel B, Dutilh B E, Op den Camp H J, van der Drift C, Cirpus I, van de Pas-Schoonen K T, Harhangi H R, van Niftrik L, Schmid M, Keltjens J, van de Vossenberg J, Kartal B, Meier H, Frishman D, Huynen M A, Mewes H W, Weissenbach J, Jetten M S, Wagner M, Le Paslier D. Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature, 2006, 440(7085): 790–794

[79] Kartal B, Maalcke W J, de Almeida N M, Cirpus I, Gloerich J, Geerts W, Op den Camp H J, Harhangi H R, Janssen-Megens E M, Francoijs K J, Stunnenberg H G, Keltjens J T, Jetten M S, Strous M. Molecular mechanism of anaerobic ammonium oxidation. Nature, 2011, 479(7371): 127–130

[80] Gori F, Tringe S G, Kartal B, Marchiori E, Jetten M S M. The metagenomic basis of anammox metabolism in Candidatus “Brocadia fulgida”. Biochemical Society Transactions, 2011, 39(6): 1799–1804

[81] Hu Z, Speth D R, Francoijs K J, Quan Z X, Jetten M S. Metagenome analysis of a complex community reveals the metabolic blueprint of anammox bacterium “Candidatus Jettenia asiatica”. Frontiers in Microbiology, 2012, 3: 366

[82] Fuchsman C A, Rocap G. Whole-genome reciprocal BLAST analysis reveals that planctomycetes do not share an unusually large number of genes with Eukarya and Archaea. Applied and Environmental Microbiology, 2006, 72(10): 6841–6844

[83] De Clippeleir H, Defoirdt T, Vanhaecke L, Vlaeminck S E, Carballa M, Verstraete W, Boon N. Long-chain acylhomoserine lactones increase the anoxic ammonium oxidation rate in an OLAND biofilm. Applied Microbiology and Biotechnology, 2011, 90(4): 1511–1519

[84] Kartal B, Koleva M, Arsov R, van der Star W, Jetten M S, Strous M. Adaptation of a freshwater anammox population to high salinity wastewater. Journal of Biotechnology, 2006, 126(4): 546–553

[85] Kartal B, Rattray J, van Niftrik L A, van de Vossenberg J, Schmid M C, Webb R I, Schouten S, Fuerst J A, Damsté J S, Jetten M S, Strous M. Candidatus “Anammoxoglobus propionicus” a new propionate oxidizing species of anaerobic ammonium oxidizing bacteria. Systematic and Applied Microbiology, 2007, 30(1): 39–49

[86] Strous M, Kuenen J G, Jetten M S. Key physiology of anaerobic ammonium oxidation. Applied and Environmental Microbiology, 1999, 65(7): 3248–3250

[87] Sonthiphand P, Hall M W, Neufeld J D. Biogeography of anaerobic ammonia-oxidizing (anammox) bacteria. Frontiers in Microbiology, 2014, 5: 1–14

[88] Lam P, Jensen M M, Lavik G, McGinnis D F, Müller B, Schubert C J, Amann R, Thamdrup B, Kuypers M M. Linking crenarchaeal and bacterial nitrification to anammox in the Black Sea. Proceedings of the National Academy of Sciences of the United States of America, 2007, 104(17): 7104–7109

[89] Woebken D, Fuchs B M, Kuypers M M, Amann R. Potential interactions of particle-associated anammox bacteria with bacterial and archaeal partners in the Namibian upwelling system. Applied and Environmental Microbiology, 2007, 73(14): 4648–4657

[90] Sliekers A O, Haaijer S, Schmid M, Harhangi H, Verwegen K, Kuenen J G, Jetten M S. Nitrification and anammox with urea as the energy source. Systematic and Applied Microbiology, 2004, 27(3): 271–278

[91] Vázquez-Padín J, Mosquera-Corral A, Campos J L, Méndez R, Revsbech N P. Microbial community distribution and activity dynamics of granular biomass in a CANON reactor. Water Research, 2010, 44(15): 4359–4370

[92] van Kessel M A, Speth D R, Albertsen M, Nielsen P H, Op den Camp H J, Kartal B, Jetten M S, Lücker S. Complete nitrification by a single microorganism. Nature, 2015, 528(7583): 555–559

[93] Dalsgaard T, Thamdrup B, Farias L, Revsbech N P. Anammox and denitrification in the oxygen minimum zone of the eastern South Pacific. Limnology and Oceanography, 2012, 57(5): 1331–1346

[94] Du R, Cao S, Li B, Niu M, Wang S, Peng Y. Performance and microbial community analysis of a novel DEAMOX based on partial-denitrification and anammox treating ammonia and nitrate wastewaters. Water Research, 2017, 108: 46–56

[95] Zhang X, Zhang H, Ye C, Wei M, Du J. Effect of COD/N ratio on nitrogen removal and microbial communities of CANON process in membrane bioreactors. Bioresource Technology, 2015, 189: 302–308

[96] Okabe S, Oshiki M, Takahashi Y, Satoh H. N₂O emission from a partial nitrification-anammox process and identification of a key biological process of N₂O emission from anammox granules. Water Research, 2011, 45(19): 6461–6470

[97] Ding J, Fu L, Ding Z W, Lu Y Z, Cheng S H, Zeng R J. Environmental evaluation of coexistence of denitrifying anaerobic methane-oxidizing archaea and bacteria in a paddy field. Applied Microbiology and Biotechnology, 2015, 100(1): 1–8

[98] Kindaichi T, Yuri S, Ozaki N, Ohashi A. Ecophysiological role and function of uncultured Chloroflexi in an anammox reactor. Water Science and Technology, 2012, 66(12): 2556–2561

[99] Prokopenko M G, Hirst M B, De Brabandere L, Lawrence D J, Berelson W M, Granger J, Chang B X, Dawson S, Crane E J 3rd, Chong L, Thamdrup B, Townsend-Small A, Sigman D M. Nitrogen losses in anoxic marine sediments driven by Thioploca-anammox bacterial consortia. Nature, 2013, 500(7461): 194–198

Acknowledgements

This work was supported by National Natural Science Foundation of China (Grant No. 31470543), Natural Science Foundation of Heilongjiang Province (No. ZD201412) and Harbin Science and Technology Program (No. 2016RAXXJ010).

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