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

  • Dawen Gao
  • Xiaolong Wang
  • Hong Liang
  • Qihang Wei
  • Yuan Dou
  • Longwei Li
Review Article


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.


Anammox Metabolism Metagenome Ecological distribution Microbial interactions 



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).


  1. 1.
    Dalsgaard T, Thamdrup B, Canfield D E. Anaerobic ammonium oxidation (anammox) in the marine environment. Research in Microbiology, 2005, 156(4): 457–464CrossRefGoogle Scholar
  2. 2.
    Broda E. Two kinds of lithotrophs missing in nature. Zeitschrift fur allgemeine Mikrobiologie, 1977, 17(6): 491–493CrossRefGoogle Scholar
  3. 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): 177–184CrossRefGoogle Scholar
  4. 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): 1246–1251Google Scholar
  5. 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): 6817–6825CrossRefGoogle Scholar
  6. 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): 608–611CrossRefGoogle Scholar
  7. 7.
    Woebken D, Lam P, Kuypers M M, Naqvi SW, 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): 3106–3119CrossRefGoogle Scholar
  8. 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): 771–783CrossRefGoogle Scholar
  9. 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): 36–47CrossRefGoogle Scholar
  10. 10.
    van de Vossenberg J, Woebken D, Maalcke WJ, 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): 1275–1289CrossRefGoogle Scholar
  11. 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): 402–416CrossRefGoogle Scholar
  12. 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): 606–608CrossRefGoogle Scholar
  13. 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): 4752–4757CrossRefGoogle Scholar
  14. 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: 80–87CrossRefGoogle Scholar
  15. 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): 156–168CrossRefGoogle Scholar
  16. 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): 1660–1670Google Scholar
  17. 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): 6478–6483CrossRefGoogle Scholar
  18. 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): 153–161CrossRefGoogle Scholar
  19. 19.
    Schmid MC, 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): 1476–1484CrossRefGoogle Scholar
  20. 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): 1312–1318CrossRefGoogle Scholar
  21. 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): 413–420CrossRefGoogle Scholar
  22. 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): 577–589CrossRefGoogle Scholar
  23. 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): 111–120CrossRefGoogle Scholar
  24. 24.
    Kartal B, Kuypers MM, 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): 635–642CrossRefGoogle Scholar
  25. 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): 1857–1863CrossRefGoogle Scholar
  26. 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): 6829–6832CrossRefGoogle Scholar
  27. 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): 8834–8842CrossRefGoogle Scholar
  28. 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): 789–798CrossRefGoogle Scholar
  29. 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): 1237–1246CrossRefGoogle Scholar
  30. 30.
    Nicholls J C, Trimmer M. Widespread occurrence of the anammox reaction in estuarine sediments. Aquatic Microbial Ecology, 2009, 55(2): 105–113CrossRefGoogle Scholar
  31. 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: 9–19CrossRefGoogle Scholar
  32. 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): 238–245CrossRefGoogle Scholar
  33. 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): 316–319CrossRefGoogle Scholar
  34. 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): 571–582CrossRefGoogle Scholar
  35. 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): 1194–1207CrossRefGoogle Scholar
  36. 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): 2869–2883CrossRefGoogle Scholar
  37. 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): 1785–1798CrossRefGoogle Scholar
  38. 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): 311–320CrossRefGoogle Scholar
  39. 39.
    Zhu G, Wang S, Wang Y, Wang C, Risgaard-Petersen N, Jetten MS, Yin C. Anaerobic ammonia oxidation in a fertilized paddy soil. The ISME Journal, 2011, 5(12): 1905–1912Google Scholar
  40. 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): 15–22CrossRefGoogle Scholar
  41. 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): 464–476CrossRefGoogle Scholar
  42. 42.
    Moore T A. Detection of Anammox Bacteria in Ammonium-Contaminated Groundwater. Waterloo, Canada: University of Waterloo, 2011Google Scholar
  43. 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): 2124–2131CrossRefGoogle Scholar
  44. 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): 1930–1942CrossRefGoogle Scholar
  45. 45.
    Naeher S, Huguet A, Roose-Amsaleg C L, Laverman AM, 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): 237–250CrossRefGoogle Scholar
  46. 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): 47–64CrossRefGoogle Scholar
  47. 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): 1521–1531CrossRefGoogle Scholar
  48. 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): 168–176CrossRefGoogle Scholar
  49. 49.
    Humbert S, Tarnawski S, Fromin N, Mallet MP, Aragno M, Zopfi J. Molecular detection of anammox bacteria in terrestrial ecosystems: Distribution and diversity. The ISME Journal, 2010, 4(3): 450–454CrossRefGoogle Scholar
  50. 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 MS, Kartal B. New anaerobic, ammonium-oxidizing community enriched from peat soil. Applied and Environmental Microbiology, 2011, 77(3): 966–971CrossRefGoogle Scholar
  51. 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): 527–537CrossRefGoogle Scholar
  52. 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): 117–123CrossRefGoogle Scholar
  53. 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): 343–350CrossRefGoogle Scholar
  54. 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): 1233–1241CrossRefGoogle Scholar
  55. 55.
    Thamdrup B, Dalsgaard T, Jensen M M, Ulloa O, Farias L, Escribano R. Anaerobic ammonium oxidation in the oxygendeficient waters off northern Chile. Limnology and Oceanography, 2006, 51(5): 2145–2156CrossRefGoogle Scholar
  56. 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): 384–393CrossRefGoogle Scholar
  57. 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): 1896–1904Google Scholar
  58. 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): 923–933CrossRefGoogle Scholar
  59. 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): 1493–1502CrossRefGoogle Scholar
  60. 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): 740–752CrossRefGoogle Scholar
  61. 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): 99–110CrossRefGoogle Scholar
  62. 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): 360–366CrossRefGoogle Scholar
  63. 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): 938–947CrossRefGoogle Scholar
  64. 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): 2059–2067CrossRefGoogle Scholar
  65. 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): 1–10Google Scholar
  66. 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): 166–174CrossRefGoogle Scholar
  67. 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 MS M, Strous M. Linking ultrastructure and function in four genera of anaerobic ammoniumoxidizing bacteria: cell plan, glycogen storage, and localization of cytochrome C proteins. Journal of Bacteriology, 2008, 190(2): 708–717CrossRefGoogle Scholar
  68. 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): 51–66CrossRefGoogle Scholar
  69. 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): 708–712CrossRefGoogle Scholar
  70. 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): 701–715CrossRefGoogle Scholar
  71. 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): 1–6Google Scholar
  72. 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): 61–67CrossRefGoogle Scholar
  73. 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): 283–288CrossRefGoogle Scholar
  74. 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): 3133–3143CrossRefGoogle Scholar
  75. 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): 394–397CrossRefGoogle Scholar
  76. 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): 65–84CrossRefGoogle Scholar
  77. 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): 311–317CrossRefGoogle Scholar
  78. 78.
    Strous M, Pelletier E, Mangenot S, Rattei T, Lehner A, TaylorMW, 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): 790–794CrossRefGoogle Scholar
  79. 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): 127–130CrossRefGoogle Scholar
  80. 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): 1799–1804CrossRefGoogle Scholar
  81. 81.
    Hu Z, Speth D R, Francoijs K J, Quan Z X, Jetten MS. Metagenome analysis of a complex community reveals the metabolic blueprint of anammox bacterium “Candidatus Jettenia asiatica”. Frontiers in Microbiology, 2012, 3: 366CrossRefGoogle Scholar
  82. 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): 6841–6844CrossRefGoogle Scholar
  83. 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): 1511–1519CrossRefGoogle Scholar
  84. 84.
    Kartal B, Koleva M, Arsov R, van der Star W, Jetten MS, Strous M. Adaptation of a freshwater anammox population to high salinity wastewater. Journal of Biotechnology, 2006, 126(4): 546–553CrossRefGoogle Scholar
  85. 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): 39–49CrossRefGoogle Scholar
  86. 86.
    Strous M, Kuenen J G, Jetten M S. Key physiology of anaerobic ammonium oxidation. Applied and Environmental Microbiology, 1999, 65(7): 3248–3250Google Scholar
  87. 87.
    Sonthiphand P, Hall M W, Neufeld J D. Biogeography of anaerobic ammonia-oxidizing (anammox) bacteria. Frontiers in Microbiology, 2014, 5: 1–14CrossRefGoogle Scholar
  88. 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): 7104–7109CrossRefGoogle Scholar
  89. 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): 4648–4657CrossRefGoogle Scholar
  90. 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): 271–278CrossRefGoogle Scholar
  91. 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): 4359–4370CrossRefGoogle Scholar
  92. 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): 555–559CrossRefGoogle Scholar
  93. 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): 1331–1346CrossRefGoogle Scholar
  94. 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: 46–56CrossRefGoogle Scholar
  95. 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: 302–308CrossRefGoogle Scholar
  96. 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): 6461–6470CrossRefGoogle Scholar
  97. 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): 1–8Google Scholar
  98. 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): 2556–2561CrossRefGoogle Scholar
  99. 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, 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): 194–198CrossRefGoogle Scholar

Copyright information

© Higher Education Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Dawen Gao
    • 1
  • Xiaolong Wang
    • 1
  • Hong Liang
    • 1
  • Qihang Wei
    • 1
  • Yuan Dou
    • 1
  • Longwei Li
    • 1
  1. 1.State Key Laboratory of Urban Water Resource and EnvironmentHarbin Institute of TechnologyHarbinChina

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