Skip to main content
Log in

Nitrogen Cycle in Engineered and Natural Ecosystems—Past and Current

  • Water Pollution (S Sengupta and L Nghiem, Section Editors)
  • Published:
Current Pollution Reports Aims and scope Submit manuscript

Abstract

Due to modern urbanization and rapid population growth, the nitrogen cycle has been significantly disturbed within differing ecosystems. Focusing specifically on imbalances present in an aquatic ecosystem, it is imperative that the wastewater engineering community addresses the need to conserve energy and resources better by developing more effective tools for application in wastewater treatment plants. The Academy of Engineers recently identified nitrogen cycle management as one of the 14 predominant challenges that engineers need to be addressing in the immediate future. This validates a definite sense of urgency to find practical solutions for implementation in wastewater treatment plants. In order to determine the best means for effective nitrogen cycle management, an in-depth examination of disturbances in the cycle provide an understanding of what is needed to resolve these issues. This article provides an in-depth discussion of past research, developments found in present studies, as well as providing potential strategies for improving the future of nitrogen cycle management.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Abeling U, Seyfried CF. Anaerobic-aerobic treatment of high-strength ammonia wastewater-nitrogen removal via nitrite. Wat. Sci. Tech. 1992;26(5–6):1007–15.

    CAS  Google Scholar 

  2. Abeliovich A, Vonshak A. Anaerobic metabolism of Nitrosomonas europaea. Arch Microbiol. 1992;158:267–70.

    Article  CAS  Google Scholar 

  3. Ahn JH, Kim SP, Park HK, Rahm B, Pagilla K, Chandran K. N2O emissions from activated sludge processes, 2008-2009: results of a national monitoring survey in the United States. Environmental Science & Technology. 2010;44(12):4505–11.

    Article  CAS  Google Scholar 

  4. Aleem MIH, Hoch GE, Varner JE. Water as the source of oxidant and reductant in bacterial chemosynthesis. Proc NatlAcadSciUSA. 1965;54:869–73.

    Article  CAS  Google Scholar 

  5. Alinsafi A, Adouani N, Beline F, Lendormi T, Limousy L, Sire O. Nitrite effect on nitrous oxide emission from denitrifying activated sludge. Process Biochem. 2008;43:683–9.

    Article  CAS  Google Scholar 

  6. Allen MB, Van Niel CB. Experiments on bacterial denitrification. J Bacteriol. 1952;64(3):397.

    CAS  Google Scholar 

  7. Anderson J. The metabolisms of hydroxylamine to nitrite by Nitrosomonas europaea. Biochem J. 1964;91:8–17.

    Article  CAS  Google Scholar 

  8. Anderson KK, Hooper AB. O2 and H2O are each the source of one O in NO2 produced from NH3 by Nitrosomonas; 15N-NMR evidence. FEBS Lett. 1983;164:236–40.

    Article  Google Scholar 

  9. Andrews JH, Harris RF. R- and K-selection and microbial ecology. In: Marshall KC, editor. Advances in microbial ecology. New York: Plenum Press; 1986.

    Google Scholar 

  10. Anthonisen AC. Inhibition of nitrification by ammonia and nitrous acid. JWPCF. 1976;48(5):835–52.

    CAS  Google Scholar 

  11. Arai H, Igarashi Y, Kodama T. Expression of the nir and nor genes for denitrification of Pseudomonas aeruginosa requires a novel CRP/FNR-related transcriptional regulator, DNR, in addition to ANR. FEBS Lett. 1995;371:73–6.

    Article  CAS  Google Scholar 

  12. Arciero DM, Hooper AB. Hydroxylamine oxidoreductase from Nitrosomonas europaea is a multimer of an octa-heme subunit. J Biol Chem. 1993;268(20):14645–54.

    CAS  Google Scholar 

  13. Arp DJ, Bottomley PJ. Nitrifers: more than 100 years from isolation to genome sequences. Microbe-American Society for microbiology. 2006;1(5):229.

    Google Scholar 

  14. Bai Y, Sun Q, Wen D, Tang X. Abundance of ammonia-oxidizing bacteria and archaea in industrial and domestic wastewater treatment systems. FEMS Microbiol Ecol. 2012;80(2):323–30.

    Article  CAS  Google Scholar 

  15. Beijerinck MW. Ueber die Bakterien, welche sich im Dunkeln mit Kohlensa hren ko $ nnen. Centralbl Bakteriol Parasitenkd Infektionskr Hyg Abt II. 1904;11:593-599.

  16. Bergmann DJ, Arciero DM, Hooper AB. Organization of the hao gene cluster of Nitrosomonas europaea: genes for two tetraheme c cytochromes. J Bacteriol. 1994;176(11):3148–53.

    Article  CAS  Google Scholar 

  17. Berks BC, Ferguson SJ, Moir JW, Richardson DJ. Enzymes and associated electron transport systems that catalyse the respiratory reduction of nitrogen oxides and oxyanions. Biochimica et Biophysica Acta (BBA)-Bioenergetics. 1995;1232(3):97–173.95.

    Article  Google Scholar 

  18. Bhattacharjee AS, Motlagh AM, Jetten MS, Goel R. Methane dependent denitrification-from ecosystem to laboratory-scale enrichment for engineering applications. Water Res. 2016;99:244–52.

    Article  CAS  Google Scholar 

  19. Bock E, Koops H-P, Ahlers B, Harms H. Oxidation of inorganic nitrogen compounds as energy source. In: Balows H, Trüper HG, Dworkin M, Harder W, Schleifer K-H, editors. The prokaryotes. 2nd ed. New York, N.Y: Springer Verlag; 1992. p. 414–30.

    Google Scholar 

  20. Bock E, Schmidt I, Stuven R, Zart D. Nitrogen loss caused by denitrifying Nitrosomonas cells using ammonium or hydrogen as electron donors and nitrite as electron acceptor. Arch Microbiol. 1996;163:16–20.

    Article  Google Scholar 

  21. Bollmann A, Bär-Gilissen MJ, Laanbroek HJ. Growth at low ammonium concentrations and starvation response as potential factors involved in niche differentiation among ammonia-oxidizing bacteria. Appl Environ Microbiol. 2002;68(10):4751–7.

    Article  CAS  Google Scholar 

  22. Bollmann A, Laanbroek HJ. Continuous culture enrichments of ammonia-oxidizing bacteria at low ammonium concentrations. FEMS Microbiol Ecol. 2001;37(3):211–21.

    Article  CAS  Google Scholar 

  23. Braker G, Fesefeldt A, Witzel KP. Development of PCR primer systems for amplification of nitrite reductase genes (nirK and nirS) to detect denitrifying bacteria in environmental samples. Appl Environ Microbiol. 1998;64:3769–75.

    CAS  Google Scholar 

  24. Braker G, Tiedje JM. Nitric oxide reductase (norB) genes from pure cultures and environmental samples. Appl Environ Microbiol. 2003;69(6):3476–83.

    Article  CAS  Google Scholar 

  25. Braun C, Zumft WG. The structural genes of the nitric oxide reductase complex from pseudomonas stutzeri are part of a 30-kilobase gene cluster for denitrification. J Bacteriol. 1992;174:2394–7.

    Article  CAS  Google Scholar 

  26. Broda E. Two kinds of lithotrophs missing in nature. Zeitschrift für allgemeine Mikrobiologie. 1977;17(6):491–3.

    Article  CAS  Google Scholar 

  27. Brouwer M, Van Loosdrecht MCM, Heijnen JJ. One reactor system for ammonium removal via nitrite. STOWA report. 1996; pp. 96–01.

  28. Bru D, Sarr A, Philippot L. Relative abundances of proteobacterial membrane-bound and periplasmic nitrate reductases in selected environments. Appl Environ Microbiol. 2007;73:5971–4.

    Article  CAS  Google Scholar 

  29. Burford JR, Bremner JM. Relationships between the denitrification capacities of soils and total, water-soluble and readily decomposable soil organic matter. Soil Biol Biochem. 1975;7:389–94.

    Article  CAS  Google Scholar 

  30. Camargo JA, Alonso Á. Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: a global assessment. Environ Int. 2006;32(6):831–49.

    Article  CAS  Google Scholar 

  31. Canfield DE, Glazer AN, Falkowski PG. The evolution and future of Earth’s nitrogen cycle. Science. 2010;330(6001):192–6.

    Article  CAS  Google Scholar 

  32. Capone DG, Popa R, Flood B, Nealson KH. Follow the nitrogen. Atmosphere. 2006;1:2–5.

    Google Scholar 

  33. Cecen F, Gonenc IE. Nitrogen removal characteristics of nitrification and denitrification filters. Wat. Sci. Tech. 1994;29(10–11):409–16.

    CAS  Google Scholar 

  34. Chamchoi N, Nitisoravut S, Schmidt JE. Inactivation of ANAMMOX communities under concurrent operation of anaerobic ammonium oxidation (ANAMMOX) and denitrification. Bioresour Technol. 2008;99:3331–6.

    Article  CAS  Google Scholar 

  35. Chandran K, Stein LY, Klotz MG, van Loosdrecht MCM. Nitrous oxide production by lithotrophic ammonia oxidizing bacteria and implications for engineered nitrogen removal systems. Biochem Soc Trans. 2011;39(6):1832–7.

    Article  CAS  Google Scholar 

  36. Cole JA. Assimilatory and dissimilatory reduction of nitrate to ammonia. Symp Soc Gen Microbiol. 1988;42:281–329.

    Google Scholar 

  37. Colliver BB, Stephenson T. Production of nitrogen oxide and dinitrogen oxide by autotrophic nitrifiers. Biotechnol Adv. 2000;18(3):219–32.

    Article  CAS  Google Scholar 

  38. Costa E, Pérez J, Kreft JU. Why is metabolic labour divided in nitrification? Trends Microbiol. 2006;14(5):213–9.

    Article  CAS  Google Scholar 

  39. Daims H, Lebedeva EV, Pjevac P, Han P, Herbold C, Albertsen M, et al. Complete nitrification by Nitrospira bacteria. Nature. 2015;528(7583):504–9.

    CAS  Google Scholar 

  40. Daims H, Lücker S, Wagner M. A new perspective on microbes formerly known as nitrite-oxidizing bacteria. Trends Microbiol. 2016;24(9):699–712.

  41. Daims H, Nielsen PH, Nielsen JL, Juretschko S, Wagner M. Novel Nitrospira-like bacteria as dominant nitrite-oxidizers in biofilms from wastewater treatment plants: diversity and in situ physiology. Water Sci.Technol. 2000;41:85–90.

    CAS  Google Scholar 

  42. Daims H, Nielsen JL, Nielsen PH, Schleifer KH, Wagner M. In situ characterization of Nitrospira-like nitrite-oxidizing bacteria active in wastewater treatment plants. Appl Environ Microbiol. 2001;67(11):5273–84.

    Article  CAS  Google Scholar 

  43. Dapena-Mora A, Campos JL, Mosquera-Corral A, Jetten MSM, Méndez R. Stability of the ANAMMOX process in a gas-lift reactor and a SBR. J Biotechnol. 2004;110(2):159–70.

    Article  CAS  Google Scholar 

  44. Desloover J, De Clippeleir H, Boeckx P, Du Laing G, Colsen J, Verstraete W, et al. Floc-based sequential partial nitritation and anammox at full scale with contrasting N 2 O emissions. Water Res. 2011;45(9):2811–21.

    Article  CAS  Google Scholar 

  45. Deutzmann JS, Wörner S, Schink B. Activity and diversity of methanotrophic bacteria at methane seeps in eastern Lake Constance sediments. Appl Environ Microbiol. 2011;77(8):2573–81.

    Article  CAS  Google Scholar 

  46. Dionisi HM, Layton AC, Harms G, Gregory IR, Robinson KG, Sayler GS. Quantification of Nitrosomonas oligotropha-like ammonia-oxidizing bacteria and Nitrospira spp. from full-scale wastewater treatment plants by competitive PCR. Appl Environ Microbiol. 2002;68:245–53.

    Article  CAS  Google Scholar 

  47. Dosta J, Fernandez I, Vazquez-Padin JR, Mosquera-Coral A, Campos JL, Mata-Alvarez J, et al. Short and long term effects of temperature on the anammox process. J Hazard Mater. 2007;154:688–93.

    Article  CAS  Google Scholar 

  48. Egli K, Fanger U, Alvarez PJJ, Siegrist H, Van der Meer JR, Zehnder AJB. Enrichment and characterization of an anammox bacterium from a rotating biological contactor treating ammonium-rich leachate. Arch Microbiol. 2001;175:198–207.

    Article  CAS  Google Scholar 

  49. Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W. Environmental factors shaping the ecological niches of ammonia-oxidizing archaea. FEMS Microbiol Rev. 2009;33(5):855–69.

    Article  CAS  Google Scholar 

  50. Ettwig KF, Butler MK, Le Paslier D, Pelletier E, Mangenot S, Kuypers MM, et al. Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature. 2010;464(7288):543–8.

    Article  CAS  Google Scholar 

  51. Ettwig KF, van Alen T, van de Pas-Schoonen KT, Jetten MS, Strous M. Enrichment and molecular detection of denitrifying methanotrophic bacteria of the NC10 phylum. Appl Environ Microbiol. 2009;75:3656–62.

    Article  CAS  Google Scholar 

  52. Fernández I, Vázquez-Padín JR, Mosquera-Corral A, Campos JL, Méndez R. Biofilm and granular systems to improve anammox biomass retention. Biochem Eng J. 2008;42(3):308–13.

    Article  CAS  Google Scholar 

  53. Focht DD, Chang AC. Nitrification and denitrification process related to wastewater treatment. AdvApplMicrobiol. 1975;19:153–86.

    CAS  Google Scholar 

  54. Francis C, Mankin J. High nitrate denitrification in continuous flow-stirred reactors. Water Res. 1977;11:289–94.

    Article  CAS  Google Scholar 

  55. Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, et al. Nitrogen cycles: past, present, and future. Biogeochemistry. 2004;70(2):153–226.

    Article  CAS  Google Scholar 

  56. Gejlsbjerg B, Frette L, Westermann P. Dynamics of N2O production from activated sludge. Water Res. 1998;32:2113–21.

    Article  CAS  Google Scholar 

  57. Gieseke A, Purkhold U, Wagner M, Amann R, Schramm A. Community structure and activity dynamics of nitrifying bacteria in a phosphate-removing biofilm. Appl Environ Microbiol. 2001;67:1351–62.

    Article  CAS  Google Scholar 

  58. Glass C, Silverstein J, Oh J. Inhibition of denitrification in activated sludge by nitrite. Water Environ Res. 1997;69(6):1086–93.

    Article  CAS  Google Scholar 

  59. Goreau TJ, Kaplan WA, Wofsy SC, McElroy MB, Valois FW, Watson SW. Production of NO2 and N2O by nitrifying bacteria at reduced concentrations of oxygen. Appl Environ Microbiol. 1980;40:526–32.

    CAS  Google Scholar 

  60. van de Graaf AA, Bruijn P, Robertson LA, Jetten MSM, Kuenen JG. Autotrophic growth of anaerobic, ammonium-oxidising microorganisms in a fluidized bed reactor. Microbiology (UK). 1996;142:2187–96.

    Article  Google Scholar 

  61. Gruber-Dorninger C, Pester M, Kitzinger K, Savio DF, Loy A, Rattei T, et al. Functionally relevant diversity of closely related Nitrospira in activated sludge. The ISME journal. 2015;9(3):643–55.

    Article  CAS  Google Scholar 

  62. Gubry-Rangin C, Hai B, Quince C, Engel M, Thomson BC, James P, et al. Niche specialization of terrestrial archaeal ammonia oxidizers. Proc Natl Acad Sci. 2011;108(52):21206–11.

    Article  CAS  Google Scholar 

  63. Hanaki K, Hong Z, Matsuo T. Production of nitrous oxide gas during denitrification of wastewater. Water Sci Technol. 1992;26(5–6):1027–36.

    CAS  Google Scholar 

  64. Hao, X., Heijnen, J.J., Van Loosdrechy, M.C.M. Sensitivity analysis of a biofilm model describing a one stage completely autotrophic nitrogen removal (CANON) process. Biotechnology and Bioengineering, 2001 Vol 77, No. 3.

  65. Haroon MF, Hu S, Shi Y, Imelfort M, Keller J, Hugenholtz P, et al. Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature. 2013;500(7464):567–70.

    Article  CAS  Google Scholar 

  66. Hellinga C, Schellen AAJC, Mulder JW, Van Loosdrecht MCM, Heijnen JJ. The SHARON process: an innovative method for nitrogen removal from ammonium-rich waste water. Water Sci.Technol. 1998;37:135–42.

    Article  CAS  Google Scholar 

  67. Helmer C, Kunst S, Juretschko S, Schmid MC, Schleifer KH, Wagner M. Nitrogen loss in a nitrifying biofilm system. Water SciTechnol. 1998;39:13–21.

    Google Scholar 

  68. Helmer C, Tromm C, Hippen A, Rosenwinkel KH, Seyfried CF, Kunst S. Single stage biological nitrogen removal by nitritation and anaerobic ammonium oxidation in biofilm systems. Water Sci.Technol. 2001;43:311–20.

    CAS  Google Scholar 

  69. Hendrickx TL, Wang Y, Kampman C, Zeeman G, Temmink H, Buisman CJ. Autotrophic nitrogen removal from low strength waste water at low temperature. Water Res. 2012;46(7):2187–93.

    Article  CAS  Google Scholar 

  70. Henry S, Baudoin E, López-Gutiérrez JC, Martin-Laurent F, Brauman A, et al. Quantification of denitrifying bacteria in soils by nirK gene targeted real-time PCR. J Microbiol Methods. 2004;59:327–35.

    Article  CAS  Google Scholar 

  71. Hippen A, Rosenwinkel KH, Baumgarten G, Seyfried CF. Aerobic deammonification: a new experience in the treatment of wastewaters. Wat. Sci. Tech. 1997;35(10):111–20.

    Article  CAS  Google Scholar 

  72. Holloway P, McCormick W, Watson RJ, Chan Y-K. Identification and analysis of the dissimilatory nitrous oxide reduction genes, nosRZDFY, of Rhizobium meliloti. J Bacteriol. 1996;178:1505–14.

    Article  CAS  Google Scholar 

  73. Hooper AB, Terry KR. Hydroxylamine oxidoreductase of Nitrosomonas: production of nitric oxide from hydroxylamine. Biochimica et Biophysica Acta (BBA) -Enzymology. 1979;571(1):12–20.

    Article  CAS  Google Scholar 

  74. Hu S, Zeng RJ, Burow LC, Lant P, Keller J, Yuan Z. Enrichment of denitrifying anaerobic methane oxidizing microorganisms. Environ Microbiol Rep. 2009;1:377–84.

    Article  CAS  Google Scholar 

  75. Hunik, JH, Engineering aspects of nitrification with immobilized cells. PhD Thesis, Wageningen Agricultural University, The Netherlands; 1993.

  76. Hwang C, Wu WM, Gentry TJ, Carley J, Carroll SL, Schadt C, et al. Changes in bacterial community structure correlate with initial operating conditions of a field-scale denitrifying fluidized bed reactor. Appl Microbiol Biotechnol. 2006;71(5):748–60.

    Article  CAS  Google Scholar 

  77. Hyman MR, Arp DJ. 14C2H2 and 14CO2-labeling studies of the de novo synthesis of polypeptides by Nitrosomonas europaea during recovery from acetylene and light inactivation of ammonia monooxygenase. J Biol Chem. 1992;267:1534–45.

    CAS  Google Scholar 

  78. Hyman MR, Wood PM. Suicidal inactivation and labelling of ammonia monooxygenase by acetylene. Biochem J. 1985;227:719–25.

    Article  CAS  Google Scholar 

  79. Inamori R, Gui P, Dass P, Matsumura M, Xu KQ, Kondo T. Investigating CH4 and N2O emissions from eco-engineering wastewater treatment processes using constructed wetland microcosms. Process Biochem. 2007;20(42):363–73.

    Article  CAS  Google Scholar 

  80. Islas-Lima S, Thalasso F, Gomez-Hernandez J. Evidence of anoxic methane oxidation coupled to denitrification. Water Res. 2004;38(1):13–6.

    Article  CAS  Google Scholar 

  81. Isaka K, Sumino T, Tsuneda S. High nitrogen removal performance at moderately low temperature utilizing anaerobic ammonium oxidation reactions. J Biosci Bioeng. 2007;103:486–90.

    Article  CAS  Google Scholar 

  82. Jeanningros Y, Vlaeminck SE, Kaldate A, Verstraete W, Graveleau L. Fast start-up of a pilot-scale deammonification sequencing batch reactor from an activated sludge inoculum. Water Sci Technol. 2010;61(6):1393–400.

    Article  CAS  Google Scholar 

  83. Jenni S, Vlaeminck SE, Morgenroth E, Udert KM. Successful application of nitritation/anammox to wastewater with elevated organic carbon to ammonia ratios. Water Res. 2013;49:316–26.

    Article  CAS  Google Scholar 

  84. Jetten MSM, Horn SJ, van Loosdrecht MCM. Towards a more sustainable municipal wastewater treatment system. Wat. Sci. Tech. 1997;35(9):171–80.

    Article  CAS  Google Scholar 

  85. Jetten MSM, Strous M, van de Pas-Schoonen KT, Schalk J, van Dongen L, et al. The anaerobic oxidation of ammonium. FEMS Microbiol Reviews. 1998;22:421–37.

    Article  CAS  Google Scholar 

  86. Joss A, Salzgeber D, Eugster J, König R, Rottermann K, Burger S, et al. Full-scale nitrogen removal from digester liquid with partial nitritation and anammox in one SBR. Environmental Science & Technology. 2009;43(14):5301–6.

    Article  CAS  Google Scholar 

  87. Juretschko S, Timmermann G, Schmid M, Schleifer KH, Pommerening-Roser A, et al. Combined molecular and conventional analyses of nitrifying bacterium diversity in activated sludge—Nitrosococcus mobilis and Nitrospira-like bacteria as dominant populations. Appl Environ Microbiol. 1998;64:3042–51.

    CAS  Google Scholar 

  88. Kalyuhznaya MG, Martens-Habbena W, Wang T, Hackett M, Stolyar SM, Stahl DA, et al. Methylophilaceae link methanol oxidation to denitrification in freshwater lake sediment as suggested by stable isotope probing and pure culture analysis. Environ Microbiol Rep. 2009;1(5):385–92.

    Article  CAS  Google Scholar 

  89. Kampman C, Hendrickx TL, Luesken FA, van Alen TA, den Camp HJO, Jetten MS, et al. Enrichment of denitrifying methanotrophic bacteria for application after direct low-temperature anaerobic sewage treatment. J Hazard Mater. 2012;227:164–71.

    Article  CAS  Google Scholar 

  90. Kampschreur MJ, Tan NCG, Picioreanu C, Jetten MSM, Schmidt I, Van Loosdrecht MCM. Role of nitrogen oxides in the metabolism of ammonia-oxidizing bacteria. Biochem Soc Trans. 2006;34(1):179–81.

    Article  CAS  Google Scholar 

  91. Kampschreur MJ, Tan NCG, Kleerebezem R, Picioreanu C, Jetten MSM, van Loosdrecht MCM. Effect of dynamic process conditions on nitrogen oxides emission from a nitrifying culture. Environ Sci Technol. 2008a;42(2):429–35.

    Article  CAS  Google Scholar 

  92. Kampschreur MJ, van der Star WRL, Wielders HA, Mulder JW, Jetten MSM, van Loosdrecht MCM. Dynamics of nitric oxide and nitrous oxide emission during full-scale reject water treatment. Water Res. 2008b;42(3):812–26.

    Article  CAS  Google Scholar 

  93. Kampschreur MJ, Temmink H, Kleerebezem R, Jetten MSM, Van Loosdrecht MCM. Nitrous oxide emission during wastewater treatment. Water Res. 2009;43:4093–103.

    Article  CAS  Google Scholar 

  94. Kartal B, Kuenen JG, van Loosdrecht MCM. Sewage treatment with anammox. Science. 2010;328:702–3.

    Article  CAS  Google Scholar 

  95. Kester RA, De Boer W, Laanbroek HJ. Production of NO and N2O by pure cultures of nitrifying and denitrifying bacteria during changes in aeration. Appl Environ Microbiol. 1997;63:3872–7.

    CAS  Google Scholar 

  96. Khan ST, Hiraishi A. Isolation and characterization of a new poly (3-hydroxybutyrate)-degrading, denitrifying bacterium from activated sludge. FEMS Microbiol Lett. 2001;205(2):253–7.

    Article  Google Scholar 

  97. Koch G, Egli K, Van Der Meer JR, Siegrist H. Mathematical modeling of autotrophic denitrification in a nitrifying biofilm of a rotating biological contracter. Water Science & Technology. 2000;41:191.

    CAS  Google Scholar 

  98. Könneke M, Bernhard AE, José R, Walker CB, Waterbury JB, Stahl DA. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature. 2005;437(7058):543–6.

    Article  CAS  Google Scholar 

  99. Koops HP, Böttcher B, Möller UC, Pommerening-Röser A, Stehr G. 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. Microbiology. 1991;137(7):1689–99.

    CAS  Google Scholar 

  100. Koops HP, Pommerening-Röser. Distribution and ecophysiology of the nitrifying bacteria emphasizing cultured species. FEMS Microbiol Ecol. 2001;37(1):1–9.

    Article  CAS  Google Scholar 

  101. Körner H, Zumft WG. Expression of denitrification enzymes in response to the dissolved oxygen level and respiratory substrate in continuous culture of Pseudomonas stutzeri. Appl Environ Microbiol. 1989;55(7):1670–6.

  102. Kuai LP, Verstraete W. Autotrophic denitrification with elemental Sulphur in small-scale wastewater treatment facilities. Environ Technol. 1998;20(2):201–9.

    Article  Google Scholar 

  103. Lackner S, Terada A, Smets BF. Heterotrophic activity compromises autotrophic nitrogen removal in membraneaerated biofilms: results of a modeling study. Water Res. 2008;42(4–5):1102–12.

    Article  CAS  Google Scholar 

  104. Laureni M, Falas P, Robin O, Wick A, Weissbrodt DG, Nielsen JL, et al. Mainstream partial nitritation and anammox: long term process stability and effluent quality at low temperatures. Water Res. 2016;101:628–39.

    Article  CAS  Google Scholar 

  105. Law Y, Ni BJ, Lant P, Yuan Z. N2O production rate of an enriched ammonia-oxidizing bacteria culture exponentially correlates to its ammonia oxidation rate. Water Res. 2012;46:3409–19.

    Article  CAS  Google Scholar 

  106. Limpiyakorn T, Sonthiphand P, Rongsayamanont C, Polprasert C. Abundance of amoA genes of ammonia-oxidizing archaea and bacteria in activated sludge of full-scale wastewater treatment plants. Bioresour Technol. 2011;102(4):3694–701.

    Article  CAS  Google Scholar 

  107. Lindsay MR, Webb RI, Strous M, Jetten MS, Butler MK, Forde RJ, et al. Cell compartmentalisation in planctomycetes: novel types of structural organisation for the bacterial cell. ArchMicrobiol. 2001;175:413–29.

    CAS  Google Scholar 

  108. Logemann S, Schantl J, Bijvank S, Van Loosdrecht MCM, Kuenen JG, Jetten M. Molecular microbial diversity in a nitrifying reactor system without sludge retention. FEMS MicrobiolEcol. 1998;27:239–49.

    Article  CAS  Google Scholar 

  109. Luesken FA, Sánchez J, Van Alen TA, Sanabria J, den Camp HJO, Jetten MS, et al. Simultaneous nitrite-dependent anaerobic methane and ammonium oxidation processes. Appl Environ Microbiol. 2011;77(19):6802–7.

    Article  CAS  Google Scholar 

  110. Luo Y, Su BO, Currie WS, Dukes JS, Finzi A, Hartwig U, et al. Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience. 2004;54(8):731–9.

    Article  Google Scholar 

  111. Ma B, Zhang S, Zhang L, Yi P, Wang J, Wang S, et al. The feasibility of using a two-stage autotrophic nitrogen removal process to treat sewage. Bioresour Technol. 2011;102(17):8331–4.

    Article  CAS  Google Scholar 

  112. Martens-Habbena W, Berube PM, Urakawa H, José R, Stahl DA. Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature. 2009;461(7266):976–9.

    Article  CAS  Google Scholar 

  113. Matějů V, Čižinská S, Krejčí J, Janoch T. Biological water denitrification—a review. Enzym Microb Technol. 1992;14(3):170–83.

    Article  Google Scholar 

  114. Mauret M, Paul E, Puech-Costes E, Maurette MT, Baptiste P. Application of experimental research methodology to the study of nitrification in mixed culture. Wat. Sci. Tech. 1996;34(1–2):245–52.

    Article  CAS  Google Scholar 

  115. Miyahara M, Kim SW, Fushinobu S, Takaki K, Yamada T, Watanabe A, et al. Potential of aerobic denitrification by Pseudomonas stutzeri TR2 to reduce nitrous oxide emissions from wastewater treatment plants. Applied and Environmental Microbiology, July. 2010;2010:4619–25.

    Article  CAS  Google Scholar 

  116. Modin O, Fukushi K, Yamamoto K. Denitrification with methane as external carbon source. Water Res. 2007;41(12):2726–38.

    Article  CAS  Google Scholar 

  117. Mohan SB, Schmid M, Jetten M, Cole J. Detection and widespread distribution of the nrfA gene encoding nitrite reduction to ammonia, a short circuit in the biological nitrogen cycle that competes with denitrification. FEMS Microbiol Ecol. 2004;49(3):433–43.

    Article  CAS  Google Scholar 

  118. Montoya JP, Holl CM, Zehr JP, Hansen A, Villareal TA, Capone DG. High rates of N2 fixation by unicellular diazotrophs in the oligotrophic Pacific Ocean. Nature. 2004;430(7003):1027–32.

    Article  CAS  Google Scholar 

  119. Moreno-Vivián C, Ferguson SJ. Definition and distinction between assimilatory, dissimilatory and respiratory pathways. Mol Microbiol. 1998;29(2):664–6.

    Article  Google Scholar 

  120. Mosquera-Corral A, Gonzalez F, Campos JL, Mendez R. Partial nitrification in a SHARON reactor in the presence of salts and organic carbon compounds. Process Biochem. 2005;40(9):3109–18.

    Article  CAS  Google Scholar 

  121. Mulder A, Graaf A, Robertson LA, Kuenen JG. Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor. FEMS Microbiol Ecol. 1995;16(3):177–84.

    Article  CAS  Google Scholar 

  122. NAE, 2008. Grand challenges for engineering. http://www.engineeringchallenges.org/ (accessed 10.11.09.)

  123. Nair RR, Dhamole PB, Lele SS, D’Douza SF. Biological denitrification of high strength nitrate waste using preadapted denitrifying sludge. Chemosphere. 2007;67:1612–7.

    Article  CAS  Google Scholar 

  124. Nikolaev YA, Kozlov MN, Kevbrina MV, Dorofeev AG, Pimenov NV, Kallistova AY, et al. Candidatus “Jettenia moscovienalis” sp. nov., a new species of bacteria carrying out anaerobic ammonium oxidation. Mikrobiologiya. 2014;84(2):236–43.

    Google Scholar 

  125. Okabe S, Satoh H, Watanabe Y. In situ analysis of nitrifying biofilms as determined by in situ hybridization and the use of microelectrodes. Appl Environ Microbiol. 1999;65(7):3182–91.

    CAS  Google Scholar 

  126. Paredes, D., Kuschk, P., Mbwette, T.S.A., Stange, F., Muller, R.A., Koser, H. New aspects of microbial nitrogen transformations in the context of wastewater treatment—a review. 2007.

  127. Park HD, Wells GF, Bae H, Criddle CS, Francis CA. Occurrence of ammonia-oxidizing archaea in wastewater treatment plant bioreactors. Appl Environ Microbiol. 2006;72(8):5643–7.

    Article  CAS  Google Scholar 

  128. Peng L, Ni BJ, Law Y, Yuan Z. Modeling of N2O production by ammonia oxidizing bacteria: integration of catabolism and anabolism. In: The 9th IWA Symposium on Systems Analysis and Integrated Assessment (Watermatex 2015), Gold Coast, Australia, 2015a. June 14–17.

  129. Peng L, Ni BJ, Ye L, Yuan Z. Selection of mathematical models for N2O production by ammonia oxidizing bacteria under varying dissolved oxygen and nitrite concentrations. Chem Eng J. 2015b;281:661–8.

    Article  CAS  Google Scholar 

  130. Pester M, Maixner F, Berry D, Rattei T, Koch H, Lücker S, et al. NxrB encoding the beta subunit of nitrite oxidoreductase as functional and phylogenetic marker for nitrite-oxidizing Nitrospira. Environ Microbiol. 2014;16(10):3055–71.

    Article  CAS  Google Scholar 

  131. Peu P, Béline F, Picard S, Héduit A. Measurement and quantification of nitrous oxide emissions from municipal activated sludge plants in France, Beijing, China: IWA World Water Congress; 2006, 10–14 September.

  132. Piña-Ochoa E, Høgslund S, Geslin E, Cedhagen T, Revsbech NP, Nielsen LP, et al. Widespread occurrence of nitrate storage and denitrification among Foraminifera and Gromiida. Proc Natl Acad Sci. 2010;107(3):1148-53.

  133. Pinto AJ, Marcus DN, Ijaz UZ, Bautista-de lose Santos QM, Dick GJ, Raskin L. Metagenomic evidence for the presence of comammox Nitrospira-like bacteria in a drinking water system. mSphere. 2016;1(1):e00054–15.

    Article  Google Scholar 

  134. Poughon L, Dussap C-G, Gros J-B. Energy model and metabolic flux analysis for autotrophic nitrifiers. Biotechnology & Bioengineering. 2000;72:416–33.

    Article  Google Scholar 

  135. Prosser JI. Autotrophic nitrification in bacteria. Adv Microb Physiol. 1989;30:125–81.

    Article  CAS  Google Scholar 

  136. Purkhold U, Pommerening-Roser A, Juretschko S, Schmid MC, Koops HP, Wagner M. Phylogeny of all recognized species of ammonia oxidizers based on comparative 16S rRNA and amoA sequence analysis: implications for molecular diversity surveys. Appl Environ Microbiol. 2000;66:5368–82.

    Article  CAS  Google Scholar 

  137. Quinlan AV. Optimum temperature shift for Nitrobacter winogradskyi: effect of dissolved oxygen and nitrite concentrations. Wat Res. 1986;20(5):611–7.

    Article  CAS  Google Scholar 

  138. Rabus R, Widdel F. Anaerobic degradation of ethylbenzene and other aromatic hydrocarbons by new denitrifying bacteria. Arch Microbiol. 1995;163(2):96–103.

    Article  CAS  Google Scholar 

  139. Raghoebarsing AA, Pol A, Van de Pas-Schoonen KT, Smolders AJ, Ettwig KF, Rijpstra WIC, et al. A microbial consortium couples anaerobic methane oxidation to denitrification. Nature. 2006;440(7086):918–21.

    Article  CAS  Google Scholar 

  140. Rütting T, Boeckx P, Müller C, Klemedtsson L. Assessment of the importance of dissimilatory nitrate reduction to ammonium for the terrestrial nitrogen cycle. Biogeosciences. 2011;8(7):1779–91.

    Article  CAS  Google Scholar 

  141. Sauder LA, Peterse F, Schouten S, Neufeld JD. Low-ammonia niche of ammonia-oxidizing archaea in rotating biological contactors of a municipal wastewater treatment plant. Environ Microbiol. 2012;14(9):2589–600.

    Article  CAS  Google Scholar 

  142. Schalk J, Oustad H, Kuenen JG, Jetten MSM. The aerobic oxidation of hydrazine: a novel reaction in microbial nitrogen metabolism. FEMS Microbiol Lett. 1998;158:61–7.

    Article  CAS  Google Scholar 

  143. Schalk J, De Vries S, Kuenen JG, Jetten MSM. Involvement of a novel hydroxylamine oxidoreductase in anaerobic ammonium oxidation. Biochemistry. 2000;39:5405–12.

    Article  CAS  Google Scholar 

  144. Schleper C, Nicol GW. Ammonia-oxidising Archaea—physiology, ecology and evolution. Adv Microb Physiol. 2010;57:1–41.

    Article  CAS  Google Scholar 

  145. Schmid M, Twachtmann U, Klein M, Strous M, Juretschko S, Jetten M, et al. Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Syst Appl Microbiol. 2000;23:93–106.

    Article  CAS  Google Scholar 

  146. Schmidt I, Bock E. Anaerobic ammonia oxidation with nitrogen dioxide by Nitrosomonas eutropha. Arch Microbiol. 1997;167(2):106–11.

    Article  CAS  Google Scholar 

  147. Schmidt I, Bock E, Jetten MSM. Ammonia oxidation by Nitrosomonas eutropha with NO2 as oxidant is not inhibited by acetylene. Microbiology. 2001;147(8):2247–53.

    Article  CAS  Google Scholar 

  148. Schmidt I, Sliekers O, Schmid M, Bock E, Fuerst J, Kuenen JG, et al. New concepts of microbial treatment processes for the nitrogen removal in wastewater. FEMS Microbiol Rev. 2003;27(4):481–92.

    Article  CAS  Google Scholar 

  149. Schramm A, De Beer D, Wagner M, Amann RI. Identification and activities in situ of Nitrosospira and Nitrospira spp.as dominant populations in a nitrifying fluidized bed reactor. Appl Environ Microbiol. 1998;64:3480–5.

    CAS  Google Scholar 

  150. Schulthess RV, Wild D, Gujer W. Nitric and nitrous oxides from denitrifying activated sludge at low oxygen concentration. Water Sci Technol. 1994;30:123–32.

    CAS  Google Scholar 

  151. Schulthess RV, Kuhni M, Gujer W. Release of nitric and nitrous oxides from denitrifying activated sludge. Water Res. 1995;29(1):215–26.

    Article  CAS  Google Scholar 

  152. Shen LD, Hu BL. Microbiology, ecology, and application of the nitrite-dependent anaerobic methane oxidation process. Front Microbiol. 2012;3:269.

    Google Scholar 

  153. Siegrist H, Reithaar S, Koch G, Lais P. Nitrogen loss in a nitrifying rotating contactor treating ammonium-rich wastewater without organic carbon. Water Sci.Technol. 1998;38:241–8.

    Article  CAS  Google Scholar 

  154. Sliekers AO, Derwort N, Strous M, Kuenen JG, Jetten MSM. Completely autotrophic nitrogen removal over nitrite in one single reactor. Water Research, in press. 2001;2001

  155. Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, et al. Climate change 2007: the physical science basis. Cambridge: Cambridge University Press; 2007.

    Google Scholar 

  156. Sperl GT, Hoare DS. Denitrification with methanol: a selective enrichment for Hyphomicrobium species. J Bacteriol. 1971;108(2):733–6.

    CAS  Google Scholar 

  157. Srinandan CS, Shah M, Patel B, Nerurkar AS. Assessment of denitrifiying bacterial composition in activated sludge. Bioresour Technol. 2011;10:9481–9.

    Article  CAS  Google Scholar 

  158. Steinert K, Wagner V, Kroth-Pancic PG, Bickel-Sandkotter S. Characterization and subunit structure of the ATP synthase of the halophilic archaeon Haloferax volcanii and organization of the ATP synthase genes. J Biol Chem. 1997;272:6261–9.

    Article  CAS  Google Scholar 

  159. Straub KL, Benz M, Schink B, Widdel F. Anaerobic, nitrate-dependent microbial oxidation of ferrous iron. Appl Environ Microbiol. 1996;62(4):1458–60.

    CAS  Google Scholar 

  160. Strohm TO, Griffin B, Zumft WG, Schink B. Growth yields in bacterial denitrification and nitrate ammonification. Appl Environ Microbiol. 2007;73(5):1420–4.

    Article  CAS  Google Scholar 

  161. Strous M, Van Gerven E, Kuenen JG, Jetten M. Effects of aerobic and microaerobic conditions on anaerobic ammonium-oxidizing (anammox) sludge. ApplEnvironMicrobiol. 1997;63:2446–8.

    CAS  Google Scholar 

  162. Strous M, Heijnen JJ, Kuenen JG, Jetten MSM. The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Appl Microbiol Biotechnol. 1998;50:589–96.

    Article  CAS  Google Scholar 

  163. Strous M, Fuerst J, Kramer E, Logemann S, Muyzer G, van de Pas K, et al. Missing lithotroph identified as new planctomycete. Nature. 1999a;400:446–9.

    Article  CAS  Google Scholar 

  164. Strous, M. Microbiology of anaerobic ammonium oxidation. PhD Thesis. Department of Microbiology. Delft, TU Technical University, The Netherlands. 2000. ISBN 90–9013621-5.

  165. Sui Q, Liu C, Dong H, Zhu Z. Effect of ammonium nitrogen concentration on the ammonia-oxidizing bacteria community in a membrane bioreactor for the treatment of anaerobically digested swine wastewater. J Biosci Bioeng. 2014;118(3):277–83.

    Article  CAS  Google Scholar 

  166. Sun W, Sierra R, Field JA. Anoxic oxidation of arsenite linked to denitrification in sludges and sediments. Water Res. 2008;42(17):4569–77.

    Article  CAS  Google Scholar 

  167. Suwa Y, Imamura Y, Suzuki T, Tashiro T, Urushigawa Y. Ammonia-oxidizing bacteria with different sensitivities to (NH4)2SO4 in activated sludges. Water Res. 1994;28(7):1523–32.

    Article  CAS  Google Scholar 

  168. Takaya N, Catalan-Sakairi MAB, Sakaguchi Y, Kato I, Zhou Z, Shoun H. Aerobic denitrifying bacteria that produce low levels of nitrous oxide. Appl Environ Microbiol. 2003;69(6):3152–7.

    Article  CAS  Google Scholar 

  169. Tallec G, Garnier J, Billen G, Gousailles M. Nitrous oxide emissions from secondary activated sludge in nitrifying conditions of urban wastewater treatment plants: effect of oxygenation level. Water Res. 2006a;40(15):2972–80.

    Article  CAS  Google Scholar 

  170. Tanaka Y, Fukumori Y, Yamanaka T. Purification of cytochrome a1c1 from Nitrobacter agilis and characterization of nitrite oxidation system of the bacterium. Arch Microbiol. 1983;135:265–71.

    Article  CAS  Google Scholar 

  171. Teske A, Alm E, Regan JM, Toze S, Rittman BE, Stahl DA. Evolutionary relationships among ammonia- and nitrite-oxidizing bacteria. J Bacteriol. 1994;176:6623–30.

    Article  CAS  Google Scholar 

  172. Thamdrup B. New pathways and processes in the global nitrogen cycle. Annu Rev Ecol Evol Syst. 2012;43:407–28.

    Article  Google Scholar 

  173. Third KA, Sliekers AO, Kuenen JG, Jetten MSM. The CANON system (completely autotrophic nitrogen-removal over nitrite) under ammonium limitation: interaction and competition between three groups of bacteria. Syst Appl Microbiol. 2001;24:588–96.

    Article  CAS  Google Scholar 

  174. Third KA, Sliekers AO, Kuenen JG, Jetten MM. The CANON system (completely autotrophic nitrogen-removal over nitrite) under ammonium limitation: interaction and competition between three groups of bacteria. Syst Appl Microbiol. 2002;24:588–96.

    Article  Google Scholar 

  175. Tiedje JM, Sexstone AJ, Myrold DD, Robinson JA. Denitrification: ecological niches, competition and survival. Antonie Van Leeuwenhoek. 1983;48(6):569–83.

    Article  Google Scholar 

  176. Treusch AH, Leininger S, Kletzin A, Schuster SC, Klenk HP, Schleper C. Novel genes for nitrite reductase and Amo-related proteins indicate a role of uncultivated mesophilic crenarchaeota in nitrogen cycling. Environ Microbiol. 2005;7(12):1985–95.

    Article  CAS  Google Scholar 

  177. Turk O, Mavinic DS. Preliminary assessment of a shortcut in nitrogen removal from wastewater. Can J Civ Eng. 1986;13:600–5.

    Article  Google Scholar 

  178. Turk O, Mavinic DS. Selective inhibition: a novel concept for removing nitrogen from highly nitrogenous wastes. Environ Technol Lett. 1987;8:419–26.

    Article  CAS  Google Scholar 

  179. Van Dongen UGJM, Jetten MS, Van Loosdrecht MCM. The SHARON®-anammox® process for treatment of ammonium rich wastewater. Water Sci Technol. 2001a;44(1):153–60.

    CAS  Google Scholar 

  180. Van de Graaf AA, De Bruijn P, Robertson LA, Jetten MSM, Kuenen JG. Autotrophic growth of anaerobic ammonium-oxidizing micro-organisms in a fuidized bed reactor. Microbiology UK. 1996;142:2187–96.

    Article  CAS  Google Scholar 

  181. Van de Graaf AA, De Bruijn P, Robertson LA, Jetten MSM, Kuenen JG. Metabolic pathway of anaerobic ammonium oxidation on the basis of N-15 studies in a fuidized bed reactor. Microbiology UK. 1997;143:2415–21.

    Article  CAS  Google Scholar 

  182. Van Dongen UGJM, Jetten MS, Van Loosdrecht MCM. The SHARON®-anammox® process for treatment of ammonium rich wastewater. Water Sci Technol. 2001b;44(1):153–60.

    CAS  Google Scholar 

  183. Van Kempen R, ten Have CCR, Meijer SCF, Mulder JW, Duin JOJ, Uijterlinde CA, et al. SHARON process evaluated for improved wastewater treatment plant nitrogen effluent quality. Water Sci Technol. 2005;52(4):55–62.

    CAS  Google Scholar 

  184. van Kessel MA, Speth DR, Albertsen M, Nielsen PH, den Camp HJO, Kartal B, et al. Complete nitrification by a single microorganism. Nature. 2015;528(7583):555–9.

    Google Scholar 

  185. Van Versefeld H, Meijer E, Stouthamer A. Energy conservation during nitrate respiration in Parococcus denitri®cans. Arch Microbiol. 1977;112:17–23.

    Article  Google Scholar 

  186. Vazquez-Padin J, Fernadez I, Figueroa M, Mosquera-Corral A, Campos JL, Mendez R. Applications of anammox based processes to treat anaerobic digester supernatant at room temperature. Bioresour Technol. 2009;100:2988–94.

    Article  CAS  Google Scholar 

  187. Venter JC, Remington K, Heidelberg JF, Halpern AL, Rusch D, Eisen JA, et al. Environmental genome shotgun sequencing of the Sargasso Sea. Science. 2004;304(5667):66–74.

    Article  CAS  Google Scholar 

  188. Vlaeminck SE, Terada A, Smets BF, De Clippeleir H, Schaubroeck T, Bolca S, et al. Aggregate size and architecture determine microbial activity balance for onestage partial nitritation and anammox. Appl Environ Microbiol. 2010;76(3):900–9.

    Article  CAS  Google Scholar 

  189. Volcke EI, van Loosdrecht MC, Vanrolleghem PA. Controlling the nitrite: ammonium ratio in a SHARON reactor in view of its coupling with an anammox process. Water Sci Technol. 2006;53(4–5):45–54.

    Article  CAS  Google Scholar 

  190. Walsh DA, Zaikova E, Howes CG, Song YC, Wright JJ, Tringe SG, et al. Metagenome of a versatile chemolithoautotroph from expanding oceanic dead zones. Science. 2009;326(5952):578–82.

    Article  CAS  Google Scholar 

  191. Wang X, Wen X, Criddle C, Wells G, Zhang J, Zhao Y. Community analysis of ammonia-oxidizing bacteria in activated sludge of eight wastewater treatment systems. J Environ Sci. 2010;22(4):627–34.

    Article  CAS  Google Scholar 

  192. Wang X, Hu M, Xia Y, Wen X, Ding K. Pyrosequencing analysis of bacterial diversity in 14 wastewater treatment systems in China. Appl Environ Microbiol. 2012;78(19):7042–7.

    Article  CAS  Google Scholar 

  193. Wagner M, Rath G, Amann R, Koops H-P, Schleifer K-H. In situ identification of ammonia-oxidizing bacteria. Syst Appl Microbiol. 1995;18:251–64.

    Article  CAS  Google Scholar 

  194. Wagner M, Loy A. Bacterial community composition and function in sewage treatment systems. Curr Opin Biotechnol. 2002;13(3):218–27.

    Article  CAS  Google Scholar 

  195. Whang LM, Chien IC, Yuan SL, Wu YJ. Nitrifying community structures and nitrification performance of full-scale municipal and swine wastewater treatment plants. Chemosphere. 2009;75(2):234–42.

    Article  CAS  Google Scholar 

  196. Winkler MKH, Kleerebezem R, van Loosdrecht MCM. Integration of anammox into the aerobic granular sludge process for main stream wastewater treatment at ambient temperatures. Water Res. 2012a;46(1):136–44.

    Article  CAS  Google Scholar 

  197. Winkler MKH, Yang J, Kleerebezem R, Plaza E, Trela J, Hultman B, et al. Nitrate reduction by organotrophic anammox bacteria in a nitritation/anammox granular sludge and a moving bed biofilm reactor. Bioresour Technol. 2012b;114:217–23.

    Article  CAS  Google Scholar 

  198. Wrage N, Velthof GL, van Beusichem ML, Oenema O. Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol Biochem. 2001;33:1723–32.

    Article  CAS  Google Scholar 

  199. Wu ZD, Huang SB, Yang YL, Xu FQ, Zhang YQ, Jiang R. Isolation of an aerobic denitrifying bacterial strain from a biofilter for removal of nitrogen oxide. Aerosol Air Qual Res. 2013;13:1126–32.

    CAS  Google Scholar 

  200. Wunderlin P, Mohn J, Joss A, Emmenegger L, Siegrist H. Mechanisms of N2O production in biological wastewater treatment under nitrifying and denitrifying conditions. Water Res. 2012;46:1027–10.

    Article  CAS  Google Scholar 

  201. Yang L, Alleman JE. Investigation of batch wise nitrite build-up by an enriched nitrification culture. Wat. Sci. Tech. 1992;26(5–-6):997–1005.

    CAS  Google Scholar 

  202. Yoo H, Ahn KH, Lee HJ, Lee KH, Kwak YJ, Song KG. Nitrogen removal from synthetic wastewater by simultaneous nitrification and denitrification (SND) via nitrite in an intermittently-aerated reactor. Water Res. 1999;33(1):145–54.

    Article  CAS  Google Scholar 

  203. Yu R, Chandran K. Strategies of Nitrosomonas europaea 19718 to counter low dissolved oxygen and high nitrite concentrations. BMC Microbiol. 2010;10(1):70.

    Article  CAS  Google Scholar 

  204. Zehr JP, Kudela RM. Nitrogen cycle of the open ocean: from genes to ecosystems. Annu Rev Mar Sci. 2011;3:197–225.

    Article  Google Scholar 

  205. Zehr JP, Waterbury JB, Turner PJ, Montoya JP, Omoregie E, Steward GF, et al. Unicellular cyanobacteria fix N2 in the subtropical North Pacific Ocean. Nature. 2001;412(6847):635–8.

    Article  CAS  Google Scholar 

  206. Zhang T, Jin T, Yan Q, Shao M, Wells G, Criddle C, et al. Occurrence of ammoniaoxidizing Archaea in activated sludges of a laboratory scale reactor and two wastewater treatment plants. J Appl Microbiol. 2009;107(3):970–7.

    Article  CAS  Google Scholar 

  207. Zhang T, Ye L, Tong AHY, Shao MF, Lok S. Ammonia-oxidizing Archaea and ammonia-oxidizing bacteria in six full-scale wastewater treatment bioreactors. Appl Microbiol Biotechnol. 2011;91:1215–25.

    Article  CAS  Google Scholar 

  208. Zhu B, Sánchez J, Van Alen TA, Sanabria J, Jetten MS, Ettwig KF, et al. Combined anaerobic ammonium and methane oxidation for nitrogen and methane removal. Biochem Soc Trans. 2011;39(6):1822–5.

    Article  CAS  Google Scholar 

  209. Zhu B, van Dijk G, Fritz C, Smolders AJ, Pol A, Jetten MS, Ettwig KF. Anaerobic oxidization of methane in a minerotrophic peatland: enrichment of nitrite-dependent methane-oxidizing bacteria. Appl Environ Microbiol. 2012;78:8657–65.

    Article  CAS  Google Scholar 

  210. Zumft WG. The denitrifying procaryotes. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer K-H, editors. The procaryotes. New York, N.Y: Springer Verlag; 1992. p. 554–82.

    Google Scholar 

  211. Zumft WG. Cell biology and molecular basis of denitrification. Microbiol Mol Biol Rev. 1997;61:533–616.

    CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by the US NSF grant #1514637. The views and rationale presented in this manuscript are those of the authors and do not necessarily represent the funding agency. We greatly appreciate the time reviewers have spent on this manuscript to provide their useful comments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ramesh Goel.

Ethics declarations

Conflict of Interest

The authors have no underlined conflict of interest with any third party. Views and discussion presented in this review paper are independent views of authors based on the available literature on N cycle.

Additional information

This article is part of the Topical Collection on Water Pollution

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pappu, A.R., Bhattacharjee, A.S., Dasgupta, S. et al. Nitrogen Cycle in Engineered and Natural Ecosystems—Past and Current. Curr Pollution Rep 3, 120–140 (2017). https://doi.org/10.1007/s40726-017-0051-y

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40726-017-0051-y

Keywords

Navigation