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Qualitative and Quantitative Aspects of the Modern Nitrogen Cycle

  • Aaron L. MillsEmail author
Chapter
Part of the Advances in Environmental Microbiology book series (AEM, volume 6)

Abstract

The biogeochemical cycling of nitrogen was recognized and largely defined in the nineteenth century. Although great detail about both the processes and the organisms that carry them out have been reported during the 100+ years since the definition of the cycle was completed, only two new processes were added to the cycle, anaerobic ammonia oxidation and industrial fixation of N2 by the Haber-Bosch process. The latter process has injected large amounts of reactive nitrogen into the global environment such that many locations have excess nitrogen present that accelerates eutrophication, emission of greenhouse gasses, destruction of ozone, and some direct health effects. Nevertheless, nitrogen is still the primary limitation on food production, and as the world population continues to increase, the demand for nitrogen fertilizer will continue to drive fixation of N2 into reactive nitrogen faster than denitrification and anammox can return it to the atmosphere as the nonreactive N2.

Keywords

Nitrogen cycle Microbes 

Notes

Compliance with Ethical Standards

Conflict of Interest

Aaron L. Mills declares that he has no conflict of interest.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Alexander M (1977) Introduction to soil microbiology. Wiley, New YorkGoogle Scholar
  2. An S, Gardner WS (2002) Dissimilatory nitrate reduction to ammonium (DNRA) as a nitrogen link, versus denitrification as a sink in a shallow estuary (Laguna Madre/Baffin Bay, Texas). Mar Ecol Prog Ser 237:41–50CrossRefGoogle Scholar
  3. Baggs EM (2008) A review of stable isotope techniques for N2O source partitioning in soils: recent progress, remaining challenges and future considerations. Rapid Commun Mass Spectrom 22(11):1664–1672.  https://doi.org/10.1002/rcm.3456 PubMedCrossRefGoogle Scholar
  4. Bashan Y, Holguin G (1997) Azospirillum-plant relationships: environmental and physiological advances (1990-1996). Can J Microbiol 43:103–121CrossRefGoogle Scholar
  5. Battistelli JM (2013) Distribution of nitrogen-cycling microbes in engineered reactors for N removal from wastewater. Dissertation. University of Virginia, Charlottesville, VAGoogle Scholar
  6. Behrendt A, Tarre S, Beliavski M, Green M, Klatt J, de Beer D, Stief P (2014) Effect of high electron donor supply on dissimilatory nitrate reduction pathways in a bioreactor for nitrate removal. Bioresour Technol 171:291–297.  https://doi.org/10.1016/j.biortech.2014.08.073 PubMedCrossRefGoogle Scholar
  7. Beijerinck MW (1888) Die Bacterien der Papilionaceenknöllchen. Botansch Zeitung 46:725–804Google Scholar
  8. Beijerinck MW (1901) Ueber oligonitrophile Mikroben. Centralblatt fur Bakteriologie, Part II 7:561–582Google Scholar
  9. Belay N, Sparling R, Daniels L (1984) Dinitrogen fixation by a thermophilic methanogenic bacterium. Nature 312:286–288PubMedCrossRefGoogle Scholar
  10. Berman JA, Sachdeva R, Fuhrman JA (2010) Population ecology of nitrifying Archaea and Bacteria in the Southern California Bight. Environ Microbiol 12(5):1282–1292.  https://doi.org/10.1111/j.1462-2920.2010.02172.x CrossRefGoogle Scholar
  11. Blum LK, Mills AL (2012) Estuarine microbial ecology. In: Day JW Jr, Kemp WM, Yáñez-Arancibia A, Crump BC (eds) Estuarine ecology, 2nd edn. Wiley-Blackwell, pp 235–262Google Scholar
  12. Bremner JM, Blackmer AM, Waring SA (1980) Formation of nitrous oxide and dinitrogen by chemical decomposition of hydroxylamine in soils. Soil Biol Biochem 12:263–269CrossRefGoogle Scholar
  13. Broda E (1977) 2 Kinds of lithotrophs missing in nature. Z Allg Mikrobiol 17(6):491–493.  https://doi.org/10.1002/jobm.3630170611 PubMedCrossRefGoogle Scholar
  14. Canter LW (1997) Nitrates in groundwater. CRC, Boca Raton, FLGoogle Scholar
  15. Caskey WH, Tiedje JM (1979) Evidence of Clostridia as agents of dissimilatory reduction of nitrate to ammonia in soils. Soil Sci Soc Am J 42:913–918Google Scholar
  16. Ceci L (1975) Fish fertilizer: a native North American practice? Science 188(4183):26–30PubMedCrossRefGoogle Scholar
  17. Chatzimpiros P, Barles S (2013) Nitrogen food-print: N use related to meat and dairy consumption in France. Biogeosciences 10:471–481.  https://doi.org/10.5194/bg-10-471-2013 CrossRefGoogle Scholar
  18. Childs CR, Rabalais NN, Turner RE, Proctor LM (2002) Sediment denitrification in the Gulf of Mexico zone of hypoxia. Mar Ecol Prog Ser 240:285–290CrossRefGoogle Scholar
  19. Chung K-T, Case CL (2001) Sergei Winogradsky: founder of soil microbiology. SIM News 51(3):133–135Google Scholar
  20. Corriveau J, van Bochove E, Cluis D (2010) Sources of nitrite in streams of an intensively cropped watershed. Water Environ Res 82(7):622–632.  https://doi.org/10.2175/106143009x12529484815953 PubMedCrossRefGoogle Scholar
  21. Costa E, Perez J, Kreft JU (2006) Why is metabolic labour divided in nitrification? Trends Microbiol 14(5):213–219.  https://doi.org/10.1016/j.tim.2006.03.006 PubMedCrossRefGoogle Scholar
  22. Daims H, Nielsen JL, Nielsen PH, Schleifer KH, Wagner M (2001) In situ characterization of Nitrospira-like nitrite oxidizing bacteria active in wastewater treatment plants. Appl Environ Microbiol 67(11):5273–5284.  https://doi.org/10.1128/aem.67.11.5273-5284.2001 PubMedPubMedCentralCrossRefGoogle Scholar
  23. Daims H, Lebedeva EV, Pjevac P, Han P, Herbold C, Albertsen M, Jehmlich N, Palatinszky M, Vierheilig J, Bulaev A, Kirkegaard RH, von Bergen M, Rattei T, Bendinger B, Nielsen PH, Wagner M (2015) Complete nitrification by Nitrospira bacteria. Nature 528(7583):504–509.  https://doi.org/10.1038/nature16461 PubMedPubMedCentralCrossRefGoogle Scholar
  24. Dale OR, Tobias CR, Song B (2009) Biogeographical distribution of diverse anaerobic ammonium oxidizing (anammox) bacteria in Cape Fear River Estuary. Environ Microbiol 11(5):1194–1207.  https://doi.org/10.1111/j.1462-2920.2008.01850.x PubMedCrossRefGoogle Scholar
  25. Egli K, Fanger U, Alvarez PJJ, Siegrist H, van der Meer JR, Zehnder AJB (2001) Enrichment and characterization of an anammox bacterium from a rotating biological contactor treating ammonium-rich leachate. Arch Microbiol 175(3):198–207.  https://doi.org/10.1007/s002030100255 PubMedCrossRefGoogle Scholar
  26. Ehrich S, Behrens D, Lebedeva E, Ludwig W, Bock E (1995) A new obligately chemolithoautotrophic, nitrite-oxidizing bacterium, Nitrospira moscoviensis sp. nov. and its phylogenetic relationship. Arch Microbiol 164(1):16–23.  https://doi.org/10.1007/bf02568729 PubMedCrossRefGoogle Scholar
  27. FAO (2015) World fertilizer trends and outlook to 2018. Food and Agriculture Organization of the United Nations, RomeGoogle Scholar
  28. Fernandes SO, Bonin PC, Michotey VD, Garcia N, LokaBharathi PA (2012) Nitrogen-limited mangrove ecosystems conserve N through dissimilatory nitrate reduction to ammonium. Sci Rep 2:419.  https://doi.org/10.1038/srep00419 PubMedPubMedCentralCrossRefGoogle Scholar
  29. Ferron S, Ortega T, Forja JM (2009) Benthic fluxes in a tidal salt marsh creek affected by fish farm activities: Rio San Pedro (Bay of Cadiz, SW Spain). Mar Chem 113(1–2):50–62.  https://doi.org/10.1016/j.marchem.2008.12.002 CrossRefGoogle Scholar
  30. Firestone MK (1982) Biological denitrification. In: Stevenson FJ (ed) Nitrogen in agricultural soils. Agronomy monographs, vol 22. American Society of Agronomy, Madison, WI, pp 289–326Google Scholar
  31. Flewelling SA, Hornberger GM, Herman JS, Mills AL (2012) Travel time controls the magnitude of nitrate discharge in groundwater bypassing the riparian zone to a stream on Virginia’s coastal plain. Hydrol Process 26:1242–1253.  https://doi.org/10.1002/hyp.8219 CrossRefGoogle Scholar
  32. Flewelling SA, Hornberger GM, Herman JS, Mills AL, Robertson WM (2013) Diel patterns in coastal-stream nitrate concentrations linked to evapotranspiration in the riparian zone of a low-relief, agricultural catchment. Hydrol Proc.  https://doi.org/10.1002/hyp.9763
  33. Food and Agriculture Organization (1985) Guidelines: land evaluation for irrigated agriculture. Food and Agriculture Organization of the United Nations, RomeGoogle Scholar
  34. Fowler D, Coyle M, Skiba U, Sutton MA, Cape JN, Reis S, Sheppard LJ, Jenkins A, Grizzetti B, Galloway JN, Vitousek P, Leach A, Bouwman AF, Butterbach-Bahl K, Dentener F, Stevenson D, Amann M, Voss M (2013) The global nitrogen cycle in the twenty-first century. Philos Trans R Soc Lond B Biol Sci 368(1621):20130165.  https://doi.org/10.1098/rstb.2013.0164 PubMedPubMedCentralCrossRefGoogle Scholar
  35. Fowler D, Steadman CE, Stevenson D, Coyle M, Rees RM, Skiba UM, Sutton MA, Cape JN, Dore AJ, Vieno M, Simpson D, Zaehle S, Stocker BD, Rinaldi M, Facchini MC, Flechard CR, Nemitz E, Twigg M, Erisman JW, Butterbach-Bahl K, Galloway JN (2015) Effects of global change during the 21st century on the nitrogen cycle. Atmos Chem Phys 15(24):13849–13893.  https://doi.org/10.5194/acp-15-13849-2015 CrossRefGoogle Scholar
  36. Galloway JN, Cowling EB (2002) Reactive nitrogen and the world: 200 years of change. Ambio 31(2):64–71PubMedCrossRefGoogle Scholar
  37. Galloway JN, Aber JD, Erisman JW, Seitzinger SP, Howarth RW, Cowling EB, Cosby BJ (2003) The nitrogen cascade. Bioscience 53(4):341–356CrossRefGoogle Scholar
  38. Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Holland EA, Karl DM, Michaels AF, Porter JH, Townsend AR, Vörösmarty CJ (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70(2):153–226.  https://doi.org/10.1007/s10533-004-0370-0 CrossRefGoogle Scholar
  39. Galloway JN, Leach AM, Bleeker A, Erisman JW (2013) A chronology of human understanding of the nitrogen cycle. Philos Trans R Soc Lond B Biol Sci 368(1621):20130120.  https://doi.org/10.1098/rstb.2013.0120 PubMedPubMedCentralCrossRefGoogle Scholar
  40. Gardner WS, McCarthy MJ (2009) Nitrogen dynamics at the sediment-water interface in shallow, sub-tropical Florida Bay: why denitrification efficiency may decrease with increased eutrophication. Biogeochemistry 95(2–3):185–198.  https://doi.org/10.1007/s10533-009-9329-5 CrossRefGoogle Scholar
  41. Gardner WS, McCarthy MJ, An S, Sobolev D, Sell KS, Brock D (2006) Nitrogen fixation and dissimilatory nitrate reduction to ammonium (DNRA) support nitrogen dynamics in Texas estuaries. Limnol Oceanogr 51(1):558–568CrossRefGoogle Scholar
  42. Gayon U, Dupetit G (1883) La fermentation des nitrates. Mem Soc Sci Phys Nat Bordeaux Ser 2(5):35–36Google Scholar
  43. Gayon U, Dupetit G (1886) Recherches sur la reduction des nitrates par les infiniment petits. Mem Soc Sci Phys Nat Bordeaux Ser 3(2):201–307Google Scholar
  44. Giblin AE, Weston NB, Banta GT, Tucker J, Hopkinson CS (2010) The effects of salinity on nitrogen losses from an oligohaline estuarine sediment. Estuar Coasts 33(5):1054–1068.  https://doi.org/10.1007/s12237-010-9280-7 CrossRefGoogle Scholar
  45. Giblin AE, Tobias CR, Song B, Weston N, Banta GT, Rivera-Monroy VH (2013) The importance of dissimilatory nitrate reduction to ammonium (DNRA) in the nitrogen cycle of coastal ecosystems. Oceanography 26(3):124–131.  https://doi.org/10.5670/oceanog.2013.54 CrossRefGoogle Scholar
  46. Graham DW, Knapp CW, Van Vleck ES, Bloor K, Lane TB, Graham CE (2007) Experimental demonstration of chaotic instability in biological nitrification. ISME J 1:385–393PubMedCrossRefGoogle Scholar
  47. Gu C, Hornberger GM, Mills AL, Herman JS, Flewelling SA (2007) Nitrate reduction in streambed sediments: effects of flow and biogeochemical kinetics. Water Resour Res 43:W12413.  https://doi.org/10.11029/12007WR006027 CrossRefGoogle Scholar
  48. Hamm RE, Thompson TG (1941) Dissolved nitrogen in the sea water of the northeast Pacific with notes on the total carbon dioxide and the dissolved oxygen. J Mar Res 4:11–27Google Scholar
  49. Hasan SM, Hall JB (1977) Dissimilatory nitrate reduction in Clostridium tertium. Z Allg Mikrobiol 17:501–506PubMedCrossRefGoogle Scholar
  50. Head IM, Hiorns WD, Embley MT, McCarthy AJ, Saunders JR (1993) The phylogeny of autotrophic ammonia oxidising bacteria as determined by analysis of 16S ribosomal RNA gene sequences. J Gen Microbiol 139:1147–1153PubMedCrossRefGoogle Scholar
  51. Heath DB (1963) A journal of the Pilgrims at Plymouth: Mourt’s relation, a relation or journal of the English plantation settled at Plymouth in New England. Corinth Books, New YorkGoogle Scholar
  52. Hellriegel H, Wilfarth H (1889) Erfolgt die Assimilation des freien Stickstoffs durch die Leguminosen unter Mitwirkung Niederer Organismen? Ber Dtsch Bot Ges 7:138–143Google Scholar
  53. Hovanec TA, Taylor LT, Blakis A, Delong EF (1998) Nitrospira-like bacteria associated with nitrite oxidation in freshwater aquaria. Appl Environ Microbiol 64(1):258–264PubMedPubMedCentralGoogle Scholar
  54. Howarth RW, Teal JM (1980) Energy-flow in a salt-marsh ecosystem—the role of reduced inorganic sulfur-compounds. Am Nat 116(6):862–872CrossRefGoogle Scholar
  55. Jetten MSM, Sliekers O, Kuypers M, Dalsgaard T, van Niftrik L, Cirpus I, van de Pas-Schoonen K, Lavik G, Thamdrup B, Le Paslier D, Op den Camp HJM, Hulth S, Nielsen LP, Abma W, Third K, Engstrom P, Kuenen JG, Jorgensen BB, Canfield DE, Damste JSS, Revsbech NP, Fuerst J, Weissenbach J, Wagner M, Schmidt I, Schmid M, Strous M (2003) Anaerobic ammonium oxidation by marine and freshwater planctomycete-like bacteria. Appl Microbiol Biotechnol 63(2):107–114.  https://doi.org/10.1007/s00253-003-1422-4 PubMedCrossRefGoogle Scholar
  56. Jetten MSM, Op Den Camp HJM, Kuenen GJ, Strous M (2010) Description of the order Brocadiales. In: Krieg NR, Staley JT, Brown DR et al (eds) Bergey’s manual of systematic bacteriology, vol 4. Springer, Germany, pp 596–603Google Scholar
  57. Kartal B, Rattray J, van Niftrik LA, van de Vossenberg J, Schmid MC, Webb RI, Schouten S, Fuerst JA, Damste JSS, Jetten MSM, Strous M (2007) Candidatus “Anammoxoglobus propionicus” a new propionate oxidizing species of anaerobic ammonium oxidizing bacteria. Syst Appl Microbiol 30(1):39–49.  https://doi.org/10.1016/j.syapm.2006.03.004 PubMedCrossRefGoogle Scholar
  58. Kaspar HF (1983) Denitrification, nitrate reduction to ammonium and inorganic nitrogen pools in intertidal sediments. Mar Biol 74:133–139CrossRefGoogle Scholar
  59. Kaspar HF, Tiedje JM, Firestone RB (1981) Denitrification and dissimilatory nitrate reduction to ammonium in digested-sludge. Can J Microbiol 27(9):878–885PubMedCrossRefGoogle Scholar
  60. Kawagoshi Y, Nakamura Y, Kawashima H, Fujisaki K, Furukawa K, Fujimoto A (2010) Enrichment of marine anammox bacteria from seawater-related samples and bacterial community study. Water Sci Technol 61(1):119–126.  https://doi.org/10.2166/wst.2010.796 PubMedCrossRefGoogle Scholar
  61. Keith SM, Macfarlane GT, Herbert RA (1982) Dissimilatory nitrate reduction by a strain of Clostridium butyricum isolated from estuarine sediments. Arch Microbiol 132:62–66CrossRefGoogle Scholar
  62. Kindaichi T, Awata T, Suzuki Y, Tanabe K, Hatamoto M, Ozaki N, Ohashi A (2011a) Enrichment using an up-flow column reactor and community structure of marine anammox bacteria from coastal sediment. Microbes Environ 26(1):67–73.  https://doi.org/10.1264/jsme2.ME10158 PubMedCrossRefGoogle Scholar
  63. Kindaichi T, Awata T, Tanabe K, Ozaki N, Ohashi A (2011b) Enrichment of marine anammox bacteria in Hiroshima Bay sediments. Water Sci Technol 63(5):964–969.  https://doi.org/10.2166/wst.2011.277 PubMedCrossRefGoogle Scholar
  64. Koch H, Galushko A, Albertsen M, Schintlmeister A, Gruber-Dorninger C, Luecker S, Pelletier E, Le Paslier D, Spieck E, Richter A, Nielsen PH, Wagner M, Daims H (2014) Growth of nitrite-oxidizing bacteria by aerobic hydrogen oxidation. Science 345(6200):1052–1054.  https://doi.org/10.1126/science.1256985 PubMedCrossRefGoogle Scholar
  65. Koch H, Luecker S, Albertsen M, Kitzinger K, Herbold C, Spieck E, Nielsen PH, Wagner M, Daims H (2015) Expanded metabolic versatility of ubiquitous nitrite-oxidizing bacteria from the genus Nitrospira. Proc Natl Acad Sci USA 112(36):11371–11376.  https://doi.org/10.1073/pnas.1506533112 PubMedCrossRefGoogle Scholar
  66. Könneke M, Bernhard AE, de la Torre JR, Walker CB, Waterbury JB, Stahl DA (2005) Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437:543–546PubMedCrossRefGoogle Scholar
  67. Koop-Jakobsen K, Giblin AE (2010) The effect of increased nitrate loading on nitratie reduction via denitrification and DNRA in salt marsh sediments. Limnol Oceanogr 55(2):789–802CrossRefGoogle Scholar
  68. Kuenen JG, Jetten MSM (2001) Extraordinary anaerobic ammonium-oxidizing bacteria. ASM News 67(9):456–463Google Scholar
  69. Lam P, Lavik G, Jensen MM, van de Vossenberg J, Schmid M, Woebken D, Dimitri G, Amann R, Jetten MSM, Kuypers MMM (2009) Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc Natl Acad Sci USA 106(12):4752–4757.  https://doi.org/10.1073/pnas.0812444106 PubMedCrossRefGoogle Scholar
  70. Lamer M (1957) The world fertilizer economy. Stanford University Press, Redwood City, CAGoogle Scholar
  71. Larsen J (2012) Meat consumption in China now double that in the United States. Earth Policy Institute. http://www.earth-policy.org/plan_b_updates/2012/update102. Accessed Mar 14 2016
  72. Lebedeva EV, Off S, Zumbraegel S, Kruse M, Shagzhina A, Luecker S, Maixner F, Lipski A, Daims H, Spieck E (2011) Isolation and characterization of a moderately thermophilic nitrite-oxidizing bacterium from a geothermal spring. FEMS Microbiol Ecol 75(2):195–204.  https://doi.org/10.1111/j.1574-6941.2010.01006.x PubMedCrossRefGoogle Scholar
  73. Leigh JA (2000) Nitrogen fixation in methanogens: the Archaeal perspective. Curr Issues Mol Biol 2(4):125–131PubMedGoogle Scholar
  74. Li M, Baker BJ, Anantharaman K, Jain S, Breier JA, Dick GJ (2015) Genomic and transcriptomic evidence for scavenging of diverse organic compounds by widespread deep-sea archaea. Nat Commun 6:8933.  https://doi.org/10.1038/ncomms9933 PubMedPubMedCentralCrossRefGoogle Scholar
  75. Lücker S, Wagner M, Maixner F, Pelletier E, Koch H, Vacherie B, Rattei T, Damste JSS, Spieck E, Le Paslier D, Daims H (2010) A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. Proc Natl Acad Sci USA 107(30):13479–13484.  https://doi.org/10.1073/pnas.1003860107 PubMedCrossRefGoogle Scholar
  76. Maier RM (2000) Biogeochemical cycling. In: Maier RM, Pepper IL, Gerba CP (eds) Environmental microbiology. Academic, San Diego, CA, pp 319–346Google Scholar
  77. Marchant HK, Lavik G, Holtappels M, Kuypers MMM (2014) The fate of nitrate in intertidal permeable sediments. PLoS One 9(8):e104517.  https://doi.org/10.1371/journal.pone.0104517 PubMedPubMedCentralCrossRefGoogle Scholar
  78. Martiny AC, Albrechtsen HJ, Arvin E, Molin S (2005) Identification of bacteria in biofilm and bulk water samples from a nonchlorinated model drinking water distribution system: detection of a large nitrite-oxidizing population associated with Nitrospira spp. Appl Environ Microbiol 71(12):8611–8617.  https://doi.org/10.1128/aem.71.12.8611-8617.2005 PubMedPubMedCentralCrossRefGoogle Scholar
  79. Mazeas L, Vigneron V, Le-Menach K, Budzinski H, Audic J-M, Bernet N, Bouchez T (2008) Elucidation of nitrate reduction pathways in anaerobic bioreactors using a stable isotope approach. Rapid Commun Mass Spectrom 22(11):1746–1750.  https://doi.org/10.1002/rcm.3524 PubMedCrossRefGoogle Scholar
  80. McLain JET, Martens DA (2005) Nitrous oxide flux from soil amino acid mineralization. Soil Biol Biochem 37:289–299CrossRefGoogle Scholar
  81. Mills AL, Hornberger GM, Herman JS (2008) Sediments in low-relief coastal streams as effective filters of agricultural nitrate. In: AWRA Specialty Conference on Riparian Processes. American Water Resources Association, Norfolk, VAGoogle Scholar
  82. Molnar N, Welsh DT, Marchand C, Deborde J, Meziane T (2013) Impacts of shrimp farm effluent on water quality, benthic metabolism and N-dynamics in a mangrove forest (New Caledonia). Estuar Coast Shelf Sci 117:12–21.  https://doi.org/10.1016/j.ecss.2012.07.012 CrossRefGoogle Scholar
  83. Moore TA, Xing Y, Lazenby B, Lynch MDJ, Schiff S, Robertson WD, Timlin R, Lanza S, Ryan MC, Aravena R, Fortin D, Clark ID, Neufeld JD (2011) Prevalence of anaerobic Ammonium-oxidizing bacteria in contaminated groundwater. Environ Sci Technol 45(17):7217–7225.  https://doi.org/10.1021/es201243t PubMedCrossRefGoogle Scholar
  84. Morrissey EM, Jenkins AS, Brown BL, Franklin RB (2013) Resource availability effects on nitrate-reducing microbial communities in a freshwater wetland. Wetlands 33(2):301–310.  https://doi.org/10.1007/s13157-013-0384-2 CrossRefGoogle Scholar
  85. Mulder A, Vandegraaf AA, Robertson LA, Kuenen JG (1995) Anaerobic ammonium oxidation discovered in a denitrifying fluidized-bed reactor. FEMS Microbiol Ecol 16(3):177–183.  https://doi.org/10.1111/j.1574-6941.1995.tb00281.x CrossRefGoogle Scholar
  86. Murray PA, Zinder SH (1984) Nitrogen fixation by a methanogenic archaebacterium. Nature 312:284–286CrossRefGoogle Scholar
  87. Myrold DD (1998) Transformations of Nitrogen. In: Sylvia DM, Fuhrmann JJ, Hartel PG, Zuberer DA (eds) Principles and applications of soil microbiology. Prentice-Hall, Upper Saddle River, NJ, pp 218–258Google Scholar
  88. Nakajima J, Sakka M, Kimura T, Furukawa K, Sakka K (2008) Enrichment of anammox bacteria from marine environment for the construction of a bioremediation reactor. Appl Microbiol Biotechnol 77(5):1159–1166.  https://doi.org/10.1007/s00253-007-1247-7 PubMedCrossRefGoogle Scholar
  89. Neubauer SC, Anderson IC, Neikirk BB (2005) Nitrogen cycling and ecosystem exchanges in a Virginia tidal freshwater marsh. Estuaries 28(6):909–922.  https://doi.org/10.1007/bf02696019 CrossRefGoogle Scholar
  90. Nogaro G, Burgin AJ (2014) Influence of bioturbation on denitrification and dissimilatory nitrate reduction to ammonium (DNRA) in freshwater sediments. Biogeochemistry 120(1–3):279–294.  https://doi.org/10.1007/s10533-014-9995-9 CrossRefGoogle Scholar
  91. Palatinszky M, Herbold C, Jehmlich N, Pogoda M, Han P, von Bergen M, Lagkouvardos I, Karst SM, Galushko A, Koch H, Berry D, Daims H, Wagner M (2015) Cyanate as an energy source for nitrifiers. Nature 524(7563):105–U227.  https://doi.org/10.1038/nature14856 PubMedPubMedCentralCrossRefGoogle Scholar
  92. Payne WJ (1986) 1986: Centenary of the isolation of denitrifying bacteria. ASM News 52(12):627–629Google Scholar
  93. Pennsylvania State University Extension Service (2016) Inoculation of legumes for maximum nitrogen fixation. Pennsylvania State University. http://extension.psu.edu/plants/crops/forages/successful-forage-establishment/inoculation-of-legumes-for-maximum-nitrogen-fixation. Accessed 1 May 2016
  94. Penton CR, Devol AH, Tiedje JM (2006) Molecular evidence for the broad distribution of anaerobic ammonium-oxidizing bacteria in freshwater and marine sediments. Appl Environ Microbiol 72(10):6829–6832.  https://doi.org/10.1128/aem.01254-06 PubMedPubMedCentralCrossRefGoogle Scholar
  95. Pester M, Maixner F, Berry D, Rattei T, Koch H, Luecker S, Nowka B, Richter A, Spieck E, Lebedeva E, Loy A, Wagner M, Daims H (2014) NxrB encoding the beta subunit of nitrite oxidoreductase as functional and phylogenetic marker for nitrite-oxidizing Nitrospira. Environ Microbiol 16(10):3055–3071.  https://doi.org/10.1111/1462-2920.12300 PubMedCrossRefGoogle Scholar
  96. Pinto AJ, Marcus DN, Ijaz UZ, Bautista-de lose Santos QM, Dick GJ, Raskin L (2015) Metagenomic evidence for the presence of comammox Nitrospira-like bacteria in a drinking water system. mSphere 1(1):e00054–e00015.  https://doi.org/10.1128/mSphere.00054-15 PubMedPubMedCentralCrossRefGoogle Scholar
  97. Porubsky WP, Joye SB, Moore WS, Tuncay K, Meile C (2011) Field measurements and modeling of groundwater flow and biogeochemistry at Moses Hammock, a backbarrier island on the Georgia coast. Biogeochemistry 104(1–3):69–90.  https://doi.org/10.1007/s10533-010-9484-8 CrossRefGoogle Scholar
  98. Poulin P, Pelletier E, Koutitonski VG, Neumeier U (2009) Seasonal nutrient fluxes variability of northern salt marshes: examples from the lower St. Lawrence Estuary. Wetl Ecol Manag 17(6):655–673.  https://doi.org/10.1007/s11273-009-9141-y CrossRefGoogle Scholar
  99. Prosser JI (2011) Soil nitrifiers and nitrification. In: Ward BB, Arp DJ, Klotz MG (eds) Nitrification. ASM, Washington, DC, pp 347–384CrossRefGoogle Scholar
  100. Purkhold U, Pommerening-Röser A, Juretschko S, Schmid MC, Koops HP, Wagner M (2000) 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 66(12):5368–5382PubMedPubMedCentralCrossRefGoogle Scholar
  101. Qin W, Amin SA, Martens-Habbena W, Walker CB, Urakawa H, Devol AH, Ingalls AE, Moffett JW, Armbrust EV, Stahl DA (2014) Marine ammonia-oxidizing archaeal isolates display obligate mixotrophy and wide ecotypic variation. Proc Natl Acad Sci USA 111(34):12504–12509.  https://doi.org/10.1073/pnas.1324115111 PubMedCrossRefGoogle Scholar
  102. Quan ZX, Rhee SK, Zuo JE, Yang Y, Bae JW, Park JR, Lee ST, Park YH (2008) Diversity of ammonium-oxidizing bacteria in a granular sludge anaerobic ammonium-oxidizing (anammox) reactor. Environ Microbiol 10(11):3130–3139.  https://doi.org/10.1111/j.1462-2920.2008.01642.x PubMedCrossRefGoogle Scholar
  103. Rabalais NN, Turner RE, Wiseman WJ (2001) Hypoxia in the Gulf of Mexico. J Environ Qual 30(2):320–329PubMedCrossRefGoogle Scholar
  104. Ravishankara AR, Daniel JS, Portmann RW (2009) Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326(5949):123–125.  https://doi.org/10.1126/science.1176985 PubMedCrossRefGoogle Scholar
  105. Redfield AC (1934) On the proportions of organic derivations in seawater and their relation to the composition of plankton. In: Daniel RJ (ed) James Johnson memorial volume. University Press of Liverpool, Liverpool, pp 177–192Google Scholar
  106. Reiset J (1856) Expériences sur la putréfaction et sur la formatoin des fumiers. CR Acad Sci 42:53–59Google Scholar
  107. Rich JJ, Dale OR, Song B, Ward BB (2008) Anaerobic ammonium oxidation (Anammox) in Chesapeake Bay sediments. Microb Ecol 55(2):311–320.  https://doi.org/10.1007/s00248-007-9277-3 PubMedCrossRefGoogle Scholar
  108. Richards FA (1965) Chemical observations in some anoxic, sulfide-bearing basins and fjords. In: Pearson EA (ed) Advances in water pollution research, vol 3. Pergamon, London, pp 215–232Google Scholar
  109. Robertson GP, Vitousek PM (2009) Nitrogen in agriculture: balancing the cost of an essential resource. Annu Rev Environ Resour 34:97–125.  https://doi.org/10.1146/annurev.environ.032108.105046 CrossRefGoogle Scholar
  110. Rooks C, Schmid MC, Mehsana W, Trimmer M (2012) The depth-specific significance and relative abundance of anaerobic ammonium-oxidizing bacteria in estuarine sediments (Medway Estuary, UK). FEMS Microbiol Ecol 80(1):19–29.  https://doi.org/10.1111/j.1574-6941.2011.01266.x PubMedCrossRefGoogle Scholar
  111. Santoro AE (2016) The do-it-all nitrifier. Science 351(6271):342–343PubMedCrossRefGoogle Scholar
  112. Schloesing T (1873) Etude de la nitrification. CR Acad Sci 77:353–356Google Scholar
  113. Schloesing T, Muntz A (1877a) Sur la nitrification par les ferments organises. CR Acad Sci 85:1018Google Scholar
  114. Schloesing T, Muntz A (1877b) Sur la nitrification par les ferments organises. CR Acad Sci 84:301–303Google Scholar
  115. Schloesing T, Muntz A (1879) Sur la nitrification par les ferments organises. CR Acad Sci 87:1074Google Scholar
  116. Schmid M, Twachtmann U, Klein M, Strous M, Juretschko S, Jetten M, Metzger JW, Schleifer KH, Wagner M (2000) Molecular evidence for genus level diversity of bacteria capable of catalyzing anaerobic ammonium oxidation. Syst Appl Microbiol 23(1):93–106PubMedCrossRefGoogle Scholar
  117. Schmid MC, Risgaard-Petersen N, van de Vossenberg J, Kuypers MMM, Lavik G, Petersen J, Hulth S, Thamdrup B, Canfield D, Dalsgaard T, Rysgaard S, Sejr MK, Strous M, den Camp H, Jetten MSM (2007) Anaerobic ammonium-oxidizing bacteria in marine environments: widespread occurrence but low diversity. Environ Microbiol 9(6):1476–1484.  https://doi.org/10.1111/j.1462-2920.2007.01266.x PubMedCrossRefGoogle Scholar
  118. Schramm A, de Beer D, Wagner M, Amann R (1998) Identification and activities in situ of Nitrosospira and Nitrospira spp. as dominant populations in a nitrifying fluidized bed reactor. Appl Environ Microbiol 64(9):3480–3485PubMedPubMedCentralGoogle Scholar
  119. Schubert CJ, Durisch-Kaiser E, Wehrli B, Thamdrup B, Lam P, Kuypers MMM (2006) Anaerobic ammonium oxidation in a tropical freshwater system (Lake Tanganyika). Environ Microbiol 8(10):1857–1863.  https://doi.org/10.1111/j.1462-2920.2006.001074.x PubMedCrossRefGoogle Scholar
  120. Shu D, He Y, Yue H, Wang Q (2016) Metagenomic and quantitative insights into microbial communities and functional genes of nitrogen and iron cycling in twelve wastewater treatment systems. Chem Eng J 290:21–30.  https://doi.org/10.1016/j.cej.2016.01.024 CrossRefGoogle Scholar
  121. Smil V (1997) Global population and the nitrogen cycle. Sci Am 277(1):76–81CrossRefGoogle Scholar
  122. Smil V (2004) Enriching the earth: Fritz Haber, Carl Bosch, and the transformation of world food production. MIT, Cambridge, MAGoogle Scholar
  123. Smyth AR, Thompson SP, Siporin KN, Gardner WS, McCarthy MJ, Piehler MF (2013) Assessing nitrogen dynamics throughout the estuarine landscape. Estuar Coasts 36(1):44–55.  https://doi.org/10.1007/s12237-012-9554-3 CrossRefGoogle Scholar
  124. Song B, Tobias CR (2011) Molecular and stable isotope methods to detect and measure anaerobic ammonium oxidation (anammox) in aquatic ecosystems. Methods Enzymol 496:63–89.  https://doi.org/10.1016/B978-0-12-386489-5.00003-8 PubMedCrossRefGoogle Scholar
  125. Spieck E, Bock E (2005) The lithotrophic nitrite-oxidizing bacteria. In: Garrity G (ed) Bergey’s manual of systematic bacteriology. The proteobacteria, part A introductory assays, vol 2. Springer, New York, pp 149–153Google Scholar
  126. Strohm TO, Griffin B, Zumft WG, Schink B (2007) Growth yields in bacterial denitrification and nitrate ammonification. Appl Environ Microbiol 73(5):1420–1424.  https://doi.org/10.1128/AEM.02508-06 PubMedPubMedCentralCrossRefGoogle Scholar
  127. Strous M, Heijnen JJ, Kuenen JG, Jetten MSM (1998) The sequencing batch reactor as a powerful tool for the study of slowly growing anaerobic ammonium-oxidizing microorganisms. Appl Microbiol Biotechnol 50(5):589–596CrossRefGoogle Scholar
  128. Strous M, Fuerst JA, Kramer EHM, Logemann S, Muyzer G, van de Pas-Schoonen KT, Webb R, Kuenen JG, Jetten MSM (1999) Missing lithotroph identified as new planctomycete. Nature 400(6743):446–449PubMedCrossRefGoogle Scholar
  129. Teske A, Alm E, Regan JM, Toze S, Rittman BE, Stahl DA (1994) Evolutionary relationships among ammonia- and nitrite-oxidizing bacteria. J Bacteriol 176(21):6623–6630PubMedPubMedCentralCrossRefGoogle Scholar
  130. Tiedje JM (1988) Ecology of denitrification and dissimilatory reduction of nitrate to ammonia. In: AJB Z (ed) Biology of anaerobic microorganisms. Wiley-Liss, New York, pp 179–244Google Scholar
  131. Tobias CR, Anderson IC, Canuel EA, Macko SA (2001a) Nitrogen cycling through a fringing marsh-aquifer ecotone. Mar Ecol Prog Ser 210:25–39CrossRefGoogle Scholar
  132. Tobias CR, Macko SA, Anderson IC, Canuel EA, Harvey JW (2001b) Tracking the fate of a high concentration groundwater nitrate plume through a fringing marsh: a combined groundwater tracer and in situ isotope enrichment study. Limnol Oceanogr 46(8):1977–1989CrossRefGoogle Scholar
  133. Toh SK, Webb RI, Ashbolt NJ (2002) Enrichment of autotrophic anaerobic ammonium-oxidizing consortia from various wastewaters. Microb Ecol 43(1):154–167.  https://doi.org/10.1007/s00248-001-0033-9 PubMedCrossRefGoogle Scholar
  134. U.S. Environmental Protection Agency (2013) Inventory of U.S. greenhouse gas emissions and sinks: 1990–2011. United States Environmental Protection Agency, Washington, DCGoogle Scholar
  135. USDA (2011) Carbon to nitrogen ratios in cropping systems. USDA NRCS East National Technology Support Center. https://www.nrcs.usda.gov/wps/PA_NRCSConsumption/download?cid=nrcs142p2_052823&ext=pdf. Accessed 20 Oct 2015
  136. van de Vossenberg J, Rattray JE, Geerts W, Kartal B, van Niftrik L, van Donselaar EG, Damste JSS, Strous M, Jetten MSM (2008) Enrichment and characterization of marine anammox bacteria associated with global nitrogen gas production. Environ Microbiol 10(11):3120–3129.  https://doi.org/10.1111/j.1462-2920.2008.01643.x PubMedCrossRefGoogle Scholar
  137. van den Berg EM, van Dongen U, Abbas B, van Loosdrecht MCM (2015) Enrichment of DNRA bacteria in a continuous culture. ISME J 9:2153–2161.  https://doi.org/10.1038/ismej.2015.26 PubMedPubMedCentralCrossRefGoogle Scholar
  138. van Kessel MAHJ, Speth DR, Albertsen M, Nielsen PH, Op den Camp HJM, Kartal B, Jetten MSM, Lucker S (2015) Complete nitrification by a single microorganism. Nature 528(7583):555–559.  https://doi.org/10.1038/nature16459 PubMedPubMedCentralCrossRefGoogle Scholar
  139. van Niftrik L, Jetten MSM (2012) Anaerobic ammonium-oxidizing bacteria: unique microorganisms with exceptional properties. Microbiol Mol Biol Rev 76(3):585–596PubMedPubMedCentralCrossRefGoogle Scholar
  140. Vieillard AM, Fulweiler RW (2012) Impacts of long-term fertilization on salt marsh tidal creek benthic nutrient and N2 gas fluxes. Mar Ecol Prog Ser 471:11–22.  https://doi.org/10.3354/meps10013 CrossRefGoogle Scholar
  141. Vitousek PM, Menge DNL, Reed SC, Cleveland CC (2013) Biological nitrogen fixation: rates, patterns, and ecological controls in terrestrial ecosystems. Philos Trans R Soc Lond B Biol Sci 368:20130119.  https://doi.org/10.1098/rstb.2013.0119 PubMedPubMedCentralCrossRefGoogle Scholar
  142. Von Leibig J (1840) Die Organische Chemie in ihre Anwendung auf Agircultur und Physiologie Bieweg and Cohn. Braunschweig, GermanyGoogle Scholar
  143. Voss M, Bange HW, Dippner JW, Middleburg JJ, Montoya JP, Ward BB (2013) The marine nitrogen cycle: recent discoveries, uncertainties and the potential relevance of climate change. Philos Trans R Soc Lond B Biol Sci 368(1621):20130121.  https://doi.org/10.1098/rstb.2013.0121 PubMedPubMedCentralCrossRefGoogle Scholar
  144. Watson SW, Bock E, Valois FW, Waterbury JB, Schlosser U (1986) Nitrospira-marina gen-nov sp-nov—a chemolithotrophic nitrite-oxidizing bacterium. Arch Microbiol 144(1):1–7.  https://doi.org/10.1007/bf00454947 CrossRefGoogle Scholar
  145. Winogradsky S (1889) Rechereches physiologiques sur les sulfobactéries. Annales de l’Institut Pasteur 3:49–60Google Scholar
  146. Winogradsky S (1890) Sur les organismes de la nitrification. CR Acad Sci 110:1013–1016Google Scholar
  147. Woebken D, Fuchs BM, Kuypers MMM, Amann R (2007) Potential interactions of particle-associated anammox bacteria with bacterial and archaeal partners in the Namibian upwelling system. Appl Environ Microbiol 73(14):4648–4657.  https://doi.org/10.1128/aem.02774-06 PubMedPubMedCentralCrossRefGoogle Scholar
  148. Yool A, Martin AP, Fernandez C, Clark DR (2007) The significance of nitrification for oceanic new production. Nature 447:999–1002PubMedCrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Laboratory of Microbial EcologyUniversity of VirginiaCharlottesvilleUSA

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