The microbial nitrogen-cycling network

Key Points

  • Nitrogen is an essential component of all living organisms and the main nutrient limiting life on our planet. Its availability depends on diverse nitrogen-transforming reactions that are carried out by microorganisms.

  • Nitrogen-transforming microorganisms are metabolically versatile, rendering their classification as mere nitrifiers, denitrifiers and similar classes inadequate.

  • The classical nitrogen cycle consisting of distinct processes that follow each other in an orderly fashion does not exist. In nature, microorganisms form complex networks that link nitrogen-transforming reactions.

  • Microbial nitrogen-transforming networks both attenuate and exacerbate human-induced global change. They produce and consume the powerful greenhouse gas nitrous oxide, lead to eutrophication of aquatic systems and, at the same time, remove nitrogen from wastewater.

  • There are still many undiscovered nitrogen-transforming reactions that are thermodynamically feasible. The microorganisms catalysing these reactions and the involved biochemical pathways are waiting to be discovered.

Abstract

Nitrogen is an essential component of all living organisms and the main nutrient limiting life on our planet. By far, the largest inventory of freely accessible nitrogen is atmospheric dinitrogen, but most organisms rely on more bioavailable forms of nitrogen, such as ammonium and nitrate, for growth. The availability of these substrates depends on diverse nitrogen-transforming reactions that are carried out by complex networks of metabolically versatile microorganisms. In this Review, we summarize our current understanding of the microbial nitrogen-cycling network, including novel processes, their underlying biochemical pathways, the involved microorganisms, their environmental importance and industrial applications.

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Figure 1: Microbial transformations of nitrogen compounds.
Figure 2: Enzymes catalysing four key nitrogen-cycling reactions.
Figure 3: Potential nitrogen-transforming microbial networks in different ecosystems.

References

  1. 1

    Galloway, J. N. et al. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320, 889–892 (2008). A comprehensive overview of the human impact on biogeochemical nitrogen cycling.

    CAS  PubMed  Google Scholar 

  2. 2

    Erisman, J. W., Sutton, M. A., Galloway, J., Klimont, Z. & Winiwarter, W. How a century of ammonia synthesis changed the world. Nat. Geosci. 1, 636–639 (2008).

    CAS  Google Scholar 

  3. 3

    Stein, L. Y. & Klotz, M. G. The nitrogen cycle. Curr. Biol. 26, R94–R98 (2016).

    CAS  PubMed  Google Scholar 

  4. 4

    Yan, Y. et al. Nitrogen fixation island and rhizosphere competence traits in the genome of root-associated Pseudomonas stutzeri A1501. Proc. Natl Acad. Sci. USA 105, 7564–7569 (2008).

    CAS  PubMed  Google Scholar 

  5. 5

    Füssel, J. et al. Adaptability as the key to success for the ubiquitous marine nitrite oxidizer Nitrococcus. Sci. Adv. 3, e1700807 (2017).

    PubMed  PubMed Central  Google Scholar 

  6. 6

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

    CAS  PubMed  Google Scholar 

  7. 7

    Caranto, J. D. & Lancaster, K. M. Nitric oxide is an obligate bacterial nitrification intermediate produced by hydroxylamine oxidoreductase. Proc. Natl Acad. Sci. USA 114, 8217–8222 (2017).

    CAS  PubMed  Google Scholar 

  8. 8

    Maalcke, W. J. et al. Structural basis of biological NO generation by octaheme oxidoreductases. J. Biol. Chem. 289, 1228–1242 (2014).

    CAS  PubMed  Google Scholar 

  9. 9

    Ettwig, K. F. et al. Nitrite-driven anaerobic methane oxidation by oxygenic bacteria. Nature 464, 543–548 (2010). The discovery of oxygenic denitrification.

    CAS  PubMed  Google Scholar 

  10. 10

    Kartal, B. et al. Molecular mechanism of anaerobic ammonium oxidation. Nature 479, 127–130 (2011). Isolation and characterization of the unique enzyme that produces free hydrazine.

    CAS  PubMed  Google Scholar 

  11. 11

    Griffin, B. M., Schott, J. & Schink, B. Nitrite, an electron donor for anoxygenic photosynthesis. Science 316, 1870–1870 (2007). The discovery of phototrophic nitrite oxidation.

    CAS  PubMed  Google Scholar 

  12. 12

    Daims, H. et al. Complete nitrification by Nitrospira bacteria. Nature 528, 504–509 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  13. 13

    van Kessel, M. A. et al. Complete nitrification by a single microorganism. Nature 528, 555–559 (2015). Together with reference 12, this article reports the discovery of complete nitrification by a single microorganism.

    CAS  PubMed  PubMed Central  Google Scholar 

  14. 14

    Konneke, M. et al. Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437, 543–546 (2005). The discovery of ammonia-oxidizing archaea.

    PubMed  Google Scholar 

  15. 15

    Risgaard-Petersen, N. et al. Evidence for complete denitrification in a benthic foraminifer. Nature 443, 93–96 (2006).

    CAS  PubMed  Google Scholar 

  16. 16

    Thompson, A. W. et al. Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science 337, 1546–1550 (2012). Shows that the ubiquitous unicellular cyanobacterium UCYN-A forms a nitrogen-fixing symbiosis with an algae.

    CAS  PubMed  Google Scholar 

  17. 17

    Eady, R. R. Structure-function relationships of alternative nitrogenases. Chem. Rev. 96, 3013–3030 (1996).

    CAS  PubMed  Google Scholar 

  18. 18

    Zehr, J. P., Jenkins, B. D., Short, S. M. & Steward, G. F. Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ. Microbiol. 5, 539–554 (2003).

    CAS  PubMed  Google Scholar 

  19. 19

    Vitousek, P. M. & Howarth, R. W. Nitrogen limitation on land and in the sea: How can it occur? Biogeochemistry 13, 87–115 (1991).

    Google Scholar 

  20. 20

    Bothe, H., Schmitz, O., Yates, M. G. & Newton, W. E. Nitrogen Fixation and Hydrogen Metabolism in Cyanobacteria. Microbiol. Mol. Biol. Rev. 74, 529–551 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. 21

    Robson, R. L. & Postgate, J. R. Oxygen and hydrogen in biological nitrogen fixation. Annu. Rev. Microbiol. 34, 183–207 (1980).

    CAS  PubMed  Google Scholar 

  22. 22

    Berman-Frank, I., Lundgren, P. & Falkowski, P. Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. Res. Microbiol. 154, 157–164 (2003).

    CAS  PubMed  Google Scholar 

  23. 23

    Inomura, K., Bragg, J. & Follows, M. J. A quantitative analysis of the direct and indirect costs of nitrogen fixation: a model based on Azotobacter vinelandii. ISME J. 11, 166–175 (2017).

    CAS  PubMed  Google Scholar 

  24. 24

    MacKellar, D. et al. Streptomyces thermoautotrophicus does not fix nitrogen. Sci. Rep. 6, 20086 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. 25

    Martinez-Perez, C. et al. The small unicellular diazotrophic symbiont, UCYN-A, is a key player in the marine nitrogen cycle. Nat. Microbiol. 1, 16163 (2016).

    CAS  PubMed  Google Scholar 

  26. 26

    Brune, A. Symbiotic digestion of lignocellulose in termite guts. Nat. Rev. Microbiol. 12, 168–180 (2014).

    CAS  PubMed  Google Scholar 

  27. 27

    Lechene, C. P., Luyten, Y., McMahon, G. & Distel, D. L. Quantitative imaging of nitrogen fixation by individual bacteria within animal cells. Science 317, 1563–1566 (2007).

    CAS  PubMed  Google Scholar 

  28. 28

    Burris, R. H. & Roberts, G. Biological nitrogen fixation. Annu. Rev. Nutr. 13, 317–335 (1993).

    CAS  PubMed  Google Scholar 

  29. 29

    Hooper, A. B., Vannelli, T., Bergmann, D. J. & Arciero, D. M. Enzymology of the oxidation of ammonia to nitrite by bacteria. Antonie Leeuwenhoek 71, 59–67 (1997).

    CAS  PubMed  Google Scholar 

  30. 30

    Arp, D. J. & Stein, L. Y. Metabolism of inorganic N compounds by ammonia-oxidizing bacteria. Crit. Rev. Biochem. Mol. Biol. 38, 471–495 (2003).

    CAS  PubMed  Google Scholar 

  31. 31

    Prosser, J. I. & Nicol, G. W. Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ. Microbiol. 10, 2931–2941 (2008).

    CAS  Google Scholar 

  32. 32

    Wuchter, C. et al. Archaeal nitrification in the ocean. Proc. Natl Acad. Sci. USA 103, 12317–12322 (2006).

    CAS  PubMed  Google Scholar 

  33. 33

    Francis, C. A., Roberts, K. J., Beman, J. M., Santoro, A. E. & Oakley, B. B. Ubiquity and diversity of ammonia-oxidizing archaea in water columns and sediments of the ocean. Proc. Natl Acad. Sci. USA 102, 14683–14688 (2005). Shows that ammonia-oxidizing archaea are ubiquitous in the oceans.

    CAS  PubMed  Google Scholar 

  34. 34

    Leininger, S. et al. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442, 806–809 (2006). Shows that archaea are major ammonia oxidizers in soils.

    CAS  Google Scholar 

  35. 35

    Lehtovirta-Morley, L. E., Stoecker, K., Vilcinskas, A., Prosser, J. I. & Nicol, G. W. Cultivation of an obligate acidophilic ammonia oxidizer from a nitrifying acid soil. Proc. Natl Acad. Sci. USA 108, 15892–15897 (2011). The discovery of an acidophilic ammonia oxidizer.

    CAS  PubMed  Google Scholar 

  36. 36

    Tourna, M. et al. Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc. Natl Acad. Sci. USA 108, 8420–8425 (2011).

    CAS  PubMed  Google Scholar 

  37. 37

    Burton, S. A. & Prosser, J. I. Autotrophic ammonia oxidation at low pH through urea hydrolysis. Appl. Environ. Microbiol. 67, 2952–2957 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. 38

    Palatinszky, M. et al. Cyanate as an energy source for nitrifiers. Nature 524, 105–108 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. 39

    Kits, K. D. et al. Kinetic analysis of a complete nitrifier reveals an oligotrophic lifestyle. Nature 549, 269–272 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  40. 40

    Hakemian, A. S. & Rosenzweig, A. C. The biochemistry of methane oxidation. Annu. Rev. Biochem. 76, 223–241 (2007).

    CAS  PubMed  Google Scholar 

  41. 41

    Stein, L. Y. & Klotz, M. G. Nitrifying and denitrifying pathways of methanotrophic bacteria. Biochem. Soc. Trans. 39, 1826–1831 (2011).

    CAS  PubMed  Google Scholar 

  42. 42

    Stoecker, K. et al. Cohn's Crenothrix is a filamentous methane oxidizer with an unusual methane monooxygenase. Proc. Natl Acad. Sci. USA 103, 2363–2367 (2006).

    CAS  PubMed  Google Scholar 

  43. 43

    Oswald, K. et al. Crenothrix are major methane consumers in stratified lakes. ISME J. 11, 2124–2140 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. 44

    Simon, J. & Klotz, M. G. Diversity and evolution of bioenergetic systems involved in microbial nitrogen compound transformations. Biochim. Biophys. Acta 1827, 114–135 (2013). An extensive overview of enzymes involved in microbial nitrogen transformations.

    CAS  PubMed  Google Scholar 

  45. 45

    Kozlowski, J. A., Stieglmeier, M., Schleper, C., Klotz, M. G. & Stein, L. Y. Pathways and key intermediates required for obligate aerobic ammonia-dependent chemolithotrophy in bacteria and Thaumarchaeota. ISME J. 10, 1836–1845 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. 46

    Kartal, B. et al. How to make a living from anaerobic ammonium oxidation. FEMS Microbiol. Rev. 37, 428–461 (2013).

    CAS  PubMed  Google Scholar 

  47. 47

    Ren, T., Roy, R. & Knowles, R. Production and consumption of nitric oxide by three methanotrophic bacteria. Appl. Environ. Microbiol. 66, 3891–3897 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. 48

    Nyerges, G. & Stein, L. Y. Ammonia cometabolism and product inhibition vary considerably among species of methanotrophic bacteria. FEMS Microbiol. Lett. 297, 131–136 (2009).

    CAS  PubMed  Google Scholar 

  49. 49

    Schott, J., Griffin, B. M. & Schink, B. Anaerobic phototrophic nitrite oxidation by Thiocapsa sp. strain KS1 and Rhodopseudomonas sp. strain LQ17. Microbiology 156, 2428–2437 (2010).

    CAS  PubMed  Google Scholar 

  50. 50

    Strous, M. et al. Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440, 790–794 (2006).

    PubMed  Google Scholar 

  51. 51

    Strous, M. et al. Missing lithotroph identified as new planctomycete. Nature 400, 446–449 (1999). The discovery of anaerobic ammonium-oxidizing bacteria.

    CAS  PubMed  Google Scholar 

  52. 52

    Koch, H. et al. Growth of nitrite-oxidizing bacteria by aerobic hydrogen oxidation. Science 345, 1052–1054 (2014).

    CAS  PubMed  Google Scholar 

  53. 53

    Koch, H. et al. Expanded metabolic versatility of ubiquitous nitrite-oxidizing bacteria from the genus Nitrospira. Proc. Natl Acad. Sci. USA 112, 11371–11376 (2015).

    CAS  PubMed  Google Scholar 

  54. 54

    Maia, L. B. & Moura, J. J. How biology handles nitrite. Chem. Rev. 114, 5273–5357 (2014).

    CAS  PubMed  Google Scholar 

  55. 55

    Pachiadaki, M. G. et al. Major role of nitrite-oxidizing bacteria in dark ocean carbon fixation. Science 358, 1046–1051 (2017).

    CAS  PubMed  Google Scholar 

  56. 56

    Philippot, L., Hallin, S. & Schloter, M. Ecology of denitrifying prokaryotes in agricultural soil. Adv. Agronomy 96, 249–305 (2007).

    CAS  Google Scholar 

  57. 57

    Lam, P. & Kuypers, M. M. Microbial nitrogen-cycling processes in oxygen minimum zones. Annu. Rev. Mar. Sci. 3, 317–345 (2011).

    Google Scholar 

  58. 58

    Kraft, B. et al. The environmental controls that govern the end product of bacterial nitrate respiration. Science 345, 676–679 (2014).

    CAS  PubMed  Google Scholar 

  59. 59

    Lundberg, J. O., Weitzberg, E. & Gladwin, M. T. The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat. Rev. Drug Discov. 7, 156–167 (2008).

    CAS  PubMed  Google Scholar 

  60. 60

    Moreno-Vivian, C., Cabello, P., Martinez-Luque, M., Blasco, R. & Castillo, F. Prokaryotic nitrate reduction: molecular properties and functional distinction among bacterial nitrate reductases. J. Bacteriol. 181, 6573–6584 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. 61

    Preisler, A. et al. Biological and chemical sulfide oxidation in a Beggiatoa inhabited marine sediment. ISME J. 1, 341–353 (2007).

    CAS  PubMed  Google Scholar 

  62. 62

    Tsementzi, D. et al. SAR11 bacteria linked to ocean anoxia and nitrogen loss. Nature 536, 179–183 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  63. 63

    Lam, P. et al. Revising the nitrogen cycle in the Peruvian oxygen minimum zone. Proc. Natl Acad. Sci. USA 106, 4752–4757 (2009).

    CAS  PubMed  Google Scholar 

  64. 64

    Bristow, L. A. et al. N2 production rates limited by nitrite availability in the Bay of Bengal oxygen minimum zone. Nat. Geosci. 10, 24–29 (2017).

    CAS  Google Scholar 

  65. 65

    Zumft, W. G. Cell biology and molecular basis of denitrification. Microbiol. Mol. Biol. Rev. 61, 533–616 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  66. 66

    Haroon, M. F. et al. Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage. Nature 500, 567–570 (2013). The discovery of nitrate-reducing methanotrophic archaea.

    CAS  PubMed  Google Scholar 

  67. 67

    Ettwig, K. F. et al. Archaea catalyze iron-dependent anaerobic oxidation of methane. Proc. Natl Acad. Sci. USA 113, 12792–12796 (2016).

    CAS  PubMed  Google Scholar 

  68. 68

    Cardoso, R. B. et al. Sulfide oxidation under chemolithoautotrophic denitrifying conditions. Biotechnol. Bioengineer. 95, 1148–1157 (2006).

    CAS  Google Scholar 

  69. 69

    Weber, K. A., Achenbach, L. A. & Coates, J. D. Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nat. Rev. Microbiol. 4, 752–764 (2006).

    CAS  PubMed  Google Scholar 

  70. 70

    Gruber, N. The marine nitrogen cycle: overview and challenges. Nitrogen Marine Environ. 2, 1–50 (2008).

    Google Scholar 

  71. 71

    Stolz, J. F. & Basu, P. Evolution of nitrate reductase: molecular and structural variations on a common function. Chembiochem 3, 198–206 (2002).

    CAS  PubMed  Google Scholar 

  72. 72

    Malm, S. et al. The roles of the nitrate reductase NarGHJI, the nitrite reductase NirBD and the response regulator GlnR in nitrate assimilation of Mycobacterium tuberculosis. Microbiology 155, 1332–1339 (2009).

    CAS  PubMed  Google Scholar 

  73. 73

    Blöchl, E. et al. Pyrolobus fumarii, gen. and sp. nov., represents a novel group of archaea, extending the upper temperature limit for life to 113 C. Extremophiles 1, 14–21 (1997).

    PubMed  Google Scholar 

  74. 74

    Kamp, A., de Beer, D., Nitsch, J. L., Lavik, G. & Stief, P. Diatoms respire nitrate to survive dark and anoxic conditions. Proc. Natl Acad. Sci. USA 108, 5649–5654 (2011).

    CAS  PubMed  Google Scholar 

  75. 75

    Zhou, Z. et al. Ammonia fermentation, a novel anoxic metabolism of nitrate by fungi. J. Biol. Chem. 277, 1892–1896 (2002).

    CAS  PubMed  Google Scholar 

  76. 76

    Tikhonova, T. V. et al. Molecular and catalytic properties of a novel cytochrome c nitrite reductase from nitrate-reducing haloalkaliphilic sulfur-oxidizing bacterium Thioalkalivibrio nitratireducens. Biochim. Biophys. Acta 1764, 715–723 (2006).

    CAS  PubMed  Google Scholar 

  77. 77

    Atkinson, S. J., Mowat, C. G., Reid, G. A. & Chapman, S. K. An octaheme c-type cytochrome from Shewanella oneidensis can reduce nitrite and hydroxylamine. FEBS Lett. 581, 3805–3808 (2007).

    CAS  PubMed  Google Scholar 

  78. 78

    Einsle, O. et al. Structure of cytochrome c nitrite reductase. Nature 400, 476–480 (1999).

    CAS  PubMed  Google Scholar 

  79. 79

    Haase, D., Hermann, B., Einsle, O. & Simon, J. Epsilonproteobacterial hydroxylamine oxidoreductase (εHao): characterization of a 'missing link' in the multihaem cytochrome c family. Mol. Microbiol. 105, 127–138 (2017).

    CAS  PubMed  Google Scholar 

  80. 80

    Tiedje, J. M. in in Biology of Anaerobic Microorganisms (ed. Zehnder, A. J. B.) 179–244 (Wiley, New York, NY, USA, 1988).

    Google Scholar 

  81. 81

    Brunet, R. & Garcia-Gil, L. Sulfide-induced dissimilatory nitrate reduction to ammonia in anaerobic freshwater sediments. FEMS Microbiol. Ecol. 21, 131–138 (1996).

    CAS  Google Scholar 

  82. 82

    Seitz, H.-J. & Cypionka, H. Chemolithotrophic growth of Desulfovibrio desulfuricans with hydrogen coupled to ammonification of nitrate or nitrite. Arch. Microbiol. 146, 63–67 (1986).

    CAS  Google Scholar 

  83. 83

    Robertson, E. K., Roberts, K. L., Burdorf, L. D. W., Cook, P. & Thamdrup, B. Dissimilatory nitrate reduction to ammonium coupled to Fe(II) oxidation in sediments of a periodically hypoxic estuary. Limnol. Oceanogr. 61, 365–381 (2016).

    CAS  Google Scholar 

  84. 84

    Rütting, T., Boeckx, P., Müller, C. & Klemedtsson, L. Assessment of the importance of dissimilatory nitrate reduction to ammonium for the terrestrial nitrogen cycle. Biogeosciences 8, 1779–1791 (2011).

    Google Scholar 

  85. 85

    Burgin, A. J. & Hamilton, S. K. Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways. Front. Ecol. Environ. 5, 89–96 (2007).

    Google Scholar 

  86. 86

    Lomas, M. W. & Lipschultz, F. Forming the primary nitrite maximum: nitrifiers or phytoplankton? Limnol. Oceanogr. 51, 2453–2467 (2006).

    CAS  Google Scholar 

  87. 87

    Graf, D. R., Jones, C. M. & Hallin, S. Intergenomic comparisons highlight modularity of the denitrification pathway and underpin the importance of community structure for N2O emissions. PloS ONE 9, e114118 (2014).

    PubMed  PubMed Central  Google Scholar 

  88. 88

    Bartossek, R., Nicol, G. W., Lanzen, A., Klenk, H. P. & Schleper, C. Homologues of nitrite reductases in ammonia-oxidizing archaea: diversity and genomic context. Environ. Microbiol. 12, 1075–1088 (2010).

    CAS  PubMed  Google Scholar 

  89. 89

    Kartal, B. & Keltjens, J. T. Anammox biochemistry: a tale of heme c proteins. Trends Biochem. Sci. 41, 998–1011 (2016).

    CAS  PubMed  Google Scholar 

  90. 90

    Fang, F. C. Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat. Rev. Microbiol. 2, 820–832 (2004).

    CAS  PubMed  Google Scholar 

  91. 91

    Hallin, S., Philippot, L., Löffler, F. E., Sanford, R. A. & Jones, C. M. Genomics and ecology of novel N2O-reducing microorganisms. Trends Microbiol. 26, 43–55 (2018).

    CAS  PubMed  Google Scholar 

  92. 92

    Ravishankara, A. R., Daniel, J. S. & Portmann, R. W. Nitrous Oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326, 123–125 (2009).

    CAS  PubMed  Google Scholar 

  93. 93

    Saraiva, L. M., Vicente, J. B. & Teixeira, M. The role of the flavodiiron proteins in microbial nitric oxide detoxification. Adv. Microb. Physiol. 49, 77–129 (2004).

    CAS  PubMed  Google Scholar 

  94. 94

    Rodrigues, R. et al. Desulfovibrio gigas flavodiiron protein affords protection against nitrosative stress in vivo. J. Bacteriol. 188, 2745–2751 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  95. 95

    Shoun, H., Fushinobu, S., Jiang, L., Kim, S.-W. & Wakagi, T. Fungal denitrification and nitric oxide reductase cytochrome P450nor. Phil. Trans. R. Soc. B Biol Sci. 367, 1186–1194 (2012).

    CAS  Google Scholar 

  96. 96

    Wang, J. et al. The roles of the hybrid cluster protein, Hcp, and its reductase, Hcr, in high affinity nitric oxide reduction that protects anaerobic cultures of Escherichia coli against nitrosative stress. Mol. Microbiol. 100, 877–892 (2016).

    CAS  PubMed  Google Scholar 

  97. 97

    Hino, T. et al. Structural basis of biological N2O generation by bacterial nitric oxide reductase. Science 330, 1666–1670 (2010).

    CAS  PubMed  Google Scholar 

  98. 98

    Matsumoto, Y. et al. Crystal structure of quinol-dependent nitric oxide reductase from Geobacillus stearothermophilus. Nat. Struct. Mol. Biol. 19, 238–245 (2012).

    CAS  PubMed  Google Scholar 

  99. 99

    Al-Attar, S. & de Vries, S. An electrogenic nitric oxide reductase. FEBS Lett. 589, 2050–2057 (2015).

    CAS  PubMed  Google Scholar 

  100. 100

    Liu, S. et al. Abiotic conversion of extracellular NH2OH contributes to N2O emission during ammonia oxidation. Environ. Sci. Technol. 51, 13122–13132 (2017).

    CAS  PubMed  Google Scholar 

  101. 101

    Stocker, T. F. et al. IPCC, 2013: Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (Cambridge Univ. Press, 2013).

    Google Scholar 

  102. 102

    Davidson, E. A. The contribution of manure and fertilizer nitrogen to atmospheric nitrous oxide since 1860. Nat. Geosci. 2, 659–662 (2009).

    CAS  Google Scholar 

  103. 103

    Crutzen, P., Mosier, A., Smith, K. & Winiwarter, W. N2O release from agro-biofuel production negates global warming reduction by replacing fossil fuels. Atmos. Chem. Phys. 8, 389–395 (2008).

    CAS  Google Scholar 

  104. 104

    Ettwig, K. F. et al. Bacterial oxygen production in the dark. Front. Microbiol. 3, 273 (2012).

    PubMed  PubMed Central  Google Scholar 

  105. 105

    Zumft, W. G. & Kroneck, P. M. Respiratory transformation of nitrous oxide (N2O) to dinitrogen by Bacteria and Archaea. Adv. Microb. Physiol. 52, 107–227 (2006).

    Google Scholar 

  106. 106

    Cabello, P., Roldan, M. D. & Moreno-Vivian, C. Nitrate reduction and the nitrogen cycle in archaea. Microbiology 150, 3527–3546 (2004).

    CAS  PubMed  Google Scholar 

  107. 107

    Simon, J., Einsle, O., Kroneck, P. M. & Zumft, W. G. The unprecedented nos gene cluster of Wolinella succinogenes encodes a novel respiratory electron transfer pathway to cytochrome c nitrous oxide reductase. FEBS Lett. 569, 7–12 (2004).

    CAS  PubMed  Google Scholar 

  108. 108

    Sanford, R. A. et al. Unexpected nondenitrifier nitrous oxide reductase gene diversity and abundance in soils. Proc. Natl Acad. Sci. USA 109, 19709–19714 (2012).

    CAS  PubMed  Google Scholar 

  109. 109

    Jones, C. M. et al. Recently identified microbial guild mediates soil N2O sink capacity. Nat. Climate Change 4, 801–805 (2014).

    CAS  Google Scholar 

  110. 110

    Piña-Ochoa, E. et al. Widespread occurrence of nitrate storage and denitrification among Foraminifera and Gromiida. Proc. Natl Acad. Sci. USA 107, 1148–1153 (2010).

    PubMed  Google Scholar 

  111. 111

    Philippot, L., Andert, J., Jones, C. M., Bru, D. & Hallin, S. Importance of denitrifiers lacking the genes encoding the nitrous oxide reductase for N2O emissions from soil. Global Change Biol. 17, 1497–1504 (2011).

    Google Scholar 

  112. 112

    Codispoti, L. & Christensen, J. Nitrification, denitrification and nitrous oxide cycling in the eastern tropical South Pacific Ocean. Mar. Chem. 16, 277–300 (1985).

    CAS  Google Scholar 

  113. 113

    Van de Graaf, A. A., de Bruijn, P., Robertson, L. A., Jetten, M. S. & Kuenen, J. G. Autotrophic growth of anaerobic ammonium-oxidizing micro-organisms in a fluidized bed reactor. Microbiology 142, 2187–2196 (1996).

    CAS  Google Scholar 

  114. 114

    Mulder, A., Vandegraaf, A. A., Robertson, L. A. & Kuenen, J. G. Anaerobic ammonium oxidation discovered in a denitrifying fluidized bed reactor. FEMS Microbiol. Ecol. 16, 177–183 (1995). The discovery of anaerobic ammonium oxidation.

    CAS  Google Scholar 

  115. 115

    Dietl, A. et al. The inner workings of the hydrazine synthase multiprotein complex. Nature 527, 394–397 (2015).

    CAS  PubMed  Google Scholar 

  116. 116

    Jetten, M. S. M., den Camp, H. J. M. O., Gijs Kuenen, J. & Strous, M. in Bergey's Manual of Systematics of Archaea and Bacteria (ed. Whitman, W. B.) https://doi.org/10.1002/9781118960608.fbm00160 (John Wiley & Sons, Ltd, 2015).

    Google Scholar 

  117. 117

    Harhangi, H. R. et al. Hydrazine synthase, a unique phylomarker with which to study the presence and biodiversity of anammox bacteria. Appl. Environ. Microbiol. 78, 752–758 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  118. 118

    Wang, Y. et al. Co-occurrence and distribution of nitrite-dependent anaerobic ammonium and methane-oxidizing bacteria in a paddy soil. Fems Microbiol. Lett. 336, 79–88 (2012).

    CAS  PubMed  Google Scholar 

  119. 119

    Maalcke, W. J. et al. Characterization of anammox hydrazine dehydrogenase, a key N2-producing enzyme in the global nitrogen cycle. J. Biol. Chem. 291, 17077–17092 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  120. 120

    Neumann, S. et al. Isolation and characterization of a prokaryotic cell organelle from the anammox bacterium Kuenenia stuttgartiensis. Mol. Microbiol. 94, 794–802 (2014).

    CAS  PubMed  Google Scholar 

  121. 121

    de Almeida, N. M. et al. Membrane-bound electron transport systems of an anammox bacterium: a complexome analysis. Biochim. Biophys. Acta 1857, 1694–1704 (2016).

    CAS  PubMed  Google Scholar 

  122. 122

    de Almeida, N. M. et al. Immunogold localization of key metabolic enzymes in the anammoxosome and on the tubule-like structures of Kuenenia stuttgartiensis. J. Bacteriol. 197, 2432–2441 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  123. 123

    Kuypers, M. M. et al. Anaerobic ammonium oxidation by anammox bacteria in the Black Sea. Nature 422, 608–611 (2003). The first detection of anaerobic ammonium-oxidizing bacteria in the environment.

    CAS  PubMed  Google Scholar 

  124. 124

    Kuypers, M. M. M. et al. Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proc. Natl Acad. Sci. USA 102, 6478–6483 (2005).

    CAS  PubMed  Google Scholar 

  125. 125

    Devol, A. H. Nitrogen cycle: Solution to a marine mystery. Nature 422, 575–576 (2003).

    CAS  PubMed  Google Scholar 

  126. 126

    Zhu, G. et al. Anaerobic ammonia oxidation in a fertilized paddy soil. ISME J. 5, 1905–1912 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  127. 127

    Bronk, D. A. & Steinberg, D. K. in Nitrogen in the in Marine Environment 2nd edn 385–467 (Academic Press, San Diego, 2008).

    Google Scholar 

  128. 128

    Sunagawa, S. et al. Structure and function of the global ocean microbiome. Science 348, 1261359 (2015).

    Google Scholar 

  129. 129

    Gruber, N. & Galloway, J. N. An Earth-system perspective of the global nitrogen cycle. Nature 451, 293–296 (2008).

    CAS  PubMed  Google Scholar 

  130. 130

    Vaksmaa, A. et al. Enrichment of anaerobic nitrate-dependent methanotrophic 'Candidatus Methanoperedens nitroreducens' archaea from an Italian paddy field soil. Appl. Microbiol. Biotechnol. 101, 7075–7084 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  131. 131

    Martens-Habbena, W., Berube, P. M., Urakawa, H., de la Torre, J. R. & Stahl, D. A. Ammonia oxidation kinetics determine niche separation of nitrifying Archaea and Bacteria. Nature 461, 976–979 (2009).

    CAS  Google Scholar 

  132. 132

    Schleper, C. & Nicol, G. W. Ammonia-oxidising archaea — physiology, ecology and evolution. Adv. Microb. Physiol. 57, 41 (2010).

    Google Scholar 

  133. 133

    Pjevac, P. et al. AmoA-targeted polymerase chain reaction primers for the specific detection and quantification of comammox Nitrospira in the environment. Front. Microbiol. 8, 1508 (2017).

    PubMed  PubMed Central  Google Scholar 

  134. 134

    Oshiki, M. et al. Nitrate-dependent ferrous iron oxidation by anaerobic ammonium oxidation (anammox) bacteria. Appl. Environ. Microbiol. 79, 4087–4093 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  135. 135

    Ferousi, C. et al. Iron assimilation and utilization in anaerobic ammonium oxidizing bacteria. Curr. Opin. Chem. Biol. 37, 129–136 (2017).

    CAS  PubMed  Google Scholar 

  136. 136

    Jensen, M. M. et al. Intensive nitrogen loss over the Omani Shelf due to anammox coupled with dissimilatory nitrite reduction to ammonium. ISME J. 5, 1660–1670 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  137. 137

    Jones, C. M., Graf, D. R. H., Bru, D., Philippot, L. & Hallin, S. The unaccounted yet abundant nitrous oxide-reducing microbial community: a potential nitrous oxide sink. ISME J. 7, 417–426 (2013).

    CAS  PubMed  Google Scholar 

  138. 138

    Heylen, K. & Keltjens, J. Redundancy and modularity in membrane-associated dissimilatory nitrate reduction in Bacillus. Front. Microbiol. 3, 371 (2012).

    PubMed  PubMed Central  Google Scholar 

  139. 139

    Canfield, D. E., Thamdrup, B. & Kristensen, E. Aquatic Geomicrobiology (Elsevier Academic Press, 2005).

    Google Scholar 

  140. 140

    Sutton, M. A. et al. The European Nitrogen Assessment: Sources, Effects and Policy Perspectives (Cambridge Univ. Press, 2011).

    Google Scholar 

  141. 141

    Canfield, D. E., Glazer, A. N. & Falkowski, P. G. The evolution and future of Earth's nitrogen cycle. Science 330, 192–196 (2010).

    CAS  PubMed  Google Scholar 

  142. 142

    Duce, R. A. et al. Impacts of atmospheric anthropogenic nitrogen on the open ocean. Science 320, 893–897 (2008).

    CAS  PubMed  Google Scholar 

  143. 143

    Grosskopf, T. et al. Doubling of marine dinitrogen-fixation rates based on direct measurements. Nature 488, 361–364 (2012).

    CAS  PubMed  Google Scholar 

  144. 144

    McGroddy, M. E., Daufresne, T. & Hedin, L. O. Scaling of C:N:P stoichiometry in forests worldwide: implications of terrestrial redfield-type ratios. Ecology 85, 2390–2401 (2004).

    Google Scholar 

  145. 145

    Rittmann, B. E. & McCarty, P. L. Environmental Biotechnology: Principles and Applications (Tata McGraw-Hill Education, 2012).

    Google Scholar 

  146. 146

    Kartal, B., Kuenen, J.v. & Van Loosdrecht, M. Sewage treatment with anammox. Science 328, 702–703 (2010).

    CAS  PubMed  Google Scholar 

  147. 147

    Lackner, S. et al. Full-scale partial nitritation/anammox experiences — an application survey. Water Res. 55, 292–303 (2014).

    CAS  PubMed  Google Scholar 

  148. 148

    Park, H.-D., Wells, G. F., Bae, H., Criddle, C. S. & Francis, C. A. Occurrence of ammonia-oxidizing archaea in wastewater treatment plant bioreactors. Appl. Environ. Microbiol. 72, 5643–5647 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  149. 149

    Luesken, F. A. et al. Simultaneous nitrite-dependent anaerobic methane and ammonium oxidation processes. Appl. Environ. Microbiol. 77, 6802–6807 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  150. 150

    Starkenburg, S. R., Arp, D. J. & Bottomley, P. J. Expression of a putative nitrite reductase and the reversible inhibition of nitrite-dependent respiration by nitric oxide in Nitrobacter winogradskyi Nb-255. Environ. Microbiol. 10, 3036–3042 (2008).

    CAS  PubMed  Google Scholar 

  151. 151

    Freitag, A. & Bock, E. Energy conservation in Nitrobacter. FEMS Microbiol. Lett. 66, 157–162 (1990).

    CAS  Google Scholar 

  152. 152

    Wijma, H. J., Canters, G. W., de Vries, S. & Verbeet, M. P. Bidirectional catalysis by copper-containing nitrite reductase. Biochemistry 43, 10467–10474 (2004).

    CAS  PubMed  Google Scholar 

  153. 153

    Sousa, F. L. et al. The superfamily of heme–copper oxygen reductases: types and evolutionary considerations. Biochim. Biophys. Acta 1817, 629–637 (2012).

    CAS  PubMed  Google Scholar 

  154. 154

    Rothery, R. A., Workun, G. J. & Weiner, J. H. The prokaryotic complex iron–sulfur molybdoenzyme family. Biochim. Biophys. Acta 1778, 1897–1929 (2008).

    CAS  PubMed  Google Scholar 

  155. 155

    Ishii, S., Ikeda, S., Minamisawa, K. & Senoo, K. Nitrogen cycling in rice paddy environments: past achievements and future challenges. Microbes Environ. 26, 282–292 (2011).

    PubMed  Google Scholar 

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Acknowledgements

The authors thank W. Mohr and J. Milucka (Max Planck Institute for Marine Microbiology, Bremen, Germany) for discussions. This work was supported by the Max Planck Society (MPG) and the European Research Council Grant 640422 to B.K.

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M.M.M.K., H.K.M. and B.K. researched data for the article, made substantial contributions to discussions of the content, wrote the article and reviewed and edited the manuscript before submission.

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Correspondence to Marcel M. M. Kuypers.

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Glossary

Reductants

The electron-donating compounds in a redox reaction.

Oxygenic phototrophs

Organisms that obtain energy from light and use water as the electron donor, forming molecular oxygen and sugar as products.

Bacteriocytes

Special cells in animals that contain endosymbiotic bacteria.

Thaumarchaeota

The phylum that contains the ammonia-oxidizing archaea.

Acidophilic

The propensity of organisms to grow in acidic environments (pH <6).

Methanotrophs

Organisms that oxidize methane to conserve energy.

NC10

A candidate bacterial phylum, named after the Nullarbor Caves in Australia, that contains 'Candidatus Methylomirabilis oxyfera', which is the first organism discovered that performs methane oxidation coupled to oxygenic denitrification.

Endergonic

A reaction that requires energy input.

Verrucomicrobia

A bacterial phylum with only a few described species, some of which appear to be important in the methane cycle.

Anoxygenic phototrophs

These microorganisms obtain energy from light and use compounds such as hydrogen sulfide instead of water as an electron donor and thus do not produce molecular oxygen.

Eutrophication

An increased input of nutrients that leads to excessive growth of algae or cyanobacteria.

Proton motive force

Proton dislocation creates a difference of charge and pH between two sides of a cell membrane and thereby generates an electrochemical potential, which is used for energy conservation.

Anaerobic sludge digesters

Bioreactors in which excess microbial biomass (sludge) produced during wastewater treatment is anaerobically converted to carbon dioxide, methane, ammonium and reduced sulfur compounds.

Primary nitrite maxima

The peak in nitrite concentrations at the base of the euphotic zone.

Nitric oxide dismutation

Two molecules of nitric oxide are disproportionated into one molecule of molecular oxygen and one molecule of dinitrogen gas.

Comproportionation

A chemical reaction in which two reactants containing the same element with a different oxidation state react to create a product with a single oxidation state.

Anammoxosome

A bacterial organelle found in anaerobic ammonium oxidizing (anammox) bacteria that is the only known prokaryotic membrane-bound structure that is equally divided into daughter cells upon cell division.

Exergonic

A reaction that results in the release of free energy.

Disproportionation

A chemical reaction in which a reactant is split into two species containing the same element with different oxidation states, one more oxidized and the other more reduced than the reactant.

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Kuypers, M., Marchant, H. & Kartal, B. The microbial nitrogen-cycling network. Nat Rev Microbiol 16, 263–276 (2018). https://doi.org/10.1038/nrmicro.2018.9

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