Biology:Nitrogen fixation

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Short description: Conversion of molecular nitrogen into biologically accessible nitrogen compounds


Nitrogen fixation is a chemical process by which molecular nitrogen (N2), which has a strong triple covalent bond, is converted into ammonia (NH3) or related nitrogenous compounds, typically in soil or aquatic systems[1] but also in industry. The nitrogen in air is molecular dinitrogen, a relatively nonreactive molecule that is metabolically useless to all but a few microorganisms. Biological nitrogen fixation or diazotrophy is an important microbe-mediated process that converts dinitrogen (N2) gas to ammonia (NH3) using the nitrogenase protein complex (Nif).[2][3]

Nitrogen fixation is essential to life because fixed inorganic nitrogen compounds are required for the biosynthesis of all nitrogen-containing organic compounds, such as amino acids and proteins, nucleoside triphosphates and nucleic acids. As part of the nitrogen cycle, it is essential for agriculture and the manufacture of fertilizer. It is also, indirectly, relevant to the manufacture of all nitrogen chemical compounds, which include some explosives, pharmaceuticals, and dyes.

Nitrogen fixation is carried out naturally in soil by microorganisms termed diazotrophs that include bacteria, such as Azotobacter, and archaea. Some nitrogen-fixing bacteria have symbiotic relationships with plant groups, especially legumes.[4] Looser non-symbiotic relationships between diazotrophs and plants are often referred to as associative, as seen in nitrogen fixation on rice roots. Nitrogen fixation occurs between some termites and fungi.[5] It occurs naturally in the air by means of NOx production by lightning.[6][7]

All biological reactions involving the process of nitrogen fixation are catalyzed by enzymes called nitrogenases.[8] These enzymes contain iron, often with a second metal, usually molybdenum but sometimes vanadium.

History

Schematic representation of the nitrogen cycle. Abiotic nitrogen fixation has been omitted.

Biological nitrogen fixation was discovered by Jean-Baptiste Boussingault in 1838.[9][10] Later, in 1880, the process by which it happens was discovered by German agronomist Hermann Hellriegel and Hermann Wilfarth [de][11] and was fully described by Dutch microbiologist Martinus Beijerinck.[12]

"The protracted investigations of the relation of plants to the acquisition of nitrogen begun by Saussure, Ville, Lawes and Gilbert and others culminated in the discovery of symbiotic fixation by Hellriegel and Wilfarth in 1887."[13]

"Experiments by Bossingault in 1855 and Pugh, Gilbert & Lawes in 1887 had shown that nitrogen did not enter the plant directly. The discovery of the role of nitrogen fixing bacteria by Herman Hellriegel and Herman Wilfarth in 1886-8 would open a new era of soil science."[14]

In 1901 Beijerinck showed that Azotobacter chroococcum was able to fix atmospheric nitrogen. This was the first species of the azotobacter genus, so-named by him. It is also the first known diazotroph, species that use diatomic nitrogen as a step in the complete nitrogen cycle.[citation needed]

Biological

Biological nitrogen fixation (BNF) occurs when atmospheric nitrogen is converted to ammonia by a nitrogenase enzyme.[1] The overall reaction for BNF is:

[math]\ce{ N2 + 16ATP + 16H2O + 8e- + 8H+ -> 2NH3 +H2 + 16ADP + 16 }[/math][math]\displaystyle{ \text{P}_i }[/math]

The process is coupled to the hydrolysis of 16 equivalents of ATP and is accompanied by the co-formation of one equivalent of H2.[15] The conversion of N2 into ammonia occurs at a metal cluster called FeMoco, an abbreviation for the iron-molybdenum cofactor. The mechanism proceeds via a series of protonation and reduction steps wherein the FeMoco active site hydrogenates the N2 substrate.[16] In free-living diazotrophs, nitrogenase-generated ammonia is assimilated into glutamate through the glutamine synthetase/glutamate synthase pathway. The microbial nif genes required for nitrogen fixation are widely distributed in diverse environments.[17]

For example, decomposing wood, which generally has a low nitrogen content, has been shown to host a diazotrophic community.[18][19] The bacteria enrich the wood substrate with nitrogen through fixation, thus enabling deadwood decomposition by fungi.[20]

Nitrogenases are rapidly degraded by oxygen. For this reason, many bacteria cease production of the enzyme in the presence of oxygen. Many nitrogen-fixing organisms exist only in anaerobic conditions, respiring to draw down oxygen levels, or binding the oxygen with a protein such as leghemoglobin.[1]

Importance of nitrogen

Atmospheric nitrogen is inaccessible to most organisms,[21] because its triple covalent bond is very strong. Most take up fixed nitrogen from various sources. For every 100 atoms of carbon, roughly 2 to 20 atoms of nitrogen are assimilated. The atomic ratio of carbon (C) : nitrogen (N) : phosphorus (P) observed on average in planktonic biomass was originally described by Alfred Redfield,[22] who determined the stoichiometric relationship between C:N:P atoms, The Redfield Ratio, to be 106:16:1.[22]

Nitrogenase

Main page: Biology:Nitrogenase

The protein complex nitrogenase is responsible for catalyzing the reduction of nitrogen gas (N2) to ammonia (NH3).[23] In Cyanobacteria, this enzyme system is housed in a specialized cell called the heterocyst.[24] The production of the nitrogenase complex is genetically regulated, and the activity of the protein complex is dependent on ambient oxygen concentrations, and intra- and extracellular concentrations of ammonia and oxidized nitrogen species (nitrate and nitrite).[25][26][27] Additionally, the combined concentrations of both ammonium and nitrate are thought to inhibit NFix, specifically when intracellular concentrations of 2-oxoglutarate (2-OG) exceed a critical threshold.[28] The specialized heterocyst cell is necessary for the performance of nitrogenase as a result of its sensitivity to ambient oxygen.[29]

Nitrogenase consist of two proteins, a catalytic iron-dependent protein, commonly referred to as MoFe protein and a reducing iron-only protein (Fe protein). There are three different iron dependent proteins, molybdenum-dependent, vanadium-dependent, and iron-only, with all three nitrogenase protein variations containing an iron protein component. Molybdenum-dependent nitrogenase is the most commonly present nitrogenase.[23] The different types of nitrogenase can be determined by the specific iron protein component.[30] Nitrogenase is highly conserved. Gene expression through DNA sequencing can distinguish which protein complex is present in the microorganism and potentially being expressed. Most frequently, the nifH gene is used to identify the presence of molybdenum-dependent nitrogenase, followed by closely related nitrogenase reductases (component II) vnfH and anfH representing vanadium-dependent and iron-only nitrogenase, respectively.[31] In studying the ecology and evolution of nitrogen-fixing bacteria, the nifH gene is the biomarker most widely used.[32] nifH has two similar genes anfH and vnfH that also encode for the nitrogenase reductase component of the nitrogenase complex.[33]

Microorganisms

Main page: Biology:Diazotroph

Diazotrophs are widespread within domain Bacteria including cyanobacteria (e.g. the highly significant Trichodesmium and Cyanothece), green sulfur bacteria, purple sulfur bacteria, Azotobacteraceae, rhizobia and Frankia.[34][35] Several obligately anaerobic bacteria fix nitrogen including many (but not all) Clostridium spp. Some archaea such as Methanosarcina acetivorans also fix nitrogen,.[36] and several other methanogenic taxa, are significant contributors to nitrogen fixation in oxygen-deficient soils.[37]

Cyanobacteria, commonly known as blue-green algae, inhabit nearly all illuminated environments on Earth and play key roles in the carbon and nitrogen cycle of the biosphere. In general, cyanobacteria can use various inorganic and organic sources of combined nitrogen, such as nitrate, nitrite, ammonium, urea, or some amino acids. Several cyanobacteria strains are also capable of diazotrophic growth, an ability that may have been present in their last common ancestor in the Archean eon.[38] Nitrogen fixation not only naturally occurs in soils but also aquatic systems, including both freshwater and marine.[39][40] Indeed, the amount of nitrogen fixed in the ocean is at least as much as that on land.[41] The colonial marine cyanobacterium Trichodesmium is thought to fix nitrogen on such a scale that it accounts for almost half of the nitrogen fixation in marine systems globally.[42] Marine surface lichens and non-photosynthetic bacteria belonging in Proteobacteria and Planctomycetes fixate significant atmospheric nitrogen.[43] Species of nitrogen fixing cyanobacteria in fresh waters include: Aphanizomenon and Dolichospermum (previously Anabaena).[44] Such species have specialized cells called heterocytes, in which nitrogen fixation occurs via the nitrogenase enzyme.[45][46]

Root nodule symbioses

Main page: Biology:Root nodule

Legume family

Nodules are visible on this broad bean root

Plants that contribute to nitrogen fixation include those of the legume family—Fabaceae— with taxa such as kudzu, clover, soybean, alfalfa, lupin, peanut and rooibos.[35] They contain symbiotic rhizobia bacteria within nodules in their root systems, producing nitrogen compounds that help the plant to grow and compete with other plants.[47] When the plant dies, the fixed nitrogen is released, making it available to other plants; this helps to fertilize the soil.[1][48] The great majority of legumes have this association, but a few genera (e.g., Styphnolobium) do not. In many traditional farming practices, fields are rotated through various types of crops, which usually include one consisting mainly or entirely of clover.[citation needed]

Fixation efficiency in soil is dependent on many factors, including the legume and air and soil conditions. For example, nitrogen fixation by red clover can range from 50 to 200 lb/acre (56 to 224 kg/ha).[49]

Non-leguminous

A sectioned alder tree root nodule

The ability to fix nitrogen in nodules is present in actinorhizal plants such as alder and bayberry, with the help of Frankia bacteria. They are found in 25 genera in the orders Cucurbitales, Fagales and Rosales, which together with the Fabales form a nitrogen-fixing clade of eurosids. The ability to fix nitrogen is not universally present in these families. For example, of 122 Rosaceae genera, only four fix nitrogen. Fabales were the first lineage to branch off this nitrogen-fixing clade; thus, the ability to fix nitrogen may be plesiomorphic and subsequently lost in most descendants of the original nitrogen-fixing plant; however, it may be that the basic genetic and physiological requirements were present in an incipient state in the most recent common ancestors of all these plants, but only evolved to full function in some of them.[50]

In addition, Trema (Parasponia), a tropical genus in the family Cannabaceae, is unusually able to interact with rhizobia and form nitrogen-fixing nodules.[51]

Non-legumious nodulating plants
Family Genera Species
Betulaceae
Most or all species
Boraginaceae
Cannabaceae
Casuarinaceae
Coriariaceae
Datiscaceae
Elaeagnaceae
Myricaceae
Posidoniaceae
Rhamnaceae
Rosaceae

Other plant symbionts

Some other plants live in association with a cyanobiont (cyanobacteria such as Nostoc) which fix nitrogen for them:

Some symbiotic relationships involving agriculturally-important plants are:[54]

Industrial processes

Historical

A method for nitrogen fixation was first described by Henry Cavendish in 1784 using electric arcs reacting nitrogen and oxygen in air. This method was implemented in the Birkeland–Eyde process of 1903.[56] The fixation of nitrogen by lightning is a very similar natural occurring process.

The possibility that atmospheric nitrogen reacts with certain chemicals was first observed by Desfosses in 1828. He observed that mixtures of alkali metal oxides and carbon react with nitrogen at high temperatures. With the use of barium carbonate as starting material, the first commercial process became available in the 1860s, developed by Margueritte and Sourdeval. The resulting barium cyanide reacts with steam, yielding ammonia. In 1898 Frank and Caro developed what is known as the Frank–Caro process to fix nitrogen in the form of calcium cyanamide. The process was eclipsed by the Haber process, which was discovered in 1909.[57][58]

Haber process

Main page: Chemistry:Haber process

File:THC 2003.902.022 D. C. Bardwell Study of Nitrogen Fixation.tif The dominant industrial method for producing ammonia is the Haber process also known as the Haber-Bosch process.[59] Fertilizer production is now the largest source of human-produced fixed nitrogen in the terrestrial ecosystem. Ammonia is a required precursor to fertilizers, explosives, and other products. The Haber process requires high pressures (around 200 atm) and high temperatures (at least 400 °C), which are routine conditions for industrial catalysis. This process uses natural gas as a hydrogen source and air as a nitrogen source. The ammonia product has resulted in an intensification of nitrogen fertilizer globally[60] and is credited with supporting the expansion of the human population from around 2 billion in the early 20th century to roughly 8 billion people now.[61]

Homogeneous catalysis

Main page: Chemistry:Abiological nitrogen fixation

Much research has been conducted on the discovery of catalysts for nitrogen fixation, often with the goal of lowering energy requirements. However, such research has thus far failed to approach the efficiency and ease of the Haber process. Many compounds react with atmospheric nitrogen to give dinitrogen complexes. The first dinitrogen complex to be reported was Ru(NH3)5(N2)2+.[62] Some soluble complexes do catalyze nitrogen fixation.[63]

Lightning

Lightning heats the air around it breaking the bonds of N2 starting the formation of nitrous acid.

Nitrogen can be fixed by lightning converting nitrogen gas (N2) and oxygen gas (O2) in the atmosphere into NO
x (nitrogen oxides). The N2 molecule is highly stable and nonreactive due to the triple bond between the nitrogen atoms.[64] Lightning produces enough energy and heat to break this bond[64] allowing nitrogen atoms to react with oxygen, forming NOx. These compounds cannot be used by plants, but as this molecule cools, it reacts with oxygen to form NO2,[65] which in turn reacts with water to produce HNO2 (nitrous acid) or HNO3 (nitric acid). When these acids seep into the soil, they make NO3 (nitrate), which is of use to plants.[66][64]

See also

References

  1. ↑ 1.0 1.1 1.2 1.3 Nitrogen Fixation (3rd ed.). Cambridge: Cambridge University Press. 1998. 
  2. ↑ "Biological Nitrogen Fixation" (in en). Annual Review of Biochemistry 14 (1): 685–708. June 1945. doi:10.1146/annurev.bi.14.070145.003345. ISSN 0066-4154. 
  3. ↑ "The nitrogen fixation genes". Nature 239 (5374): 495–9. October 1972. doi:10.1038/239495a0. PMID 4563018. Bibcode: 1972Natur.239..495S. 
  4. ↑ "Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate". Microbiology and Molecular Biology Reviews 63 (4): 968–89, table of contents. December 1999. doi:10.1128/MMBR.63.4.968-989.1999. PMID 10585971. 
  5. ↑ "Potential for Nitrogen Fixation in the Fungus-Growing Termite Symbiosis". Frontiers in Microbiology 7: 1993. 2016. doi:10.3389/fmicb.2016.01993. PMID 28018322. 
  6. ↑ Creative Chemistry. New York, NY: The Century Co.. 1919. pp. 19–37. https://archive.org/details/creativechemist00slosgoog. 
  7. ↑ "Atmospheric Nitrogen Fixation by Lightning". J. Atmos. Sci. 37 (1): 179–192. 1979. doi:10.1175/1520-0469(1980)037<0179:ANFBL>2.0.CO;2. Bibcode: 1980JAtS...37..179H. 
  8. ↑ "Biological Nitrogen Fixation". Nature Education Knowledge 3 (10): 15. 2011. https://www.nature.com/scitable/knowledge/library/biological-nitrogen-fixation-23570419. Retrieved 29 January 2019. 
  9. ↑ Boussingault (1838). "Recherches chimiques sur la vegetation, entreprises dans le but d'examiner si les plantes prennent de l'azote à l'atmosphere" (in French). Annales de Chimie et de Physique. 2nd series 67: 5–54. https://babel.hathitrust.org/cgi/pt?id=iau.31858046218297&view=1up&seq=9&skin=2021.  and 69: 353–367.
  10. ↑ Enriching the Earth. Massachusetts Institute of Technology. 2001. 
  11. ↑ (in German) Untersuchungen über die Stickstoffnahrung der Gramineen und Leguminosen. Berlin, Germany: Buchdruckerei der "Post" Kayssler & Co.. 1888. https://www.biodiversitylibrary.org/item/69506#page/7/mode/1up. 
  12. ↑ "Über oligonitrophile Mikroben" (in German). Centralblatt für Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene 7 (16): 561–582. 1901. https://books.google.com/books?id=tcBFAQAAMAAJ&pg=PA561. 
  13. ↑ Howard S. Reed (1942) A Short History of Plant Science, page 230, Chronic Publishing
  14. ↑ Margaret Rossiter (1975) The Emergence of Agricultural Science, page 146, Yale University Press
  15. ↑ "Chapter 7. Cleaving the N,N Triple Bond: The Transformation of Dinitrogen to Ammonia by Nitrogenases". Metal Ions in Life Sciences (Springer) 14: 147–76. 2014. doi:10.1007/978-94-017-9269-1_7. PMID 25416394. 
  16. ↑ "Nitrogenase: a draft mechanism". Accounts of Chemical Research 46 (2): 587–95. February 2013. doi:10.1021/ar300267m. PMID 23289741. 
  17. ↑ "A global census of nitrogenase diversity". Environmental Microbiology 13 (7): 1790–9. July 2011. doi:10.1111/j.1462-2920.2011.02488.x. PMID 21535343. Bibcode: 2011EnvMi..13.1790G. 
  18. ↑ "Accumulation rates and sources of external nitrogen in decaying wood in a Norway spruce dominated forest" (in en). Functional Ecology 31 (2): 530–541. 2017. doi:10.1111/1365-2435.12734. ISSN 1365-2435. Bibcode: 2017FuEco..31..530R. 
  19. ↑ "Network analysis reveals ecological links between N-fixing bacteria and wood-decaying fungi". PLOS ONE 9 (2): e88141. 2014. doi:10.1371/journal.pone.0088141. PMID 24505405. Bibcode: 2014PLoSO...988141H. 
  20. ↑ "Complementary Roles of Wood-Inhabiting Fungi and Bacteria Facilitate Deadwood Decomposition". mSystems 6 (1). January 2021. doi:10.1128/mSystems.01078-20. PMID 33436515. 
  21. ↑ "Cycling of Elements in the Biosphere" (in en). Inorganic Plant Nutrition. Encyclopedia of Plant Physiology. Berlin, Heidelberg: Springer. 1983. pp. 212–238. doi:10.1007/978-3-642-68885-0_8. ISBN 978-3-642-68885-0. 
  22. ↑ 22.0 22.1 "The Biological Control of Chemical Factors in the Environment". American Scientist 46 (3): 230A–221. 1958. ISSN 0003-0996. https://www.jstor.org/stable/27827150. 
  23. ↑ 23.0 23.1 "Mechanism of Molybdenum Nitrogenase". Chemical Reviews 96 (7): 2983–3012. November 1996. doi:10.1021/cr950055x. PMID 11848849. 
  24. ↑ "High recovery of nitrogenase activity and of Fe-labeled nitrogenase in heterocysts isolated from Anabaena variabilis". Proceedings of the National Academy of Sciences of the United States of America 75 (12): 6271–6275. December 1978. doi:10.1073/pnas.75.12.6271. PMID 16592599. Bibcode: 1978PNAS...75.6271P. 
  25. ↑ "The role of nitrogen fixation in cyanobacterial bloom toxicity in a temperate, eutrophic lake". PLOS ONE 8 (2): e56103. 2013-02-06. doi:10.1371/journal.pone.0056103. PMID 23405255. Bibcode: 2013PLoSO...856103B. 
  26. ↑ "N2 fixation in phototrophs: adaptation to a specialized way of life" (in en). Plant and Soil 230 (1): 39–48. 2001-03-01. doi:10.1023/A:1004640219659. ISSN 1573-5036. 
  27. ↑ "The cyanobacterial nitrogen fixation paradox in natural waters". F1000Research 6: 244. 2017-03-09. doi:10.12688/f1000research.10603.1. PMID 28357051. 
  28. ↑ "An increase in the level of 2-oxoglutarate promotes heterocyst development in the cyanobacterium Anabaena sp. strain PCC 7120". Microbiology 149 (Pt 11): 3257–3263. November 2003. doi:10.1099/mic.0.26462-0. PMID 14600238. 
  29. ↑ "Heterocyst Metabolism and Development" (in en). The Molecular Biology of Cyanobacteria. Advances in Photosynthesis. Dordrecht: Springer Netherlands. 1994. pp. 769–823. doi:10.1007/978-94-011-0227-8_27. ISBN 978-94-011-0227-8. 
  30. ↑ "Iron-Only Nitrogenase: Exceptional Catalytic, Structural and Spectroscopic Features" (in en). Catalysts for Nitrogen Fixation. Nitrogen Fixation: Origins, Applications, and Research Progress. Dordrecht: Springer Netherlands. 2004. pp. 281–307. doi:10.1007/978-1-4020-3611-8_11. ISBN 978-1-4020-3611-8. 
  31. ↑ "Role of Nitrogenase and Ferredoxin in the Mechanism of Bioelectrocatalytic Nitrogen Fixation by the Cyanobacteria Anabaena variabilis SA-1 Mutant Immobilized on Indium Tin Oxide (ITO) Electrodes" (in ko). Electrochimica Acta 232: 396–403. 2017. doi:10.1016/j.electacta.2017.02.148. https://www.cheric.org/research/tech/periodicals/view.php?seq=1531452. 
  32. ↑ "The natural history of nitrogen fixation". Molecular Biology and Evolution 21 (3): 541–554. March 2004. doi:10.1093/molbev/msh047. PMID 14694078. 
  33. ↑ "Characterization of anf genes specific for the alternative nitrogenase and identification of nif genes required for both nitrogenases in Rhodobacter capsulatus". Molecular Microbiology 8 (4): 673–684. May 1993. doi:10.1111/j.1365-2958.1993.tb01611.x. PMID 8332060. 
  34. ↑ Nitrogen Inputs in the Ancient Ocean - SciTechDaily
  35. ↑ 35.0 35.1 "Symbiotic Nitrogen Fixation and the Challenges to Its Extension to Nonlegumes". Applied and Environmental Microbiology 82 (13): 3698–3710. July 2016. doi:10.1128/AEM.01055-16. PMID 27084023. Bibcode: 2016ApEnM..82.3698M. 
  36. ↑ "A CRISPRi-dCas9 System for Archaea and Its Use To Examine Gene Function during Nitrogen Fixation by Methanosarcina acetivorans". Applied and Environmental Microbiology 86 (21): e01402–20. October 2020. doi:10.1128/AEM.01402-20. PMID 32826220. Bibcode: 2020ApEnM..86E1402D. 
  37. ↑ "Methanogens Are Major Contributors to Nitrogen Fixation in Soils of the Florida Everglades". Applied and Environmental Microbiology 84 (7): e02222–17. April 2018. doi:10.1128/AEM.02222-17. PMID 29374038. Bibcode: 2018ApEnM..84E2222B. 
  38. ↑ "The evolution of nitrogen fixation in cyanobacteria". Bioinformatics 28 (5): 603–606. March 2012. doi:10.1093/bioinformatics/bts008. PMID 22238262. 
  39. ↑ "Global distribution patterns of marine nitrogen-fixers by imaging and molecular methods". Nature Communications 12 (1): 4160. July 2021. doi:10.1038/s41467-021-24299-y. PMID 34230473. Bibcode: 2021NatCo..12.4160P. 
  40. ↑ "Some light on diazotrophs" (in en). Science 373 (6556): 755.7–756. 2021-08-13. doi:10.1126/science.373.6556.755-g. ISSN 0036-8075. Bibcode: 2021Sci...373..755A. 
  41. ↑ "The microbial nitrogen-cycling network". Nature Reviews. Microbiology 16 (5): 263–276. May 2018. doi:10.1038/nrmicro.2018.9. PMID 29398704. 
  42. ↑ "Trichodesmium--a widespread marine cyanobacterium with unusual nitrogen fixation properties". FEMS Microbiology Reviews 37 (3): 286–302. May 2013. doi:10.1111/j.1574-6976.2012.00352.x. PMID 22928644. 
  43. ↑ "Large-scale study indicates novel, abundant nitrogen-fixing microbes in surface ocean". https://www.sciencedaily.com/releases/2018/06/180611133453.htm. 
  44. ↑ "Nitrogen fixation and abundance of the diazotrophic cyanobacterium Aphanizomenon sp. in the Baltic Proper" (in en). Marine Ecology Progress Series 332: 107–118. 2007-03-05. doi:10.3354/meps332107. Bibcode: 2007MEPS..332..107R. http://www.int-res.com/abstracts/meps/v332/p107-118/. 
  45. ↑ "Health Effects of Toxin-Producing Cyanobacteria: "The CyanoHABs"" (in en). Human and Ecological Risk Assessment 7 (5): 1393–1407. 12 Oct 2001. doi:10.1080/20018091095087. ISSN 1080-7039. 
  46. ↑ "Nitrogen fixation and hydrogen metabolism in cyanobacteria". Microbiology and Molecular Biology Reviews 74 (4): 529–551. December 2010. doi:10.1128/MMBR.00033-10. PMID 21119016. 
  47. ↑ "The microbial nitrogen-cycling network". Nature Reviews. Microbiology 16 (5): 263–276. May 2018. doi:10.1038/nrmicro.2018.9. PMID 29398704. 
  48. ↑ Cycles of Life. Scientific American Library. 2000. 
  49. ↑ "Nitrogen Fixation and Inoculation of Forage Legumes". http://www1.foragebeef.ca/$Foragebeef/frgebeef.nsf/all/frg90/$FILE/fertilitylegumefixation.pdf. 
  50. ↑ "Ecology of Actinorhizal Plants". Nitrogen-fixing Actinorhizal Symbioses. Nitrogen Fixation: Origins, Applications, and Research Progress. 6. Springer. 2008. pp. 199–234. doi:10.1007/978-1-4020-3547-0_8. ISBN 978-1-4020-3540-1. 
  51. ↑ "LysM-type mycorrhizal receptor recruited for rhizobium symbiosis in nonlegume Parasponia". Science 331 (6019): 909–12. February 2011. doi:10.1126/science.1198181. PMID 21205637. Bibcode: 2011Sci...331..909O. 
  52. ↑ "Cycad biology, Article 1: Corraloid roots of cycads". http://www1.biologie.uni-hamburg.de/b-online/library/cycads/corraloid.htm. 
  53. ↑ "Cyanobacterium-plant symbioses". New Phytologist 147 (3): 449–481. 2000. doi:10.1046/j.1469-8137.2000.00720.x. PMID 33862930. 
  54. ↑ "Nitrogen fixation in a landrace of maize is supported by a mucilage-associated diazotrophic microbiota". PLOS Biology 16 (8): e2006352. August 2018. doi:10.1371/journal.pbio.2006352. PMID 30086128. 
  55. ↑ "Indigenous Maize: Who Owns the Rights to Mexico's 'Wonder' Plant?". July 16, 2019. https://e360.yale.edu/features/indigenous-maize-who-owns-the-rights-to-mexicos-wonder-plant. 
  56. ↑ "The Manufacture of Nitrates from the Atmosphere by the Electric Arc—Birkeland-Eyde Process". Journal of the Royal Society of Arts 57 (2949): 568–576. 1909. 
  57. ↑ "Die Umwandlungsgleichung Ba(CN)2 → BaCN2 + C im Temperaturgebiet von 500 bis 1000 °C". Z. Elektrochem. Angew. Phys. Chem. 40 (10): 693–698. 1934. doi:10.1002/bbpc.19340401005. http://onlinelibrary.wiley.com/doi/10.1002/bbpc.19340401005/abstract. Retrieved 8 August 2016. 
  58. ↑ Fixed nitrogen. 1932. https://books.google.com/books?id=87XQAAAAMAAJ. 
  59. ↑ Smil, V. 2004. Enriching the Earth: Fritz Haber, Carl Bosch, and the Transformation of World Food Production, MIT Press.
  60. ↑ "The Haber Bosch–harmful algal bloom (HB–HAB) link". Environmental Research Letters 9 (10): 105001. 2014-10-01. doi:10.1088/1748-9326/9/10/105001. ISSN 1748-9326. Bibcode: 2014ERL.....9j5001G. 
  61. ↑ "How a century of ammonia synthesis changed the world" (in en). Nature Geoscience 1 (10): 636–639. October 2008. doi:10.1038/ngeo325. ISSN 1752-0908. Bibcode: 2008NatGe...1..636E. 
  62. ↑ "Nitrogenopentammineruthenium(II) complexes". J. Chem. Soc., Chem. Commun. (24): 621–622. 1965. doi:10.1039/C19650000621. 
  63. ↑ "Catalytic N2-to-NH3 (or -N2H4) Conversion by Well-Defined Molecular Coordination Complexes". Chemical Reviews 120 (12): 5582–5636. June 2020. doi:10.1021/acs.chemrev.9b00638. PMID 32352271. 
  64. ↑ 64.0 64.1 64.2 "Production of nitrogen oxides by lightning discharges". Quarterly Journal of the Royal Meteorological Society 102 (434): 749–755. October 1976. doi:10.1002/qj.49710243404. ISSN 0035-9009. Bibcode: 1976QJRMS.102..749T. 
  65. ↑ "Atmospheric Nitrogen Fixation by Lightning". Journal of the Atmospheric Sciences 37: 179–192. August 1979. doi:10.1175/1520-0469(1980)037<0179:ANFBL>2.0.CO;2. ISSN 1520-0469. Bibcode: 1980JAtS...37..179H. 
  66. ↑ "Tropospheric Sources of NOx: Lightning And Biology". 1984. https://journals.ohiolink.edu/pg_99?126555292207822::NO::P99_ENTITY_ID,P99_ENTITY_TYPE:20567211,MAIN_FILE&cs=38gV8XNFDWVznjRjSa1erAIidpqPJBYgnOix4OM5wvpjv8vJAbG2NGhNYwWAVItkNehLIgXVYuozMCrUrENyuYA. 

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