Nitrogen fixation
Nitrogen fixation is a chemical process by which molecular nitrogen (N
2), with a strong triple covalent bond, in the air is converted into ammonia (NH
3) or related nitrogenous compounds, typically in soil or aquatic systems [1] but also in industry. Atmospheric nitrogen 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 microbials 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 includes 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
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[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.
Biological
Biological nitrogen fixation (BNF) occurs when atmospheric nitrogen is converted to ammonia by a nitrogenase enzyme.[1] The overall reaction for BNF is:
The process is coupled to the hydrolysis of 16 equivalents of ATP and is accompanied by the co-formation of one equivalent of H
2.[15] The conversion of N
2 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 N
2 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
| Part of a series on |
| Biogeochemical cycles |
|---|
 |
|
Atmospheric nitrogen is inaccessible to most organisms,[21] because its triple covalent bond is very strong. Life takes up fixed nitrogen in various ways. Considering atom acquisition, 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] The Redfield Ratio, the stoichiometric relationship between C:N:P atoms, is 106:16:1.[22]
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 express. 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
Diazotrophs are widespread within domain Bacteria including cyanobacteria (e.g. the highly significant Trichodesmium and Cyanothece), as well as green sulfur bacteria, Azotobacteraceae, rhizobia and Frankia. Several obligately anaerobic bacteria fix nitrogen including many (but not all) Clostridium spp. Some archaea also fix nitrogen, including several methanogenic taxa, which are significant contributors to nitrogen fixation in oxygen-deficient soils.[34]
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.[35] Nitrogen fixation not only naturally occurs in soils but also aquatic systems, including both freshwater and marine.[36][37] Indeed, the amount of nitrogen fixed in the ocean is at least as much as that on land.[38] 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.[39] Marine surface lichens and non-photosynthetic bacteria belonging in Proteobacteria and Planctomycetes fixate significant atmospheric nitrogen.[40] Species of nitrogen fixing cyanobacteria in fresh waters include: Aphanizomenon and Dolichospermum (previously Anabaena).[41] Such species have specialized cells called heterocytes, in which nitrogen fixation occurs via the nitrogenase enzyme.[42][43]
Legume family
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. 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.[44] When the plant dies, the fixed nitrogen is released, making it available to other plants; this helps to fertilize the soil.[1][45] 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.
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).[46]
Non-leguminous
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.[47]
In addition, Trema (Parasponia), a tropical genus in the family Cannabaceae, is unusually able to interact with rhizobia and form nitrogen-fixing nodules.[48]
| 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 lichens such as Lobaria and Peltigera
- Mosquito fern (Azolla species)
- Cycads[49]
- Gunnera
- Blasia (liverwort)
- Hornworts[50]
Some symbiotic relationships involving agriculturally-important plants are:[51]
- Sugarcane and unclear endophytes
- Foxtail millet and Azospirillum brasilense
- Kallar grass and Azoarcus sp. strain BH72
- Rice and Herbaspirillum seropedicae
- Wheat and Klebsiella pneumoniae
- Maize landrace 'Sierra Mixe' / 'olotón'[52] and various Bacteroidota and Pseudomonadota
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.[53] 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.[54][55]
Haber process
The dominant industrial method for producing ammonia is the Haber process also known as the Haber-Bosch process.[56] 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[57] 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.[58]
Homogeneous catalysis
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(NH
3)
5(N
2)2+.[59] Some soluble complexes do catalyze nitrogen fixation.[60]
Lightning
.jpg.webp)
2 starting the formation of nitrous acid.
Nitrogen can be fixed by lightning converting nitrogen gas (N
2) and oxygen gas (O
2) in the atmosphere into NOx (nitrogen oxides). The N
2 molecule is highly stable and nonreactive due to the triple bond between the nitrogen atoms.[61] Lightning produces enough energy and heat to break this bond[61] allowing nitrogen atoms to react with oxygen, forming NO
x. These compounds cannot be used by plants, but as this molecule cools, it reacts with oxygen to form NO
2,[62] which in turn reacts with water to produce HNO
2 (nitrous acid) or HNO
3 (nitric acid). When these acids seep into the soil, they make NO
3 (nitrate), which is of use to plants.[63][61]
See also
- Birkeland–Eyde process: an industrial fertilizer production process
- George Washington Carver: an American botanist
- Denitrification: an organic process of nitrogen release
- Heterocyst
- Nitrification: biological production of nitrogen
- Nitrogen cycle: the flow and transformation of nitrogen through the environment
- Nitrogen deficiency
- Nitrogen fixation package for quantitative measurement of nitrogen fixation by plants
- Nitrogenase: enzymes used by organisms to fix nitrogen
- Ostwald process: a chemical process for making nitric acid (HNO
3) - Push–pull technology: the use of both repellent and attractive organisms in agriculture
- Carbon fixation
References
- Postgate J (1998). Nitrogen Fixation (3rd ed.). Cambridge: Cambridge University Press.
- Burris RH, Wilson PW (June 1945). "Biological Nitrogen Fixation". Annual Review of Biochemistry. 14 (1): 685–708. doi:10.1146/annurev.bi.14.070145.003345. ISSN 0066-4154.
- Streicher SL, Gurney EG, Valentine RC (October 1972). "The nitrogen fixation genes". Nature. 239 (5374): 495–9. Bibcode:1972Natur.239..495S. doi:10.1038/239495a0. PMID 4563018. S2CID 4225250.
- Zahran HH (December 1999). "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. doi:10.1128/MMBR.63.4.968-989.1999. PMC 98982. PMID 10585971.
- Sapountzis P, de Verges J, Rousk K, Cilliers M, Vorster BJ, Poulsen M (2016). "Potential for Nitrogen Fixation in the Fungus-Growing Termite Symbiosis". Frontiers in Microbiology. 7: 1993. doi:10.3389/fmicb.2016.01993. PMC 5156715. PMID 28018322.
- Slosson E (1919). Creative Chemistry. New York, NY: The Century Co. pp. 19–37.
- Hill RD, Rinker RG, Wilson HD (1979). "Atmospheric Nitrogen Fixation by Lightning". J. Atmos. Sci. 37 (1): 179–192. Bibcode:1980JAtS...37..179H. doi:10.1175/1520-0469(1980)037<0179:ANFBL>2.0.CO;2.
- Wagner SC (2011). "Biological Nitrogen Fixation". Nature Education Knowledge. 3 (10): 15. Archived from the original on 13 September 2018. Retrieved 29 January 2019.
- Boussingault (1838). "Recherches chimiques sur la vegetation, entreprises dans le but d'examiner si les plantes prennent de l'azote à l'atmosphere" [Chemical investigations into vegetation, undertaken with the goal of examining whether plants take up nitrogen in the atmosphere]. Annales de Chimie et de Physique. 2nd series (in French). 67: 5–54. and 69: 353–367.
- Smil V (2001). Enriching the Earth. Massachusetts Institute of Technology.
- Hellriegel H, Wilfarth H (1888). Untersuchungen über die Stickstoffnahrung der Gramineen und Leguminosen [Studies on the nitrogen intake of Gramineae and Leguminosae] (in German). Berlin, Germany: Buchdruckerei der "Post" Kayssler & Co.
- Beijerinck MW (1901). "Über oligonitrophile Mikroben" [On oligonitrophilic microbes]. Centralblatt für Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene (in German). 7 (16): 561–582.
- Howard S. Reed (1942) A Short History of Plant Science, page 230, Chronic Publishing
- Margaret Rossiter (1975) The Emergence of Agricultural Science, page 146, Yale University Press
- Lee CC, Ribbe MW, Hu Y (2014). Kroneck PM, Sosa Torres ME (eds.). "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. doi:10.1007/978-94-017-9269-1_7. PMID 25416394.
- Hoffman BM, Lukoyanov D, Dean DR, Seefeldt LC (February 2013). "Nitrogenase: a draft mechanism". Accounts of Chemical Research. 46 (2): 587–95. doi:10.1021/ar300267m. PMC 3578145. PMID 23289741.
- Gaby JC, Buckley DH (July 2011). "A global census of nitrogenase diversity". Environmental Microbiology. 13 (7): 1790–9. doi:10.1111/j.1462-2920.2011.02488.x. PMID 21535343.
- Rinne KT, Rajala T, Peltoniemi K, Chen J, Smolander A, Mäkipää R (2017). "Accumulation rates and sources of external nitrogen in decaying wood in a Norway spruce dominated forest". Functional Ecology. 31 (2): 530–541. doi:10.1111/1365-2435.12734. ISSN 1365-2435. S2CID 88551895.
- Hoppe B, Kahl T, Karasch P, Wubet T, Bauhus J, Buscot F, Krüger D (2014). "Network analysis reveals ecological links between N-fixing bacteria and wood-decaying fungi". PLOS ONE. 9 (2): e88141. Bibcode:2014PLoSO...988141H. doi:10.1371/journal.pone.0088141. PMC 3914916. PMID 24505405.
- Tláskal V, Brabcová V, Větrovský T, Jomura M, López-Mondéjar R, Oliveira Monteiro LM, et al. (January 2021). "Complementary Roles of Wood-Inhabiting Fungi and Bacteria Facilitate Deadwood Decomposition". mSystems. 6 (1). doi:10.1128/mSystems.01078-20. PMC 7901482. PMID 33436515.
- Delwiche, C. C. (1983), Läuchli, André; Bieleski, Roderick Leon (eds.), "Cycling of Elements in the Biosphere", Inorganic Plant Nutrition, Encyclopedia of Plant Physiology, Berlin, Heidelberg: Springer, pp. 212–238, doi:10.1007/978-3-642-68885-0_8, ISBN 978-3-642-68885-0, retrieved 29 April 2021
- REDFIELD, ALFRED C. (1958). "The Biological Control of Chemical Factors in the Environment". American Scientist. 46 (3): 230A–221. ISSN 0003-0996. JSTOR 27827150.
- Burgess, Barbara K.; Lowe, David J. (1 January 1996). "Mechanism of Molybdenum Nitrogenase". Chemical Reviews. 96 (7): 2983–3012. doi:10.1021/cr950055x. ISSN 0009-2665. PMID 11848849.
- Peterson, Richard B.; Wolk, C. Peter (1 December 1978). "High recovery of nitrogenase activity and of 55Fe-labeled nitrogenase in heterocysts isolated from Anabaena variabilis". Proceedings of the National Academy of Sciences. 75 (12): 6271–6275. Bibcode:1978PNAS...75.6271P. doi:10.1073/pnas.75.12.6271. ISSN 0027-8424. PMC 393163. PMID 16592599.
- Beversdorf, Lucas J.; Miller, Todd R.; McMahon, Katherine D. (6 February 2013). "The Role of Nitrogen Fixation in Cyanobacterial Bloom Toxicity in a Temperate, Eutrophic Lake". PLOS ONE. 8 (2): e56103. Bibcode:2013PLoSO...856103B. doi:10.1371/journal.pone.0056103. ISSN 1932-6203. PMC 3566065. PMID 23405255.
- Gallon, J.R. (1 March 2001). "N2 fixation in phototrophs: adaptation to a specialized way of life". Plant and Soil. 230 (1): 39–48. doi:10.1023/A:1004640219659. ISSN 1573-5036. S2CID 22893775.
- Paerl, Hans (9 March 2017). "The cyanobacterial nitrogen fixation paradox in natural waters". F1000Research. 6: 244. doi:10.12688/f1000research.10603.1. ISSN 2046-1402. PMC 5345769. PMID 28357051.
- Li, Jian-Hong; Laurent, Sophie; Konde, Viren; Bédu, Sylvie; Zhang, Cheng-Cai (November 2003). "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. doi:10.1099/mic.0.26462-0. ISSN 1350-0872. PMID 14600238.
- Wolk, C. Peter; Ernst, Anneliese; Elhai, Jeff (1994), Bryant, Donald A. (ed.), "Heterocyst Metabolism and Development", The Molecular Biology of Cyanobacteria, Advances in Photosynthesis, Dordrecht: Springer Netherlands, pp. 769–823, doi:10.1007/978-94-011-0227-8_27, ISBN 978-94-011-0227-8, retrieved 29 April 2021
- Schneider, K.; Müller, A. (2004), Smith, Barry E.; Richards, Raymond L.; Newton, William E. (eds.), "Iron-Only Nitrogenase: Exceptional Catalytic, Structural and Spectroscopic Features", Catalysts for Nitrogen Fixation: Nitrogenases, Relevant Chemical Models and Commercial Processes, Nitrogen Fixation: Origins, Applications, and Research Progress, Dordrecht: Springer Netherlands, pp. 281–307, doi:10.1007/978-1-4020-3611-8_11, ISBN 978-1-4020-3611-8, retrieved 29 April 2021
- Kl, Knoche; E, Aoyama; K, Hasan; Sd, Minteer (2017). "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". Electrochimica Acta (in Korean). 232: 396–403. doi:10.1016/j.electacta.2017.02.148.
- Raymond, Jason; Siefert, Janet L.; Staples, Christopher R.; Blankenship, Robert E. (March 2004). "The Natural History of Nitrogen Fixation". Molecular Biology and Evolution. 21 (3): 541–554. doi:10.1093/molbev/msh047. ISSN 1537-1719. PMID 14694078.
- Schüddekopf, Kerstin; Hennecke, Silke; Liese, Ute; Kutsche, Michael; Klipp, Werner (1993). "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. doi:10.1111/j.1365-2958.1993.tb01611.x. ISSN 1365-2958. PMID 8332060. S2CID 42057860.
- Bae HS, Morrison E, Chanton JP, Ogram A (April 2018). "Methanogens Are Major Contributors to Nitrogen Fixation in Soils of the Florida Everglades". Applied and Environmental Microbiology. 84 (7): e02222–17. Bibcode:2018ApEnM..84E2222B. doi:10.1128/AEM.02222-17. PMC 5861825. PMID 29374038.
- Latysheva N, Junker VL, Palmer WJ, Codd GA, Barker D (March 2012). "The evolution of nitrogen fixation in cyanobacteria". Bioinformatics. 28 (5): 603–6. doi:10.1093/bioinformatics/bts008. PMID 22238262.
- Pierella Karlusich, Juan José; Pelletier, Eric; Lombard, Fabien; Carsique, Madeline; Dvorak, Etienne; Colin, Sébastien; Picheral, Marc; Cornejo-Castillo, Francisco M.; Acinas, Silvia G.; Pepperkok, Rainer; Karsenti, Eric (December 2021). "Global distribution patterns of marine nitrogen-fixers by imaging and molecular methods". Nature Communications. 12 (1): 4160. Bibcode:2021NatCo..12.4160P. doi:10.1038/s41467-021-24299-y. ISSN 2041-1723. PMC 8260585. PMID 34230473.
- Ash, Caroline (13 August 2021). Ash, Caroline; Smith, Jesse (eds.). "Some light on diazotrophs". Science. 373 (6556): 755.7–756. Bibcode:2021Sci...373..755A. doi:10.1126/science.373.6556.755-g. ISSN 0036-8075. S2CID 238709371.
- Kuypers, Marcel M. M.; Marchant, Hannah K.; Kartal, Boran (May 2018). "The microbial nitrogen-cycling network". Nature Reviews Microbiology. 16 (5): 263–276. doi:10.1038/nrmicro.2018.9. hdl:21.11116/0000-0003-B828-1. ISSN 1740-1526. PMID 29398704. S2CID 3948918.
- Bergman B, Sandh G, Lin S, Larsson J, Carpenter EJ (May 2013). "Trichodesmium--a widespread marine cyanobacterium with unusual nitrogen fixation properties". FEMS Microbiology Reviews. 37 (3): 286–302. doi:10.1111/j.1574-6976.2012.00352.x. PMC 3655545. PMID 22928644.
- "Large-scale study indicates novel, abundant nitrogen-fixing microbes in surface ocean". ScienceDaily. Archived from the original on 8 June 2019. Retrieved 8 June 2019.
- Rolff C, Almesjö L, Elmgren R (5 March 2007). "Nitrogen fixation and abundance of the diazotrophic cyanobacterium Aphanizomenon sp. in the Baltic Proper". Marine Ecology Progress Series. 332: 107–118. Bibcode:2007MEPS..332..107R. doi:10.3354/meps332107.
- Carmichael WW (12 October 2001). "Health Effects of Toxin-Producing Cyanobacteria: "The CyanoHABs"". Human and Ecological Risk Assessment. 7 (5): 1393–1407. doi:10.1080/20018091095087. ISSN 1080-7039. S2CID 83939897.
- Bothe H, Schmitz O, Yates MG, Newton WE (December 2010). "Nitrogen fixation and hydrogen metabolism in cyanobacteria". Microbiology and Molecular Biology Reviews. 74 (4): 529–51. doi:10.1128/MMBR.00033-10. PMC 3008169. PMID 21119016.
- Kuypers MM, Marchant HK, Kartal B (May 2018). "The microbial nitrogen-cycling network". Nature Reviews. Microbiology. 16 (5): 263–276. doi:10.1038/nrmicro.2018.9. hdl:21.11116/0000-0003-B828-1. PMID 29398704. S2CID 3948918.
- Smil V (2000). Cycles of Life. Scientific American Library.
- "Nitrogen Fixation and Inoculation of Forage Legumes" (PDF). Archived from the original (PDF) on 2 December 2016.
- Dawson JO (2008). "Ecology of actinorhizal plants". Nitrogen-fixing Actinorhizal Symbioses. Nitrogen Fixation: Origins, Applications, and Research Progress. Vol. 6. Springer. pp. 199–234. doi:10.1007/978-1-4020-3547-0_8. ISBN 978-1-4020-3540-1.
- Op den Camp R, Streng A, De Mita S, Cao Q, Polone E, Liu W, et al. (February 2011). "LysM-type mycorrhizal receptor recruited for rhizobium symbiosis in nonlegume Parasponia". Science. 331 (6019): 909–12. Bibcode:2011Sci...331..909O. doi:10.1126/science.1198181. PMID 21205637. S2CID 20501765.
- "Cycad biology, Article 1: Corraloid roots of cycads". www1.biologie.uni-hamburg.de. Retrieved 14 October 2021.
- Rai AN (2000). "Cyanobacterium-plant symbioses". New Phytologist. 147 (3): 449–481. doi:10.1046/j.1469-8137.2000.00720.x. PMID 33862930.
- Van Deynze, Allen; Zamora, Pablo; Delaux, Pierre-Marc; Heitmann, Cristobal; Jayaraman, Dhileepkumar; Rajasekar, Shanmugam; Graham, Danielle; Maeda, Junko; Gibson, Donald; Schwartz, Kevin D.; Berry, Alison M.; Bhatnagar, Srijak; Jospin, Guillaume; Darling, Aaron; Jeannotte, Richard; Lopez, Javier; Weimer, Bart C.; Eisen, Jonathan A.; Shapiro, Howard-Yana; Ané, Jean-Michel; Bennett, Alan B. (7 August 2018). "Nitrogen fixation in a landrace of maize is supported by a mucilage-associated diazotrophic microbiota". PLOS Biology. 16 (8): e2006352. doi:10.1371/journal.pbio.2006352. PMC 6080747. PMID 30086128.
- Pskowski, Martha (16 July 2019). "Indigenous Maize: Who Owns the Rights to Mexico's 'Wonder' Plant?". Yale E360.
- Eyde S (1909). "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. JSTOR 41338647.
- Heinrich H, Nevbner R (1934). "Die Umwandlungsgleichung Ba(CN)2 → BaCN2 + C im Temperaturgebiet von 500 bis 1000 °C" [The conversion reaction Ba(CN)2 → BaCN2 + C in the temperature range from 500 to 1,000 °C]. Z. Elektrochem. Angew. Phys. Chem. 40 (10): 693–698. doi:10.1002/bbpc.19340401005. S2CID 179115181. Archived from the original on 20 August 2016. Retrieved 8 August 2016.
- Curtis HA (1932). Fixed nitrogen.
- Smil, V. 2004. Enriching the Earth: Fritz Haber, Carl Bosch, and the Transformation of World Food Production, MIT Press.
- Glibert, Patricia M; Maranger, Roxane; Sobota, Daniel J; Bouwman, Lex (1 October 2014). "The Haber Bosch–harmful algal bloom (HB–HAB) link". Environmental Research Letters. 9 (10): 105001. Bibcode:2014ERL.....9j5001G. doi:10.1088/1748-9326/9/10/105001. ISSN 1748-9326. S2CID 154724892.
- Erisman, Jan Willem; Sutton, Mark A.; Galloway, James; Klimont, Zbigniew; Winiwarter, Wilfried (October 2008). "How a century of ammonia synthesis changed the world". Nature Geoscience. 1 (10): 636–639. Bibcode:2008NatGe...1..636E. doi:10.1038/ngeo325. ISSN 1752-0908. S2CID 94880859.
- Allen AD, Senoff CV (1965). "Nitrogenopentammineruthenium(II) complexes". J. Chem. Soc., Chem. Commun. (24): 621–622. doi:10.1039/C19650000621.
- Chalkley MJ, Drover MW, Peters JC (June 2020). "Catalytic N2-to-NH3 (or -N2H4) Conversion by Well-Defined Molecular Coordination Complexes". Chemical Reviews. 120 (12): 5582–5636. doi:10.1021/acs.chemrev.9b00638. PMC 7493999. PMID 32352271.
- Tuck AF (October 1976). "Production of nitrogen oxides by lightning discharges". Quarterly Journal of the Royal Meteorological Society. 102 (434): 749–755. Bibcode:1976QJRMS.102..749T. doi:10.1002/qj.49710243404. ISSN 0035-9009.
- Hill RD (August 1979). "Atmospheric Nitrogen Fixation by Lightning". Journal of the Atmospheric Sciences. 37: 179–192. Bibcode:1980JAtS...37..179H. doi:10.1175/1520-0469(1980)037<0179:ANFBL>2.0.CO;2. ISSN 1520-0469.
- Levin JS (1984). "Tropospheric Sources of NOx: Lightning And Biology". Retrieved 29 November 2018.
External links
- Hirsch AM (2009). "A Brief History of the Discovery of Nitrogen-fixing Organisms" (PDF). University of California, Los Angeles.
- "Marine Nitrogen Fixation laboratory". University of Southern California.
- "Travis P. Hignett Collection of Fixed Nitrogen Research Laboratory Photographs // Science History Institute Digital Collections". digital.sciencehistory.org. Retrieved 16 August 2019. Science History Institute Digital Collections (Photographs depicting numerous stages of the nitrogen fixation process and the various equipment and apparatus used in the production of atmospheric nitrogen, including generators, compressors, filters, thermostats, and vacuum and blast furnaces).
- "Proposed Process for the Fixation of Atmospheric Nitrogen", historical perspective, Scientific American, 13 July 1878, p. 21
- A global ocean snapshot of nitrogen fixers by matching sequences to cells in the Tara Ocean