Diazotroph

Diazotrophs are bacteria and archaea that fix atmospheric nitrogen gas into a more usable form such as ammonia.[1][2][3][4][5][6][7][8][9][10]

A diazotroph is a microorganism that is able to grow without external sources of fixed nitrogen. Examples of organisms that do this are rhizobia and Frankia (in symbiosis) and Azospirillum. All diazotrophs contain iron-molybdenum or -vanadium nitrogenase systems. Two of the most studied systems are those of Klebsiella pneumoniae and Azotobacter vinelandii. These systems are used because of their genetic tractability and their fast growth.[11]

Etymology

The word diazotroph is derived from the words diazo ("di" = two + "azo" = nitrogen) meaning "dinitrogen (N₂)" and troph meaning "pertaining to food or nourishment", in summary dinitrogen utilizing. The word azote means nitrogen in French and was named by French chemist and biologist Antoine Lavoisier, who saw it as the part of air which cannot sustain life.[12]

Types of diazotrophs

Diazotrophs are scattered across Bacteria taxonomic groups (as well as a couple of Archaea). Even within a species that can fix nitrogen there may be strains that do not fix nitrogen.[13] Fixation is shut off when other sources of nitrogen are available, and, for many species, when oxygen is at high partial pressure. Bacteria have different ways of dealing with the debilitating effects of oxygen on nitrogenases, listed below.

Free-living diazotrophs

• Anaerobes—these are obligate anaerobes that cannot tolerate oxygen even if they are not fixing nitrogen. They live in habitats low in oxygen, such as soils and decaying vegetable matter. Clostridium is an example. Sulphate-reducing bacteria are important in ocean sediments (e.g. Desulfovibrio), and some Archean methanogens, like Methanococcus, fix nitrogen in muds, animal intestines[13] and anoxic soils.[14]
• Facultative anaerobes—these species can grow either with or without oxygen, but they only fix nitrogen anaerobically. Often, they respire oxygen as rapidly as it is supplied, keeping the amount of free oxygen low. Examples include Klebsiella pneumoniae, Paenibacillus polymyxa, Bacillus macerans, and Escherichia intermedia.[13]
• Aerobes—these species require oxygen to grow, yet their nitrogenase is still debilitated if exposed to oxygen. Azotobacter vinelandii is the most studied of these organisms. It uses very high respiration rates, and protective compounds, to prevent oxygen damage. Many other species also reduce the oxygen levels in this way, but with lower respiration rates and lower oxygen tolerance.[13]
• Oxygenic photosynthetic bacteria (cyanobacteria) generate oxygen as a by-product of photosynthesis, yet some are able to fix nitrogen as well. These are colonial bacteria that have specialized cells (heterocysts) that lack the oxygen generating steps of photosynthesis. Examples are Anabaena cylindrica and Nostoc commune. Other cyanobacteria lack heterocysts and can fix nitrogen only in low light and oxygen levels (e.g. Plectonema).[13] Some cyanobacteria, including the highly abundant marine taxa Prochlorococcus and Synechococcus do not fix nitrogen,[15] whilst other marine cyanobacteria, such as Trichodesmium and Cyanothece, are major contributors to oceanic nitrogen fixation.[16]
• Anoxygenic photosynthetic bacteria do not generate oxygen during photosynthesis, having only a single photosystem which cannot split water. Nitrogenase is expressed under nitrogen limitation. Normally, the expression is regulated via negative feedback from the produced ammonium ion but in the absence of N₂, the product is not formed, and the by-product H₂ continues unabated [Biohydrogen]. Example species: Rhodobacter sphaeroides, Rhodopseudomonas palustris, Rhodobacter capsulatus.[17]

Symbiotic diazotrophs

• Rhizobia—these are the species that associate with legumes, plants of the family Fabaceae. Oxygen is bound to leghemoglobin in the root nodules that house the bacterial symbionts, and supplied at a rate that will not harm the nitrogenase.[13]
• Frankias—much less is known about these 'actinorhizal' nitrogen fixers. The bacteria also infect the roots leading to the formation of nodules. Actinorhizal nodules consist of several lobes, each lobe has a similar structure as a lateral root. Frankia is able to colonize in the cortical tissue of nodules where it fixes nitrogen.[18] Actinorhizal plants and Frankias also produce haemoglobins,[19] but their role is less well established than for rhizobia.[18] Although at first it appeared that they inhabit sets of unrelated plants (alders, Australian pines, California lilac, bog myrtle, bitterbrush, Dryas), revisions to the phylogeny of angiosperms show a close relatedness of these species and the legumes.[20][18] These footnotes suggest the ontogeny of these replicates rather than the phylogeny. In other words, an ancient gene (from before the angiosperms and gymnosperms diverged) that is unused in most species was reawakened and reused in these species.
• Cyanobacteria—there are also symbiotic cyanobacteria. Some associate with fungi as lichens, with liverworts, with a fern, and with a cycad.[13] These do not form nodules (indeed most of the plants do not have roots). Heterocysts exclude the oxygen, as discussed above. The fern association is important agriculturally: the water fern Azolla harbouring Anabaena is an important green manure for rice culture.[13]
• Association with animals—although diazotrophs have been found in many animal guts, there is usually sufficient ammonia present to suppress nitrogen fixation.[13] Termites on a low nitrogen diet allow for some fixation, but the contribution to the termite's nitrogen supply is negligible. Shipworms may be the only species that derive significant benefit from their gut symbionts.[13]

Importance

In terms of generating nitrogen available to all organisms, the symbiotic associations greatly exceed the free-living species with the exception of cyanobacteria.[13]

References

1. Puri A, Padda KP, Puri CP (October 2015). "Can a diazotrophic endophyte originally isolated from lodgepole pine colonize an agricultural crop (corn) and promote its growth?". Soil Biology and Biochemistry. 89: 210–216. doi:10.1016/j.soilbio.2015.07.012.
2. Puri A, Padda KP, Chanway CP (January 2016). "Evidence of nitrogen fixation and growth promotion in canola (Brassica napus L.) by an endophytic diazotroph Paenibacillus polymyxa P2b-2R". Biology and Fertility of Soils. 52 (1): 119–125. doi:10.1007/s00374-015-1051-y. S2CID 15963708.
3. Puri A, Padda KP, Chanway CP (June 2016). "Seedling growth promotion and nitrogen fixation by a bacterial endophyte Paenibacillus polymyxa P2b-2R and its GFP derivative in corn in a long-term trial". Symbiosis. 69 (2): 123–129. doi:10.1007/s13199-016-0385-z. S2CID 17870808.
4. Padda, Kiran Preet; Puri, Akshit; Chanway, Chris P (April 2016). "Effect of GFP tagging of Paenibacillus polymyxa P2b-2R on its ability to promote growth of canola and tomato seedlings". Biology and Fertility of Soils. 52 (3): 377–387. doi:10.1007/s00374-015-1083-3. S2CID 18149924.
5. Padda KP, Puri A, Chanway CP (7 July 2016). "Plant growth promotion and nitrogen fixation in canola by an endophytic strain of Paenibacillus polymyxa and its GFP-tagged derivative in a long-term study". Botany. 94 (12): 1209–1217. doi:10.1139/cjb-2016-0075.
6. Padda, Kiran Preet; Puri, Akshit; Zeng, Qingwei; Chanway, Chris P.; Wu, Xiaoqin (2017-07-14). "Effect of GFP-tagging on nitrogen fixation and plant growth promotion of an endophytic diazotrophic strain of Paenibacillus polymyxa". Botany. 95 (9): 933–942. doi:10.1139/cjb-2017-0056. hdl:1807/79634. ISSN 1916-2790.
7. Puri, Akshit; Padda, Kiran Preet; Chanway, Chris P. (2018-12-15). "Evidence of endophytic diazotrophic bacteria in lodgepole pine and hybrid white spruce trees growing in soils with different nutrient statuses in the West Chilcotin region of British Columbia, Canada". Forest Ecology and Management. 430: 558–565. doi:10.1016/j.foreco.2018.08.049. ISSN 0378-1127.
8. Padda, Kiran Preet; Puri, Akshit; Chanway, Chris P. (2018-09-20). "Isolation and identification of endophytic diazotrophs from lodgepole pine trees growing at unreclaimed gravel mining pits in central interior British Columbia, Canada". Canadian Journal of Forest Research. 48 (12): 1601–1606. doi:10.1139/cjfr-2018-0347. hdl:1807/92505. ISSN 0045-5067.
9. Puri, Akshit; Padda, Kiran Preet; Chanway, Chris P. (2020-01-01). "Can naturally-occurring endophytic nitrogen-fixing bacteria of hybrid white spruce sustain boreal forest tree growth on extremely nutrient-poor soils?". Soil Biology and Biochemistry. 140: 107642. doi:10.1016/j.soilbio.2019.107642. ISSN 0038-0717.
10. Padda, Kiran Preet; Puri, Akshit; Chanway, Chris (2019-11-01). "Endophytic nitrogen fixation – a possible 'hidden' source of nitrogen for lodgepole pine trees growing at unreclaimed gravel mining sites". FEMS Microbiology Ecology. 95 (11). doi:10.1093/femsec/fiz172. ISSN 0168-6496. PMID 31647534.
11. Dixon R, Kahn D (August 2004). "Genetic regulation of biological nitrogen fixation". Nature Reviews. Microbiology. 2 (8): 621–31. doi:10.1038/nrmicro954. PMID 15263897. S2CID 29899253.
12. "Diazotroph - Biology-Online Dictionary | Biology-Online Dictionary". Archived from the original on 2017-03-15. Retrieved 2017-04-05.
13. Postgate, J (1998). Nitrogen Fixation, 3rd Edition. Cambridge University Press, Cambridge UK.
14. 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. doi:10.1128/AEM.02222-17. PMC 5861825. PMID 29374038.
15. Zehr JP (April 2011). "Nitrogen fixation by marine cyanobacteria". Trends in Microbiology. 19 (4): 162–73. doi:10.1016/j.tim.2010.12.004. PMID 21227699.
16. 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.
17. Blankenship RE, Madigan MT & Bauer CE (1995). Anoxygenic photosynthetic bacteria. Dordrecht, The Netherlands, Kluwer Academic.
18. Vessey JK, Pawlowski, K and Bergman B (2005). "Root-based N₂-fixing symbioses: Legumes, actinorhizal plants, Parasponia sp and cycads". Plant and Soil. 274 (1–2): 51–78. doi:10.1007/s11104-005-5881-5. S2CID 5035264.CS1 maint: multiple names: authors list (link)
19. Beckwith J, Tjepkema JD, Cashon RE, Schwintzer CR, Tisa LS (December 2002). "Hemoglobin in five genetically diverse Frankia strains". Canadian Journal of Microbiology. 48 (12): 1048–55. doi:10.1139/w02-106. PMID 12619816.
20. Soltis DE, Soltis PS, Morgan DR, Swensen SM, Mullin BC, Dowd JM, Martin PG (March 1995). "Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms". Proceedings of the National Academy of Sciences of the United States of America. 92 (7): 2647–51. Bibcode:1995PNAS...92.2647S. doi:10.1073/pnas.92.7.2647. PMC 42275. PMID 7708699.

External links

• Marine Nitrogen Fixation - The Basics (USC Capone Lab)
• Azotobacter
• Rhizobia
• Frankia & Actinorhizal Plants