Azospirillum

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Azospirillum
Scientific classification
Domain:
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Class:
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Genus:
Azospirillum

Tarrand et al. 1979 [1]
Type species
Azospirillum lipoferum [1]
Species
Synonyms
  • ConglomeromonasSkerman et al. 1983

Azospirillum is a Gram-negative, microaerophilic, non-fermentative and nitrogen-fixing bacterial genus from the family of Rhodospirillaceae. [1] [2] [3] [4] [5] Azospirillum bacteria can promote plant growth. [6]

Contents

Characteristics

The genus Azospirillum belongs in the Alphaproteobacteria class of bacteria. Azospirillum are gram-negative, do not form spores, and have a slightly twisted oblong-rod shape. [7]   [8] Azospirillum have at least one flagellum and sometimes multiple flagella, which they use to move rapidly. Azospirillum are aerobic, but many can also function as microaerobic diazotrophs, meaning, under low oxygen conditions, they can change inert nitrogen from the air into biologically usable forms. [7] [8] At least three species, A. melinis, A. thiophilum, and A. humicireducens are facultative anaerobes, and can live, if necessary, without oxygen. [7] Growth of Azospirillum is possible between 5 °C and 42 °C and in substrates with a pH of 5 to 9, with optimal growth occurring around 30 °C and 7 pH. [7] Microbiologists use nitrogen-free semi-solid media to isolate Azospirillum from samples. The most commonly used media is called "NFb". [5]

Discovery and reclassification

The first species described in the genus was originally named Spirillum lipoferum in 1925 by M.W. Beijerinck. [9] In Brazil, during the 1970s, similar strains of this species were found associated with the roots of grain plants by scientists led by Dr. Johanna Döbereiner. Her group discovered that these bacteria had the ability to fix nitrogen. [9] [5] Due to this discovery, Spirillum lipoferum was reclassified in 1978 as Azospirillum lipoferum by Jeffery Tarrand, Noel Krieg, and Döbereiner, who also added Azospirillumbrasilense to the genus. [10] By 2020, twenty-one species of Azospirillum had been described, most of which had been discovered after the year 2000. [11]

Origin of name

The prefix "Azo-" comes from the French word "azote", which means nitrogen. This prefix is used to denote the ability of the bacteria to fix atmospheric nitrogen. The ending "-spirillum" refers to the shape of the bacteria, which is similar to spiral-shaped bacteria in the genus Spirillum . [8]

Ecological and agricultural significance

Azospirillum are found in freshwater [8] and soil habitats, especially in close relationships with plant roots. [5] Associations with plants are thought to be largely beneficial. Over 113 species of plants in 35 different plant families have been documented to have benefited from association with a species of Azospirillum. [12] In addition to vascular plants, the growth of the algae Chlorella vulgaris was positively affected by the presence of Azospirillum. [13] Since the 1970s, Azospirillum strains have been researched for their effects in improving agricultural yields and improving growth of wild plants. In 2009, the first commercial inoculants containing Azospirillum came on the market, and by 2018, over 3 million doses were applied annually to crops by farmers, mainly in South America. [14]

Plant growth promotion

Azospirillum promotes growth of fine root hairs. Azo pic.tif
Azospirillum promotes growth of fine root hairs.

Azospirillum promote plant growth through a variety of mechanisms. Many Azospirillum excrete plant hormones that alter how the roots of plants grow. Affected roots frequently grow more branches and fine root hairs, which may help the plants acquire water and nutrients more efficiently. [14] In addition to these changes, Azospirillum can also alter the forms of plant nutrients such as nitrogen and phosphorus to make them more available to plants. [14] However, how much nitrogen Azospirillum contribute to crop plants via biological fixation is debated. [15] Azospirillum also make antioxidants that protect the plant roots from stresses due to drought and flooding. [14]

Plant growth can also be promoted indirectly by Azospirillum reducing plant disease. Azospirillum competes with pathogens on the roots for space and for trace nutrients such as iron. The plants' immune systems can also be primed by Azospirillum to resist attack by pathogens, a process known as induced systemic resistance. [14]

Known species and genetic diversity

Azospirillum genus harbor over than 20 described species. Despite the remarkable plant growth-promotion properties, less than half of Azospirillum species have the genome sequenced: A. brasilense, A. thiophilum, A. lipoferum, A. oryzae, A. palustre, A. doebereinerae, A. halopraeferens and several undescribed Azospirillum sp. strains. When accessing a phylogenetic tree with all Azospirillum genomes, it is possible to identify two monophyletic groups, one harboring exclusively A. brasilense strains and another the remaining species. [16] This strongly suggests a higher differentiation of A. brasilense from the remaining strains. The second clade also has very high diversity and not enough resolution to determine strains species only using genetic data.

Name [1] Paper that first described species [1] Details about species
Azospirillum agricolaLin et al. 2016Isolated from agricultural soil in Taiwan [17]
Azospirillum brasilensecorrig. Tarrand et al. 1979Isolated from roots of grasses in South America; One of the best studied species in the genus; Heavily researched for applications in agriculture; Used commercially to promote crop growth, especially in South America. [9]
Azospirillum canadenseMehnaz et al. 2007Isolated from corn roots in Canada [18]
Azospirillum doebereineraeEckert et al. 2001Isolated from Miscanthus grass roots in Germany [19]
Azospirillum fermentariumLin et al. 2013Isolated from a fermentation tank in Taiwan [20]
Azospirillum formosenseLin et al. 2012Isolated from agricultural soil in Taiwan [21]
Azospirillum griseumYang et al. 2019Isolated from water from Baiyang Lake in China [22]
Azospirillum halopraeferensReinhold et al. 1987Isolated from salt-tolerant Kallar grass in Pakistan; [23] Has been shown

to survive in seawater after experimental inoculation on the roots of mangroves [24]

Azospirillum humicireducensZhou et al. 2013Isolated from a microbial fuel cell in China [25]
Azospirillum largimobilecorrig. (Skerman et al. 1983) Ben Dekhil et al. 1997Isolated from lake water in Australia; [5] originally called Conglomeromonas largomobilis [26]
Azospirillum lipoferumTarrand et al. 1979First species to be described in the genus; First isolated from garden soil [27]
Azospirillum melinisPeng et al. 2006Isolated from molasses grass in China [28]
Azospirillum oryzaeXie and Yokota 2005Isolated from rice roots in Japan [29]
Azospirillum palustreTikhonova et al. 2019Isolated from sphagnum peat in Russia; Can use methanol as a food source [30]
Azospirillum picisLin et al. 2009Isolated from tar in Taiwan [31]
Azospirillum

ramasamyi

Anandham et al. 2019Isolated from bovine fermentation products in Korea [32]
Azospirillum rugosumYoung et al. 2008Isolated from oil contaminated soil in Taiwan [33]
Azospirillum soliLin et al. 2015Isolated from agricultural soil in Taiwan [34]
Azospirillum thermophilumZhao et al. 2020Isolated from a hot spring in China [35]
Azospirillum

thiophilum

Lavrinenko et al. 2010Isolated from a sulfide spring in Russia [36]
Azospirillum zeaeMehnaz et al. 2007Isolated from corn roots in Canada [37]

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<i>Azospirillum brasilense</i> Species of bacterium

Azospirillum brasilense is a very well studied, nitrogen-fixing (diazotroph), genetically tractable, Gram-negative, alpha-proteobacterium bacterium, first described in Brazil by the group of Johanna Döbereiner and then receiving the name "brasilense". A. brasilense is able to fix nitrogen in the presence of low oxygen levels, making it a microaerobic diazotroph. An isolate from the genus Azospirillum was isolated from nitrogen poor soils in the Netherlands in 1925, however the species A. brasilense was first described in 1978 in Brazil, since this genus is widely found in the rhizospheres of grasses around the world where it confers plant growth promotion. Whether growth promotion occurs through direct nitrogen flux from the bacteria to the plant or through hormone regulation is debated. The two most commonly studied strains are Sp7 and Sp245, both are Brazilian isolates isolated from Tropical grasses from Seropedica, Brazil.

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References

  1. 1 2 3 4 5 Parte AC. "Azospirillum". LPSN .
  2. Arora NK (2014). Plant Microbes Symbiosis: Applied Facets. Springer. ISBN   978-81-322-2068-8.
  3. "Azospirillum". www.uniprot.org.
  4. Steenhoudt O, Vanderleyden J (October 2000). "Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects". FEMS Microbiology Reviews. 24 (4): 487–506. doi: 10.1111/j.1574-6976.2000.tb00552.x . PMID   10978548.
  5. 1 2 3 4 5 Cassán FD, Okon Y, Creus CM (2015). Handbook for Azospirillum: Technical Issues and Protocols. Cham: Springer. ISBN   978-3-319-06542-7. OCLC   908335504.
  6. Katsy EI (2014). Plasticity in plant-growth-promoting and phytopathogenic bacteria. New York, NY: Imprint: Springer. ISBN   978-1-4614-9203-0.
  7. 1 2 3 4 Rosenberg E, DeLong EF, Lory S, Stackebrandt E, Thompson F, eds. (2014). The Prokaryotes: Alphaproteobacteria and Betaproteobacteria. Berlin, Heidelberg: Springer Berlin Heidelberg. doi:10.1007/978-3-642-30197-1. ISBN   978-3-642-30196-4. S2CID   12080582.
  8. 1 2 3 4 Madigan MT, Martinko JM, Parker J (2003). Brock biology of microorganisms (10th ed.). Upper Saddle River, NJ: Prentice Hall/Pearson Education. ISBN   0-13-066271-2. OCLC   49558966.
  9. 1 2 3 Fukami J, Cerezini P, Hungria M (May 2018). "Azospirillum: benefits that go far beyond biological nitrogen fixation". AMB Express. 8 (1): 73. doi: 10.1186/s13568-018-0608-1 . PMC   5935603 . PMID   29728787.
  10. Tarrand JJ, Krieg NR, Döbereiner J (August 1978). "A taxonomic study of the Spirillum lipoferum group, with descriptions of a new genus, Azospirillum gen. nov. and two species, Azospirillum lipoferum (Beijerinck) comb. nov. and Azospirillum brasilense sp. nov". Canadian Journal of Microbiology. 24 (8): 967–80. doi:10.1139/m78-160. hdl: 10919/54873 . PMID   356945.
  11. "Genus: Azospirillum". lpsn.dsmz.de. Retrieved 2020-10-20.
  12. Pereg, Lily; de-Bashan, Luz E.; Bashan, Yoav (February 2016). "Assessment of affinity and specificity of Azospirillum for plants". Plant and Soil. 399 (1–2): 389–414. Bibcode:2016PlSoi.399..389P. doi:10.1007/s11104-015-2778-9. ISSN   0032-079X. S2CID   8547931.
  13. Meza, Beatriz; de-Bashan, Luz E.; Hernandez, Juan-Pablo; Bashan, Yoav (2015-06-01). "Accumulation of intra-cellular polyphosphate in Chlorella vulgaris cells is related to indole-3-acetic acid produced by Azospirillum brasilense". Research in Microbiology. 166 (5): 399–407. doi: 10.1016/j.resmic.2015.03.001 . ISSN   0923-2508. PMID   25797155.
  14. 1 2 3 4 5 Fukami, Josiane; Cerezini, Paula; Hungria, Mariangela (2018-05-04). "Azospirillum: benefits that go far beyond biological nitrogen fixation". AMB Express. 8 (1): 73. doi: 10.1186/s13568-018-0608-1 . ISSN   2191-0855. PMC   5935603 . PMID   29728787.
  15. Bashan, Yoav; de-Bashan, Luz E. (2010-01-01), Sparks, Donald L. (ed.), "Chapter Two - How the Plant Growth-Promoting Bacterium Azospirillum Promotes Plant Growth—A Critical Assessment", Advances in Agronomy, vol. 108, Academic Press, pp. 77–136, doi:10.1016/s0065-2113(10)08002-8 , retrieved 2020-11-03
  16. Rodrigues, Gustavo Lima; Matteoli, Filipe Pereira; et al. (2022-01-01). "Characterization of cellular, biochemical and genomic features of the diazotrophic plant growth-promoting bacterium Azospirillum sp. UENF-412522, a novel member of the Azospirillum genus". Microbiological Research. 254: 126896. doi: 10.1016/j.micres.2021.126896 . PMID   34715447. S2CID   239491293.
  17. Lin, Shih-Yao; Liu, You-Cheng; Hameed, Asif; Hsu, Yi-Han; Huang, Hsin-I; Lai, Wei-An; Young, Chiu-Chung (2016-03-01). "Azospirillum agricola sp. nov., a nitrogen-fixing species isolated from cultivated soil". International Journal of Systematic and Evolutionary Microbiology. 66 (3): 1453–1458. doi: 10.1099/ijsem.0.000904 . ISSN   1466-5026. PMID   26786719.
  18. Mehnaz, Samina; Weselowski, Brian; Lazarovits, George (2007-03-01). "Azospirillum canadense sp. nov., a nitrogen-fixing bacterium isolated from corn rhizosphere". International Journal of Systematic and Evolutionary Microbiology. 57 (3): 620–624. doi: 10.1099/ijs.0.64804-0 . ISSN   1466-5026. PMID   17329796.
  19. Eckert, B; Weber, O B; Kirchhof, G; Halbritter, A; Stoffels, M; Hartmann, A (2001-01-01). "Azospirillum doebereinerae sp. nov., a nitrogen-fixing bacterium associated with the C4-grass Miscanthus". International Journal of Systematic and Evolutionary Microbiology. 51 (1): 17–26. doi: 10.1099/00207713-51-1-17 . ISSN   1466-5026. PMID   11211255.
  20. Lin, Shih-Yao; Liu, You-Cheng; Hameed, Asif; Hsu, Yi-Han; Lai, Wei-An; Shen, Fo-Ting; Young, Chiu-Chung (2013-10-01). "Azospirillum fermentarium sp. nov., a nitrogen-fixing species isolated from a fermenter". International Journal of Systematic and Evolutionary Microbiology. 63 (Pt_10): 3762–3768. doi:10.1099/ijs.0.050872-0. ISSN   1466-5026. PMID   23645021.
  21. Lin, Shih-Yao; Shen, Fo-Ting; Young, Li-Sen; Zhu, Zhi-Long; Chen, Wen-Ming; Young, Chiu-Chung (2012-05-01). "Azospirillum formosense sp. nov., a diazotroph from agricultural soil". International Journal of Systematic and Evolutionary Microbiology. 62 (Pt_5): 1185–1190. doi: 10.1099/ijs.0.030585-0 . ISSN   1466-5026. PMID   21742820.
  22. Yang, Yunzhen; Zhang, RanRan; Feng, Jie; Wang, Chao; Chen, Jifeng (2019-12-01). "Azospirillum griseum sp. nov., isolated from lakewater". International Journal of Systematic and Evolutionary Microbiology. 69 (12): 3676–3681. doi: 10.1099/ijsem.0.003460 . ISSN   1466-5026. PMID   31135333.
  23. Reinhold, B.; Hurek, T.; Fendrik, I.; Pot, B.; Gillis, M.; Kersters, K.; Thielemans, S.; De Ley, J. (1987-01-01). "Azospirillum halopraeferens sp. nov., a Nitrogen-Fixing Organism Associated with Roots of Kallar Grass (Leptochloa fusca (L.) Kunth)". International Journal of Systematic Bacteriology. 37 (1): 43–51. doi: 10.1099/00207713-37-1-43 . ISSN   0020-7713.
  24. Puente, M.Esther; Holguin, Gina; Glick, Bernard R.; Bashan, Yoav (July 1999). "Root-surface colonization of black mangrove seedlings by Azospirillum halopraeferens and Azospirillum brasilense in seawater". FEMS Microbiology Ecology. 29 (3): 283–292. Bibcode:1999FEMME..29..283P. doi: 10.1111/j.1574-6941.1999.tb00619.x .
  25. Zhou, Shungui; Han, Luchao; Wang, Yueqiang; Yang, Guiqin; Zhuang, Li; Hu, Pei (2013-07-01). "Azospirillum humicireducens sp. nov., a nitrogen-fixing bacterium isolated from a microbial fuel cell". International Journal of Systematic and Evolutionary Microbiology. 63 (Pt_7): 2618–2624. doi:10.1099/ijs.0.046813-0. ISSN   1466-5026. PMID   23264502.
  26. Ben Dekhil, Susan; Cahill, Marian; Stackebrandt, E.; Sly, L.I. (January 1997). "Transfer of Conglomeromonas largomobilis subsp. largomobilis to the Genus Azospirillum as Azospirillum largomobile comb. nov., and Elevation of Conglomeromonas largomobilis subsp. parooensis to the New Type Species of Conglomeromonas, Conglomeromonas parooensis sp. nov". Systematic and Applied Microbiology. 20 (1): 72–77. doi:10.1016/S0723-2020(97)80050-1.
  27. Hartmann, Anton; Baldani, Jose Ivo (2006), Dworkin, Martin; Falkow, Stanley; Rosenberg, Eugene; Schleifer, Karl-Heinz (eds.), "The Genus Azospirillum", The Prokaryotes, New York, NY: Springer New York, pp. 115–140, doi:10.1007/0-387-30745-1_6, ISBN   978-0-387-25495-1 , retrieved 2020-11-07
  28. Peng, Guixiang; Wang, Huarong; Zhang, Guoxia; Hou, Wei; Liu, Yang; Wang, En Tao; Tan, Zhiyuan (2006-06-01). "Azospirillum melinis sp. nov., a group of diazotrophs isolated from tropical molasses grass". International Journal of Systematic and Evolutionary Microbiology. 56 (6): 1263–1271. doi:10.1099/ijs.0.64025-0. ISSN   1466-5026. PMID   16738102.
  29. Xie, Cheng-Hui; Yokota, Akira (2005-07-01). "Azospirillum oryzae sp. nov., a nitrogen-fixing bacterium isolated from the roots of the rice plant Oryza sativa". International Journal of Systematic and Evolutionary Microbiology. 55 (4): 1435–1438. doi: 10.1099/ijs.0.63503-0 . ISSN   1466-5026. PMID   16014463.
  30. Tikhonova, Ekaterina N.; Grouzdev, Denis S.; Kravchenko, Irina K. (2019-09-01). "Azospirillum palustre sp. nov., a methylotrophic nitrogen-fixing species isolated from raised bog". International Journal of Systematic and Evolutionary Microbiology. 69 (9): 2787–2793. doi: 10.1099/ijsem.0.003560 . ISSN   1466-5026. PMID   31237535.
  31. Lin, S.-Y.; Young, C. C.; Hupfer, H.; Siering, C.; Arun, A. B.; Chen, W.-M.; Lai, W.-A.; Shen, F.-T.; Rekha, P. D.; Yassin, A. F. (2009-04-01). "Azospirillum picis sp. nov., isolated from discarded tar". International Journal of Systematic and Evolutionary Microbiology. 59 (4): 761–765. doi: 10.1099/ijs.0.65837-0 . ISSN   1466-5026. PMID   19329602.
  32. Anandham, Rangasamy; Heo, Jun; Krishnamoorthy, Ramasamy; SenthilKumar, Murugaiyan; Gopal, Nellaiappan Olgaganathan; Kim, Soo-Jin; Kwon, Soon-Wo (2019-05-01). "Azospirillum ramasamyi sp. nov., a novel diazotrophic bacterium isolated from fermented bovine products". International Journal of Systematic and Evolutionary Microbiology. 69 (5): 1369–1375. doi: 10.1099/ijsem.0.003320 . ISSN   1466-5026. PMID   30810523.
  33. Young, C. C.; Hupfer, H.; Siering, C.; Ho, M.-J.; Arun, A. B.; Lai, W.-A.; Rekha, P. D.; Shen, F.-T.; Hung, M.-H.; Chen, W.-M.; Yassin, A. F. (2008-04-01). "Azospirillum rugosum sp. nov., isolated from oil-contaminated soil". International Journal of Systematic and Evolutionary Microbiology. 58 (4): 959–963. doi: 10.1099/ijs.0.65065-0 . ISSN   1466-5026. PMID   18398202.
  34. Lin, Shih-Yao; Hameed, Asif; Liu, You-Cheng; Hsu, Yi-Han; Lai, Wei-An; Shen, Fo-Ting; Young, Chiu-Chung (2015-12-01). "Azospirillum soli sp. nov., a nitrogen-fixing species isolated from agricultural soil". International Journal of Systematic and Evolutionary Microbiology. 65 (Pt_12): 4601–4607. doi: 10.1099/ijsem.0.000618 . ISSN   1466-5026. PMID   26382036.
  35. Zhao, Zhuo-li; Ming, Hong; Ding, Chen-Long; Ji, Wei-Li; Cheng, Li-Jiao; Niu, Ming-ming; Zhang, Yan-min; Zhang, Ling-Yu; Meng, Xiao-Lin; Nie, Guo-Xing (2020-01-01). "Azospirillum thermophilum sp. nov., isolated from a hot spring". International Journal of Systematic and Evolutionary Microbiology. 70 (1): 550–554. doi: 10.1099/ijsem.0.003788 . ISSN   1466-5026. PMID   31651377.
  36. Lavrinenko, Ksenia; Chernousova, Elena; Gridneva, Elena; Dubinina, Galina; Akimov, Vladimir; Kuever, Jan; Lysenko, Anatoly; Grabovich, Margarita (2010-12-01). "Azospirillum thiophilum sp. nov., a diazotrophic bacterium isolated from a sulfide spring". International Journal of Systematic and Evolutionary Microbiology. 60 (12): 2832–2837. doi:10.1099/ijs.0.018853-0. ISSN   1466-5026. PMID   20081019. S2CID   2151995.
  37. Mehnaz, Samina; Weselowski, Brian; Lazarovits, George (2007-12-01). "Azospirillum zeae sp. nov., a diazotrophic bacterium isolated from rhizosphere soil of Zea mays". International Journal of Systematic and Evolutionary Microbiology. 57 (12): 2805–2809. doi: 10.1099/ijs.0.65128-0 . ISSN   1466-5026. PMID   18048728.

Further reading