Ammonia fungi

Short description: Fungi that grow quickly in the presence of ammonia

Laccaria amethystina, one of many types of ammonia fungi

Ammonia fungi are characterized by the rapid development and high germination rates of fruiting bodies in the presence of ammonia or other nitrogen-containing materials with alkaline soil conditions.[1] These fungi naturally occur after decomposition events like animal excretion or death.[2] Reproduction can be classified into two categories including early and late phase ammonia fungi. The addition of high amounts of ammonia, urea, or other nitrogen-containing materials can cause ideal soil conditions that the ammonia fungi thrive in and then revert to pre-application conditions.[1] Ammonia fungi that develop sporophores after applications of nitrogen-containing materials are currently being studied in the field and laboratory for their mechanisms of colonization, establishment, and occurrence of fruiting bodies.[1][3][4]

## Contents

* 1 Evolution
* 2 Environment
* 2.1 Symbiotic relationships
* 2.2 Soil conditions
* 3 Reproduction
* 3.1 Early phase ammonia fungi
* 3.2 Late phase ammonia fungi
* 4 Conservation efforts
* 4.1 Threats
* 5 Further research
* 6 Species
* 7 References

## Evolution

Fungi naturally need essential bioelements including nitrogen, phosphorus, iron, and other trace elements that would otherwise limit their growth.[5] However, it is believed that the evolution of each species of ammonium transporters/ammonia permeases may have developed in a unique manner.[6] One theory suggests the convergent evolution of nitrate assimilation cluster in green algae could have had a general selective advantage toward nitrate assimilation genes.[7] Fungi may also have a mutualistic relationship towards the surrounding plants in which nitrogen is taken up by the plant in the form of ammonium through a protein transporter of fungal origin, leading to a relationship between plant and fungi.[8] A symbiotic relationship between the arbuscular mycorrhizal fungi networks and plant roots may exist through the provision of nitrogen and phosphate.[9] Evolution for species of ammonia fungi should be treated individually and generalizations may be hard to make for the whole category.[6]

## Environment

Ammonia fungi are typically found in temperate forested areas but have been documented in field environments.[1] This is largely dependent on the species of ammonia fungi being referred to but environments with well-rotted wood and plant debris are preferred by many species.[10] Many species prefer to occupy dung including Peziza moravecii, Amblyosporium botrytiis, and Chaetomium globosum.[11] Coprinopsis stercorea specifically grows solely on the dung of sheep, goats, and donkeys.[12] Chaetomium globosum also reside on plants, soils, and straw in forested and mountain soils across a variety of biomes.[13] Coprinopsis echinospora have been found on cotton clothing during decomposition research.[14] Collybia cookei can be found on the decomposing remains of other mushrooms.[15] Hebelome vinosophyllum can be found growing on the remains of animals in Vietnamese forests in Southeast Asia.[16] Most species prefer woodland with nutrient-enriched nitrogen-treated soils.[16]

Laccaria bicolor, a type of ammonia fungi found in temperate forests in North America and Northern Europe that is also carnivorous

Species not only have preferences for sites but also more general locations in which to be found. Ascobolus denudatus can be found in Europe.[17] Coprinopsis neophlyctidospora is new to science and has only been found in the boreal forests of Alberta, Canada.[18] Coprinopsis phlycitdospora can be found in the Netherlands, Japan, New Zealand, and Australia.[19] Crucispora rhombisperma has recently been discovered in Taiwan.[20] Laccaria amethystina is mainly found in Northern temperate zones, in deciduous and coniferous forests, though it has been found in Central and South America as well. Anamika lactariolens can be found in China.[21] Hebeloma radicosum can be found in Japan, Europe, and North America.[22] Laccaria bicolor is found in temperate forests in North America and Northern Europe.[23]

### Symbiotic relationships

Ammonia fungi contribute to the nitrogen cycle and play a significant role in maintaining it. This in turn helps soil bacteria, microbes, and the overall soil structure. The relationship between plant roots and mycorrhizal networks can fix nitrogen in the soil and provide symbiosis to other species such as leaf-cutter ants and termites.[24] Ammonia fungi can also be symbiotes on larger scales with people, animals, and plants. Laccaria amethystina[25] and L. bicolor are edible, but may not be considered choice. Coprinopsis cinera is edible when eaten directly after collecting.[citation needed] Ammonia fungi may also contribute to the ecosystem in other ways being more predatory than mutualistic. Laccaria bicolor is a species of carnivorous fungi, that will catch and kill springtails.[26] Ammonia fungi also contribute to the denitrification of soils and reduce greenhouse gas emissions as well, making a symbiotic relationship with many more species and the soil itself.[24]

### Soil conditions

The addition of ammonia or urea causes numerous chemical and biological changes, for example, the pH of soil litter is increased to 8–10 and the high alkaline conditions interrupts the process of nutrient recycling.[27] Water content in soil increases after the application of urea or ammonia and then decreases after the development of early phase fungi. This usually takes about 6 months after a substantial addition of ammonia. Ammonia concentrations in the soil take up to 2 years to return to pre-application levels of ammonia with the assistance of the second round of late phase fungi.[1] Ammonia fungi are most active in the O horizon of soil followed by the A and B horizons.[28]

## Reproduction

After ammonia application in forest soils, fungi can be classified into early phase ammonia fungi and late phase ammonia fungi depending on when they develop their fruiting bodies.[2] Ammonia fungi develop in a specific order starting with anamorphic fungi, cup fungi (Ascomycota), and agaric fungi with small basidiomata. These fungi are considered early phase (EP) ammonia fungi. After the development of these fungi, argaric fungi with larger basidiomata develop and are classified as late phase (LP) ammonia fungi. These fungi reproduction cycles can be difficult to replicate in laboratory settings.[1] In the field, successful reproduction cycles come with the colonization of the fungus and ability to produce its reproductive structures.[29]

### Early phase ammonia fungi

Early phase (EP) ammonia fungi include anamorphic fungi, ascomycota, and smaller basidiomycota.[2] These species occupy alkaline to neutral soils that have higher ammonium-nitrogen concentrations.[2] This is due to either a preference or tolerance to the high concentrations of ammonium.[29] They are also saprotrophic.[2] EP ammonia fungi typically only occur in one cycle.[30] Anamorphic fungi develop first, being able to handle pH conditions above 8. Once they are able to reduce the pH to 7, ascomycota fungi develop. After the ascomycota fungi reduce the pH to 6, the smaller basidiomycota develop. This is considered the late part of early phase ammonia fungi.[31] EP fungi can develop anywhere from 20 to 200 days after the application of urea.[28]

### Late phase ammonia fungi

Once the pH is in the range of 3.5–6.0 the late phase ammonia fungi, larger basidiomata, will develop, occupying weaker acidic conditions.[2][31] Anything that develops after this group of fungi will also be considered a LP ammonia fungus. These species are typically present 2–3 years after urea and ammonium applications. LP fungi use ammonium within the soil to develop and begin to turn it into nitrate-nitrogen gradually over time.[31] Quantity and size of LP fungi are typically larger than EP fungi. LP ammonia fungi can occur over multiple cycles and typically last longer than EP fungi. This is based on the species composition and dominance, along with treatment of urea and time of the year.[30] LP fungi are biotrophic with few being saprobic.[1]

## Conservation efforts

Propagation techniques are being developed in order to better understand Ammonia fungi and how they function within ammonium heavy sites.[1] This however is difficult due to numerous abiotic and biotic factors including interactions between ammonia fungi species, interactions with the agar media, and spore longevity. Germination can also be difficult in laboratory settings.[1] Addressing the increasing threat to habitat for ammonia fungi is necessary through these methods to be able to better protect it. This includes not only conservation of the forests in which these fungi can be found but also soil conservation efforts too.[32] Overall, protection of habitat for rare ammonia fungi will be necessary to protecting species in the long run. More research must also be done on fungi in general to discover more species of ammonia fungi and create better conservation management strategies for the fungi that are currently being threatened by human activity or under additional environmental stressors and threats.[33]

### Threats

Ammonia fungi are threatened by the same threats that most fungi experience including mining operations, deforestation, invasive agricultural practices, and land and air pollution. Air pollution in particular can damage mycorrhizal structures.[8] Decomposition of excessive ammonia in the atmosphere may actually cause harm to fine mycorrhizal structures.[8]

## Further research

Little is known about many species of ammonia fungi, with new fungi being discovered often.[18] It is necessary to research ammonia fungi given their role in the nitrogen cycle and the role they play in soil conservation.[24] There is also little information about the interactions between ammonia fungi and non-ammonia fungi, leading to gaps in literature which could help us to understand fungi in general. It will be necessary to continue researching ammonia fungi to begin to bridge some of the gaps that currently exist in this field.[31]

## Species

Ascobolus denudatus, one type of Ascomycota fungi

* Anamorphic fungi
* Amblyosporium botrytis[34][35][36][4]
* Cladorrhinum foescundissimum[34][36]
* Doratomyces purpureofuscus[34]

* Ascomycota
* Ascobolus denudatus[34][35][36]
* Chaetomium globosum[34]
* Psuedombrophila petrakii[35][4]
* Peziza moravecii[34][35]
* Humaria velonovskyi[34]Coprinopsis stercorea, one type of Basidiomycota fungi

* Basidiomycota
* Coprinopsis cinera[34][36]
* Coprinopsis echinospora[34][4]
* Coprinopsis neolagopus[34][35][36]
* Coprinopsis neophlyctidospora[18]
* Coprinopsis phlycitdospora[34][35][36][4]
* Coprinopsis stercorea[34][35]
* Crucispora rhombisperma[34][35][36]
* Laccaria amethystina[37]
* Lyophyllum tylicolor[34][35][36][4]
* Sagaranella tylicolor[34]

* Late Successional Phase
* Collybia cookei[34][35]
* Collybia cookei, one type of Late Successional Phase fungiAnamika lactariolens[36]
* Calocybe leucocephela[34][35]
* Hebeloma luchuense[38]
* Hebeloma radicosum[36][39]
* Hebeloma spoliatum[34][35][36][4]
* Hebelome vinosophyllum[34][35][36][4]
* Laccaria bicolor[34][40][35][4]

## References

1. ↑ 1.0 1.1 1.2 1.3 1.4 1.5 1.6 1.7 1.8 Suzuki, Akira (January 2009). "Propagation strategy of ammonia fungi". Mycoscience 50 (1): 39–51. doi:10.1007/s10267-008-0453-1.
2. ↑ 2.0 2.1 2.2 2.3 2.4 2.5 Licyayo, Dinah Corazon M.; Suzuki, Akira (2006). "Growth responses of ammonia fungi to different concentrations of ammonium-nitrogen". Mushroom Science and Biotechnology 14 (3): 145–156. doi:10.24465/msb.14.3_145.
3. ↑ Suzuki A. (2006). "Experimental and physiological ecology of ammonia fungi: studies using natural substances and artificial media". Mycoscience 47: 3–17. doi:10.1007/s10267-005-0270-8.
4. ↑ 4.0 4.1 4.2 4.3 4.4 4.5 4.6 4.7 4.8 Sagara, Naohiko; Yamanaka, Takashi; Tibbett, Mark (2008). "Soil Fungi Associated with Graves and Latrines: Toward a Forensic Mycology". Soil Analysis in Forensic Taphonomy. pp. 67–107. doi:10.1201/9781420069921. ISBN 978-0-429-24949-5. https://books.google.com/books?id=aksRkfr1d6kC&pg=PA67.
5. ↑ Naranjo-Ortiz, Miguel A.; Gabaldón, Toni (August 2019). "Fungal evolution: major ecological adaptations and evolutionary transitions". Biological Reviews 94 (4): 1443–1476. doi:10.1111/brv.12510. PMID 31021528.
6. ↑ 6.0 6.1 McDonald, T. R.; Dietrich, F. S.; Lutzoni, F. (2012). "Multiple Horizontal Gene Transfers of Ammonium Transporters/Ammonia Permeases from Prokaryotes to Eukaryotes: Toward a New Functional and Evolutionary Classification". Molecular Biology and Evolution 29 (1): 51–60. doi:10.1093/molbev/msr123. PMID 21680869.
7. ↑ Slot, Jason C.; Hibbett, David S. (31 October 2007). "Horizontal Transfer of a Nitrate Assimilation Gene Cluster and Ecological Transitions in Fungi: A Phylogenetic Study". PLOS ONE 2 (10). doi:10.1371/journal.pone.0001097. PMID 17971860. Bibcode: 2007PLoSO...2.1097S.
8. ↑ 8.0 8.1 8.2 Barman, Jagnaseni; Samanta, Aveek; Saha, Babita; Datta, Siraj (December 2016). "Mycorrhiza: The oldest association between plant and fungi". Resonance 21 (12): 1093–1104. doi:10.1007/s12045-016-0421-6.
9. ↑ Guether, Mike; Neuhäuser, Benjamin; Balestrini, Raffaella; Dynowski, Marek; Ludewig, Uwe; Bonfante, Paola (May 2009). "A Mycorrhizal-Specific Ammonium Transporter from Lotus japonicus Acquires Nitrogen Released by Arbuscular Mycorrhizal Fungi". Plant Physiology 150 (1): 73–83. doi:10.1104/pp.109.136390. PMID 19329566.
10. ↑ Licyayo, Dinah Corazon M.; Suzuki, Akira (3 July 2017). "Effect of biotic and abiotic factors on conidial germination of a saprobic ammonia fungus Amblyosporium botrytis". Mycology 8 (3): 197–204. doi:10.1080/21501203.2017.1363093. PMID 30123640.
11. ↑ Chapman, E. S.; Fergus, C. L. (September 1975). "Germination of Ascospores of Chaetomium Globosum". Mycologia 67 (5): 1048–1052. doi:10.1080/00275514.1975.12019842.
12. ↑ Petersen, Ronald H. (July 1960). "Some Soil and Coprophilous Fungi from the South Pacific Area". Mycologia 52 (4): 552–556. doi:10.1080/00275514.1960.12024928.
13. ↑ Dunn, Michael; Domsch, K. H.; Gams, W.; Anderson, Traute-Heidi (August 1982). "Compendium of Soil Fungi". Taxon 31 (3): 600. doi:10.2307/1220704. Bibcode: 1982Taxon..31..600D.
14. ↑ Webster, Emily R.; Sharples, George P.; Khalil, Ahmed; Gilhooly, Philip; Sihanonth, Prakitsin; Whalley, Anthony J.S. (May 2010). "An unexpected appearance of: Coprinopsis echinospora". Field Mycology 11 (2): 41. doi:10.1016/j.fldmyc.2010.04.004.
15. ↑ "Nomenclatural novelties and typifications proposed in Mycotaxon 117". Mycotaxon 117 (1): 517–519. 22 November 2011. doi:10.5248/117.517. https://www.biodiversitylibrary.org/part/383050.
16. ↑ 16.0 16.1 Ho, Bao-Thuy Quyen; Pham, Nguyen-Duc Hoang; Shimizu, Kiminori; Fukiharu, Toshimitsu; Truong, Binh Nguyen; Suzuki, Akira (21 August 2014). "The first record of Hebeloma vinosophyllum (Strophariaceae) in Southeast Asia". Mycotaxon 128 (1): 25–36. doi:10.5248/128.25.
17. ↑ Jordan, Michael (2004). The Encyclopedia of Fungi of Britain and Europe. Frances Lincoln. ISBN 978-0-7112-2379-0. [page needed]
18. ↑ 18.0 18.1 18.2 Raut, Jay K.; Suzuki, Akira; Fukiharu, Toshimitsu; Shimizu, Kiminori; Kawamoto, Susumu; Tanaka, Chihiro (9 May 2011). "Coprinopsis neophlyctidospora sp. nov., a new ammonia fungus from boreal forests in Canada". Mycotaxon 115 (1): 227–238. doi:10.5248/115.227.
19. ↑ Suzuki, Akira; Tsuchida, Shinji; Fukada, Junji; Tanaka, Chihiro; Tsuda, Mitsuya; Oda, Takashi; Bougher, Neale L.; Tommerup, Inez C. et al. (June 2002). "ITS rDNA variation of the Coprinopsis phlyctidospora (syn.: Coprinus phlyctidosporus) complex in the Northern and Southern Hemispheres". Mycoscience 43 (3): 229–238. doi:10.1007/s102670200033.
20. ↑ Wen-Neng, Chou; Yang, Bi-Hua; Hsieh, Huei-Mei; Ju, Yu-Ming (2021). "Crucispora rhombisperma newly recorded in Taiwan". Fungal Science 36 (1): 33–36. https://libknowledge.nmns.edu.tw/nmns/upload/fulltext/000006294/201000c/Crucispora rhombisperma newly recorded in Taiwan.pdf. Retrieved 18 April 2025.
21. ↑ Gafforov, Yusufjon (September 2009). "Anamika lactariolens: new record for China and its world distribution". International Scientific Conference, Actual problems of Algology, Mycology and Hydrobotany. https://www.researchgate.net/publication/272520398.
22. ↑ Sagara, Naohiko (August 1995). "A request — Pinpoint marking of Hebeloma radicosum fruiting sites". Mycologist 9 (3): 128. doi:10.1016/s0269-915x(09)80279-6.
23. ↑ Mueller, Gregory M.; Gardes, Monique (May 1991). "Intra- and interspecific relations within Laccaria bicolor sensu lato". Mycological Research 95 (5): 592–601. doi:10.1016/S0953-7562(09)80073-7.
24. ↑ 24.0 24.1 24.2 Singh, Mani (2021). "Fungi and Nitrogen Cycle: Symbiotic Relationship, Mechanism and Significance". Soil Nitrogen Ecology. Soil Biology. 62. pp. 391–406. doi:10.1007/978-3-030-71206-8_20. ISBN 978-3-030-71205-1.
25. ↑ Arora, David (1986). Mushrooms Demystified: A Comprehensive Guide to the Fleshy Fungi (2nd ed.). Berkeley, California: Ten Speed Press. pp. 172-73. ISBN 978-0-89815-170-1. https://archive.org/details/arora-david-mushrooms-demystified-a-comprehensive-guide-to-the-fleshy-fungi-ten-speed-press-1986/page/172/mode/2up.
26. ↑ Klironomos, John N.; Hart, Miranda M. (April 2001). "Animal nitrogen swap for plant carbon". Nature 410 (6829): 651–652. doi:10.1038/35070643. PMID 11287942.
27. ↑ Soponsathien, Siriphan (1998). "Some characteristics of ammonia fungi 1. In relation to their ligninolytic enzyme activities.". The Journal of General and Applied Microbiology 44 (5): 337–345. doi:10.2323/jgam.44.337. PMID 12501413.
28. ↑ 28.0 28.1 Imamura, Akio; Yumoto, Takakazu; Yanai, Junta (April 2006). "Urease activity in soil as a factor affecting the succession of ammonia fungi". Journal of Forest Research 11 (2): 131–135. doi:10.1007/s10310-005-0195-2. Bibcode: 2006JFR....11..131I.
29. ↑ 29.0 29.1 Suzuki, Akira (February 2006). "Experimental and physiological ecology of ammonia fungi: studies using natural substrates and artificial media". Mycoscience 47 (1): 3–17. doi:10.1007/S10267-005-0270-8.
30. ↑ 30.0 30.1 Imamura, Akio; Yumoto, Takakazu (April 2004). "The time of urea treatment and its effects on the succession of ammonia fungi in two warm temperate forests in Japan". Mycoscience 45 (2): 123–130. doi:10.1007/S10267-003-0165-5.
31. ↑ 31.0 31.1 31.2 31.3 Barua, Babla Shingha; Suzuki, Akira; Hoang, Pham Nguyen Duc (March 2012). "Effects of different nitrogen sources on interactions between ammonia fungi and non-ammonia fungi". Mycology 3 (1): 36–53. doi:10.1080/21501203.2011.654352.
32. ↑ Yang, Yue; Tong, Yan'an; Liang, Lian-you; Li, Hong-chang; Han, Wen-she (December 2021). "Dynamics of soil bacteria and fungi communities of dry land for 8 years with soil conservation management". Journal of Environmental Management 299. doi:10.1016/j.jenvman.2021.113544. PMID 34467869. Bibcode: 2021JEnvM.29913544Y.
33. ↑ Dahlberg, Anders; Genney, David R.; Heilmann-Clausen, Jacob (May 2010). "Developing a comprehensive strategy for fungal conservation in Europe: current status and future needs". Fungal Ecology 3 (2): 50–64. doi:10.1016/j.funeco.2009.10.004. Bibcode: 2010FunE....3...50D.
34. ↑ 34.00 34.01 34.02 34.03 34.04 34.05 34.06 34.07 34.08 34.09 34.10 34.11 34.12 34.13 34.14 34.15 34.16 34.17 34.18 34.19 Sagara, Naohiko (30 December 1975). "Ammonia Fungi: A Chemoecological Grouping of Terrestrial Fungi". Contributions from the Biological Laboratory, Kyoto University 24 (4): 205–276. Template:CORE output.
35. ↑ 35.00 35.01 35.02 35.03 35.04 35.05 35.06 35.07 35.08 35.09 35.10 35.11 35.12 35.13 Sagara, Naohiko (31 December 1995). "Association of ectomycorrhizal fungi with decomposed animal wastes in forest habitats: a cleaning symbiosis?". Canadian Journal of Botany 73 (S1): 1423–1433. doi:10.1139/b95-406.
36. ↑ 36.00 36.01 36.02 36.03 36.04 36.05 36.06 36.07 36.08 36.09 36.10 36.11 Fukiharu, T; Horigome, R (1996). "Ammonia fungi in the Abukuma Mountains and its biogeographical distribution around Japan (in Japanese with English summary).". Mem Natl Sci Mus Tokyo 29: 105–112. [verification needed]
37. ↑ Imamura A. (2001). "Report on Laccaria amethystina, newly confirmed as an ammonia fungus". Mycoscience 42 (6): 623–25. doi:10.1007/BF02460961.
38. ↑ "Ammonia fungi of Iriomote Island in the southern Ryukyus, Japan and a new ammonia fungus, Hebeloma luchuense". Mycoscience 36 (4): 425–30. 1995. doi:10.1007/BF02268627.
39. ↑ Sagara, N.; Hongo, T.; Murakami, Y.; Hashimoto, T.; Nagamasu, H.; Fukiharu, T.; Asakawa, Y. (August 2000). "Hebeloma radicosoides sp. nov., an agaric belonging to the chemoecological group ammonia fungi". Mycological Research 104 (8): 1017–1024. doi:10.1017/s0953756299002439.
40. ↑ Mueller, Gregory Michael (1992). Systematics of Laccaria (Agaricales) in the continental United States and Canada, with discussions on extralimital taxa and descriptions of extant types. Fieldiana Botany. 30. doi:10.5962/bhl.title.2598. BHL page 2646935. OCLC 910492746. [page needed]

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