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Epicoccum nigrum

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Epicoccum nigrum
E. nigrum growing on Lycoperdon pyriforme
Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Fungi
Division: Ascomycota
Class: Dothideomycetes
Order: Pleosporales
Family: Didymellaceae
Genus: Epicoccum
Species:
E. nigrum
Binomial name
Epicoccum nigrum
Link
Synonyms

Epicoccum purpurascens Ehrenb.
Epicoccum vulgare Corda
Phoma epicoccina Punith.
Toruloidea tobaica Svilv.

Epicoccum nigrum is a species of fungus in the phylum Ascomycota. A plant pathogen and endophyte, it is a widespread fungus which produces coloured pigments that can be used as antifungal agents against other pathogenic fungi. The fluorescent stain epicocconone is extracted from it.

Growth and morphology

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Epicoccum nigrum (1825) is a fungus with no known teleomorph form.[1] It has been classified as a member of the Hyphomycetes,[2] in the Deuteromycota, as well as the Fungi Imperfecti because it is only known to reproduce asexually. Despite that it is not yeast-like, it has been included in the broad, unrelated category of fungi known as black yeasts.[2] The fungus grows felty colonies in bright shades of yellow, orange, and red, often with brown or black throughout.[1][2] Colonies grow quickly, reaching about 6 cm in diameter in 2 days at room temperature.[1] Mycelia contain both chitin and cellulose.[1]

Epicoccum nigrum forms blastoconidia that are darkly coloured, warted and spherical, reaching 15 to 25 μm in diameter.[1] Conidia grow on a sporodochium, formed by warty and fibrous hyphae.[1][3] Sporets have been found to contain up to 15 cells.[4] The spores of E. nigrum are actively released depending on temperature, light, and relative humidity conditions.[5] The mechanism of release involves the separation of the conidium from the sporodochium via a double septum. It capitalizes on the spherical shape of the conidia, allowing it to "bounce" off the sporodochium.[6] Conidia then become airborne with movement or wind.[7] Sporulation is induced under Wood's light, or sometimes upon exposure to cold temperatures with a subsequent return to room temperature.[1] Pigment production is also sensitive to light and temperature changes.[8] Ideal growth temperatures range between 23–28 °C (73–82 °F), and ideal growth pH ranges from 5.0 to 6.0.[1] Although E. nigrum will grow in a range of water activity (aw of 0.99 to 0.97),[9] growth is optimized at water vapour saturation.[1]

Epicoccum nigrum produces a variety of biomedically and industrially useful metabolites, including important antifungal agents and pigments, including: flavipin, epicorazines A and B, epirodin, epicocconone, and a variety of carotenoid pigments.[10][11] Epicoccum nigrum has also been utilized in the biosynthetic manufacture of silver- and gold nanoparticles.[12][13]

Habitat and ecology

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A highly robust and ubiquitous fungus,[14] E. nigrum has an almost global spread, occurring in the Americas, Asia, and Europe.[1] Spores of E. nigrum have been cultured from a variety of environments, predominantly soil (i.e. peat, forest floor, raw humus, compost, tundra, sewage)[1] and sand (e.g., dunes, saline sands).[1][15] It is a saprophytic fungus, forming pustules (composed of sporodochia and conidia) on dead and dying plants.[4] This species is commonly found growing on cereals and seeds, as well as other crops including corn, beans, potatoes, peas and peaches.[1][16] It has been found to grow colonies on leaves submersed in water as cold as 0 °C (32 °F), and is considered a facultative marine fungus.[17] It is capable of colonizing algae and marsh grasses.[17] In indoor environments, E. nigrum has been found on paintings and wallpaper,[18] cotton and textiles,[1][4] in dust,[16][18] and in air.[1][16][19][20] It is tolerant of changes in water availability, and hyphal growth has been found to resume within an hour of exposure to water.[17]

Biomedical, industrial, and agricultural uses

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Epicoccum nigrum has a wide array of medical, industrial, and agricultural applications. It produces a variety of pigmented and non-pigmented antifungal and antibacterial compounds.[11][21] These antimicrobial compounds are effective against other fungi and bacteria present in soil.[11] Flavipin, and epirodins A and B are pigmented antifungal agents;[10][11] non-pigmented compounds include epicorazines A and B.[11] Endophytic fungi such as E. nigrum are being explored as alternative sources of antibiotics to treat important resistant infections.[22] Polysaccharide antioxidants are also produced by E. nigrum.[23] Epicocconone is a fluorescent pigment unique to E. nigrum.[24] Epicocconone is valuable in terms of its ability to pigment cells orange, which then fluoresce red without impacting cell structure or function.[24]

Industrially, E. nigrum has a variety of broad applications. It has demonstrated a capacity to biosynthesize nanoparticles from silver and gold, which have applications in chemical, industrial, and medical processes.[12][13] It has been applied as biological treatment for mechanical oily effluent, reducing the content of hydrogen peroxide, phenols, and chemical oxygen demand in the oily effluent.[25] Epicoccum nigrum pigments have been considered as natural replacements for artificial pigments currently used in food.[26] It produces a variety of pigments, ranging from darker oranges to yellows and greens.[26] These pigments were synthesized by nonpathogenic strains of E. nigrum.[26]

In Brazil, E. nigrum is used to support root growth and control sugarcane pathogens.[27] It is a biocontrol antifungal agent active against brown rot in stone fruit, caused the species Monilinia laxa and Monilinia fructigena.[28] In contrast to these uses for E. nigrum metabolites, there has been an investigation into methods of controlling E. nigrum fungal colonies that have contaminated historic and cultural artifacts.[29] The fungus was found to be quite sensitive to essential oils from plants such as lavender and rosemary.[29] This is important in terms of the preservation of artifacts in humid climates, where fungal growth is an important determinant in the deterioration of stone structures and wood frames.[29]

Epidemiology

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Epicoccum nigrum produces the glycoprotein allergen Epi p 1 which binds to IgE, sometimes cross-reacting with other fungal allergens.[16] Cross-reactivity was found to exist with Alternaria alternata, Curvularia lunata, Cladosporium herbarum, and Penicillium citrinum.[30] Epicoccum nigrum is associated with respiratory fungal allergies, including allergic asthma, rhinitis, hypersensitivity pneumonitis, and allergic fungal sinusitis.[16][31] Two pediatric cases of hypersensitivity pneumonitis caused by E. nigrum were reported in children living in a damp and mouldy home, with daily exposure to E. nigrum in the shower.[32] The fungus has been found on human skin and in spit samples.[1] It does not typically cause systemic infection, although one case has been reported in an immunocompromised patient.[33]

History and reclassification

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Epicoccum nigrum has been treated under a variety of names in the genus Epicoccum. It was first identified in 1815 by botanist Johaan Heinrich Friedrich Link.[34] Today, all previously identified species are considered to be different variants of the species E. nigrum.[4] These include: E. purpurascens, E. diversisporum, E. versicolor, E. vulgare, E. granulatum, E. menispermi, and E. neglectum.[4][34] More recently, two distinct genotypes for E. nigrum have been identified with the combined use of DNA sequencing, morphology, physiology, and recombination factors.[35] This indicates the existence of cryptic species, and a subsequent call to re-classify E. nigrum into more than one species.[35]

References

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  1. ^ a b c d e f g h i j k l m n o p Anderson, K.H. Domsch, W. Gams, Traute-Heidi (1981). Compendium of soil fungi. London: Academic Press. ISBN 978-0-12-220401-2.{{cite book}}: CS1 maint: multiple names: authors list (link)
  2. ^ a b c Pfaller, [edited by] Elias J. Anaissie, Michael R. McGinnis, Michael A. (2009). Clinical mycology (2nd ed.). [Edinburgh?]: Churchill Livingstone. ISBN 978-1-4160-5680-5. {{cite book}}: |first1= has generic name (help)CS1 maint: multiple names: authors list (link)
  3. ^ Mims, C.W.; Richardson, E.A. (October 2005). "Ultrastructure of sporodochium and conidium development in the anamorphic fungus". Canadian Journal of Botany. 83 (10): 1354–1363. doi:10.1139/b05-137.
  4. ^ a b c d e Schol-Schwarz, M. Beatrice (June 1959). "The genus Epicoccum Link". Transactions of the British Mycological Society. 42 (2): 149–IN3. doi:10.1016/S0007-1536(59)80024-3.
  5. ^ Meredith, Donald S. (1966). "Diurnal periodicity and violent liberation of conidia in epicoccum". Phytopathology. 56: 988.
  6. ^ Webster, J. (June 1966). "Spore projection in Epicoccum and Arthrinium". Transactions of the British Mycological Society. 49 (2): 339–IN14. doi:10.1016/S0007-1536(66)80068-2.
  7. ^ McGinnis, Michael R. (January 2007). "Indoor mould development and dispersal". Medical Mycology. 45 (1): 1–9. doi:10.1080/13693780600928495. PMID 17325938.
  8. ^ Gribanovski-Sassu, Olga; Foppen, F.H. (September 1968). "Light and temperature effect on Epicoccum nigrum". Phytochemistry. 7 (9): 1605–1612. Bibcode:1968PChem...7.1605G. doi:10.1016/S0031-9422(00)88613-6.
  9. ^ ALDRED, DAVID; PENN, JULIA; MAGAN, NARESH (February 2005). "Water availability and metabolomic profiles of Epicoccum nigrum and Sarophorum palmicola grown in solid substrate fermentation systems". Mycologist. 19 (1): 18–23. doi:10.1017/S0269915X05001035.
  10. ^ a b Bamford, P.C.; Norris, G.L.F.; Ward, G. (September 1961). "Flavipin production by Epicoccum spp". Transactions of the British Mycological Society. 44 (3): 354–356. doi:10.1016/S0007-1536(61)80028-4.
  11. ^ a b c d e Brown, Averil E.; Finlay, Ruth; Ward, J.S. (January 1987). "Antifungal compounds produced by Epicoccum purpurascens against soil-borne plant pathogenic fungi". Soil Biology and Biochemistry. 19 (6): 657–664. doi:10.1016/0038-0717(87)90044-7.
  12. ^ a b Qian, Yongqing; Yu, Huimei; He, Dan; Yang, Hui; Wang, Wanting; Wan, Xue; Wang, Li (6 March 2013). "Biosynthesis of silver nanoparticles by the endophytic fungus Epicoccum nigrum and their activity against pathogenic fungi". Bioprocess and Biosystems Engineering. 36 (11): 1613–1619. doi:10.1007/s00449-013-0937-z. PMID 23463299. S2CID 19159298.
  13. ^ a b Sheikhloo, Zeinab; Salouti, Mojtaba; Katiraee, Farzad (15 September 2011). "Biological Synthesis of Gold Nanoparticles by Fungus Epicoccum nigrum". Journal of Cluster Science. 22 (4): 661–665. doi:10.1007/s10876-011-0412-4. S2CID 97716088.
  14. ^ Ahumada-Rudolph, Ramón; Cajas-Madriaga, Daniel; Rudolph, Anny; Reinoso, Rodrigo; Torres, Cristian; Silva, Mario; Becerra, José (August 2014). "Variation of sterols and fatty acids as an adaptive response to changes in temperature, salinity and pH of a marine fungus Epicoccum nigrum isolated from the Patagonian Fjords". Revista de Biología Marina y Oceanografía. 49 (2): 293–305. doi:10.4067/S0718-19572014000200009.
  15. ^ Debrecen, edited by Mahendra Rai, University of (2010). Progress in mycology. Dordrecht: Springer. ISBN 978-90-481-3712-1. {{cite book}}: |first1= has generic name (help)CS1 maint: multiple names: authors list (link)
  16. ^ a b c d e Miller, edited by Brian Flannigan, Robert A. Samson, J. David (2011). Microorganisms in home and indoor work environments : diversity, health impacts, investigation and control (2nd ed.). Boca Raton, FL: CRC Press. ISBN 978-1-4200-9334-6. {{cite book}}: |first1= has generic name (help)CS1 maint: multiple names: authors list (link)
  17. ^ a b c Cole, Edited by Garry; Kendrick, Edited by Bryce (1981). Biology of conidial fungi. New York [u.a.]: Acad. Press. ISBN 978-0-12-179501-6. {{cite book}}: |first1= has generic name (help)
  18. ^ a b Singh, Jagjit, ed. (1994). Building Mycology Management of Decay and Health in Buildings (1st ed.). Hoboken: Taylor & Francis Ltd. ISBN 978-0-203-97473-5.
  19. ^ PUSZ, Wojciech; PLĄSKOWSKA, Elzbieta; YILDIRIM, İsmet; WEBER, Ryszard (2015). "Fungi occurring on the plants of the genus Amaranthus L." Turkish Journal of Botany. 39: 147–161. doi:10.3906/bot-1403-106.
  20. ^ Wilman, Karolina; Stępień, Łukasz; Fabiańska, Izabela; Kachlicki, Piotr (29 January 2014). "Plant-Pathogenic Fungi in Seeds of Different Pea Cultivars in Poland". Archives of Industrial Hygiene and Toxicology. 65 (3): 329–338. doi:10.2478/10004-1254-65-2014-2480. PMID 25205690.
  21. ^ Gribanovski-Sassu, Olga; Foppen, Fredrik H. (January 1967). "The carotenoids of the fungus Epicoccum nigrum link". Phytochemistry. 6 (6): 907–909. Bibcode:1967PChem...6..907G. doi:10.1016/S0031-9422(00)86041-0.
  22. ^ Radić, Nataša; Štrukelj, Borut (November 2012). "Endophytic fungi—The treasure chest of antibacterial substances". Phytomedicine. 19 (14): 1270–1284. doi:10.1016/j.phymed.2012.09.007. PMID 23079233.
  23. ^ Sun, Hai-Hong; Mao, Wen-Jun; Jiao, Jie-Ying; Xu, Jia-Chao; Li, Hong-Yan; Chen, Yin; Qi, Xiao-Hui; Chen, Yan-Li; Xu, Jian; Zhao, Chun-Qi; Hou, Yu-Jiao; Yang, Yu-Pin (29 January 2011). "Structural Characterization of Extracellular Polysaccharides Produced by the Marine Fungus Epicoccum nigrum JJY-40 and Their Antioxidant Activities". Marine Biotechnology. 13 (5): 1048–1055. doi:10.1007/s10126-011-9368-5. PMID 21279405. S2CID 5103926.
  24. ^ a b Bell, Phillip J. L.; Karuso, Peterq (2003). "Epicocconone, A Novel Fluorescent Compound from the Fungus Epicoccum nigrum". Journal of the American Chemical Society. 125 (31): 9304–9305. doi:10.1021/ja035496+. PMID 12889954.
  25. ^ Queissada, Daniel Delgado; Silva, Flávio Teixeira da; Penido, Juliana Sundfeld; Siqueira, Carolina Dell'Aquila; Paiva, Tereza Cristina Brazil de (2013). "Epicoccum nigrum and Cladosporium sp. for the treatment of oily effluent in an air-lift reactor". Brazilian Journal of Microbiology. 44 (2): 607–612. doi:10.1590/S1517-83822013000200041. PMC 3833166. PMID 24294260.
  26. ^ a b c Mapari, Sameer A. S.; Meyer, Anne S.; Thrane, Ulf (16 July 2008). "Evaluation of Epicoccum nigrum for growth, morphology and production of natural colorants in liquid media and on a solid rice medium". Biotechnology Letters. 30 (12): 2183–2190. doi:10.1007/S10529-008-9798-y. PMID 18629439. S2CID 25396842.
  27. ^ Fávaro, Léia Cecilia de Lima; Sebastianes, Fernanda Luiza de Souza; Araújo, Welington Luiz; Liles, Mark R. (4 June 2012). "Epicoccum nigrum P16, a Sugarcane Endophyte, Produces Antifungal Compounds and Induces Root Growth". PLOS ONE. 7 (6): e36826. Bibcode:2012PLoSO...736826F. doi:10.1371/journal.pone.0036826. PMC 3366970. PMID 22675473.
  28. ^ De Cal, A.; Larena, I.; Liñán, M.; Torres, R.; Lamarca, N.; Usall, J.; Domenichini, P.; Bellini, A.; de Eribe, X.O.; Melgarejo, P. (February 2009). "Population dynamics of a biocontrol agent against brown rot in stone fruit". Journal of Applied Microbiology. 106 (2): 592–605. doi:10.1111/j.1365-2672.2008.04030.x. PMID 19200324.
  29. ^ a b c Stupar, M.; Grbić, M. Lj.; Džamić, A.; Unković, N.; Ristić, M.; Jelikić, A.; Vukojević, J. (July 2014). "Antifungal activity of selected essential oils and biocide benzalkonium chloride against the fungi isolated from cultural heritage objects". South African Journal of Botany. 93: 118–124. doi:10.1016/j.sajb.2014.03.016.
  30. ^ Bisht, Vandana; Singh, Bhanu Pratap; Arora, Naveen; Gaur, Shailendra Nath; Sridhara, Susheela (September 2002). "Antigenic and allergenic cross-reactivity of Epicoccum nigrum with other fungi". Annals of Allergy, Asthma & Immunology. 89 (3): 285–291. doi:10.1016/S1081-1206(10)61956-4. PMID 12269649.
  31. ^ Kurup, Viswanath P; Shen, Horng-Der; Banerjee, Banani (July 2000). "Respiratory fungal allergy". Microbes and Infection. 2 (9): 1101–1110. doi:10.1016/S1286-4579(00)01264-8. PMID 10967290.
  32. ^ Hogan, Mary Beth (1 September 1996). "Basement Shower Hypersensitivity Pneumonitis Secondary to <italic>Epicoccum nigrum</italic>". Chest. 110 (3): 854–856. doi:10.1378/chest.110.3.854. PMID 8797443.
  33. ^ Suraiya, S.; Azira, N. (July 2010). "PP-067 Intramuscular Epicoccum nigrum infection in an immunocompromised patient: A case report". International Journal of Infectious Diseases. 14: S45–S46. doi:10.1016/S1201-9712(10)60135-X.
  34. ^ a b "Epicoccum nigrum Link 1816". Species Fungorum.
  35. ^ a b Fávaro, Léia Cecilia de Lima; de Melo, Fernando Lucas; Aguilar-Vildoso, Carlos Ivan; Araújo, Welington Luiz; Litvintseva, Anastasia P. (11 August 2011). "Polyphasic Analysis of Intraspecific Diversity in Epicoccum nigrum Warrants Reclassification into Separate Species". PLOS ONE. 6 (8): e14828. Bibcode:2011PLoSO...614828F. doi:10.1371/journal.pone.0014828. PMC 3154903. PMID 21853017.
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