Epicoccum nigrum

Epicoccum nigrum
E. nigrum growing on Lycoperdon pyriforme
Scientific classification
Kingdom: Fungi
Phylum: Ascomycota
Class: Dothidiomycetes
Order: Pleosporales
Family: Pleosporaceae
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

Epicoccum nigrum (1825) Link ex. Link 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

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

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

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

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

  1. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 Anderson, K.H. Domsch, W. Gams, Traute-Heidi (1981). Compendium of soil fungi. London: Academic Press. ISBN 0-12-220401-8.
  2. 1 2 3 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.
  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. 1 2 3 4 5 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.
  8. ↑ Gribanovski-Sassu, Olga; Foppen, F.H. (September 1968). "Light and temperature effect on Epicoccum nigrum". Phytochemistry. 7 (9): 1605–1612. 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. 1 2 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. 1 2 3 4 5 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. 1 2 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.
  13. 1 2 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.
  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.
  16. 1 2 3 4 5 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.
  17. 1 2 3 Cole, Edited by Garry; Kendrick, Edited by Bryce (1981). Biology of conidial fungi. New York [u.a.]: Acad. Press. ISBN 0-12-179501-2.
  18. 1 2 Singh, edited by Jagjit (1994). Building Mycology Management of Decay and Health in Buildings. (1st ed.). Hoboken: Taylor & Francis Ltd. ISBN 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). doi:10.2478/10004-1254-65-2014-2480.
  21. ↑ Gribanovski-Sassu, Olga; Foppen, Fredrik H. (January 1967). "The carotenoids of the fungus Epicoccum nigrum link". Phytochemistry. 6 (6): 907–909. 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.
  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.
  24. 1 2 Bell, Phillip J. L.; Karuso, Peterq (2003). "Epicocconone, A Novel Fluorescent Compound from the Fungus Epicoccum nigrum". Journal of the American Chemical Society. 125: 9304–9305. doi:10.1021/ja035496+.
  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.
  26. 1 2 3 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.
  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. doi:10.1371/journal.pone.0036826.
  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.
  29. 1 2 3 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.
  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.
  32. ↑ Hogan, Mary Beth (1 September 1996). "Basement Shower Hypersensitivity Pneumonitis Secondary to <italic>Epicoccum nigrum</italic>". CHEST Journal. 110 (3): 854. doi:10.1378/chest.110.3.854.
  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. 1 2 "Epicoccum nigrum Link 1816". Species Fungorum.
  35. 1 2 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. doi:10.1371/journal.pone.0014828.
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