Growth and morphological characteristics of some pyrophilous discomycetes in culture
Keywords:
Anthracobia; Pyronema; Tricharina; growth parameters; culture description; Raman spectroscopy
Abstract
Three pyrophilous discomycetes species (Anthracobia maurilabra (Cooke) Boud., Pyronema domesticum (Sowerby) Sacc. and Tricharina praecox (P. Karst.) Dennis) have been cultivated and studied in vitro. Cultures were obtained from fresh apothecia сollected in the Holosiivskyi National Nature Park (Kyiv, Ukraine). The culture growth and morphological characteristics of the studied fungi on different media (beer wort agar, Czapek Dox agar, potato-dextrose agar) were analyzed. All investigated species can quite easily grow under laboratory conditions on different tested nutrient media. Potato-dextrose agar was the most suitable medium for the enhancement of radial growth and the best expresses all the phenotypes of the colony of studied fungi. Macro- and micromorphological descriptions of all fungal colonies and illustrations are provided. The micromorphological analysis showed that common to the mycelium of all studied species of fungi was the presence of numerous drops of oil in the hyphae, anastomoses like T. praecox, а net- like structure of A. maurilabra similar to nematode capture hook. Beside this, A. maurilabra and P. domesticum formed the sexual stage under experimental conditions. Forming fruiting bodies of A. maurilabra in culture has not been reported before. Moreover, P. domesticum was found to form abundant dark brown sclerotia on potato-dextrose agar and Czapek Dox agar. Possible pigment composition in the P. domesticum sclerotia is discussed based on the Raman spectroscopy study, performed on this genus for the first time. The established cultural characteristics can be useful for taxonomic identification of fungal species and for pure quality control of mycelial cultures during their introduction, preservation and future potential applications in biotechnological areas.References
Barrera, V. A., & Romero, A. I. (2001). Tricharina striispora from Argentina and the finding of its anamorph, Ascorhizoctonia. Mycotaxon, 77, 31–37.
Bisko, N. A., Babitskaia, V. G., Buchalo, A. S., Krupodorova, T. A., Lomberg, M. L., Mykchaylova, O. B., Puchkova, T. A., Solomko, E. F., & Scherba, V. V. (2012). Biologicheskie osobennosti lekarstvennyh makromicetov v kulture. Tom 2 [Biological features of medicinal macromycetes in culture. Vol. 2]. M. G. Kholodny Institute of Botany, National Academy of Sciences of Ukraine, Kiev (in Russian).
Bruns, T. D., Chung. J. A., Carver. A. A., & Glassman. S. I. (2020). A simple pyrocosm for studying soil microbial response to fire reveals a rapid, massive response by Pyronema species. PLoS One, 15(3), e0222691.
Buchalo, A., Mykchaylova, O., Lomberg, M., & Vasser, S. P. (2009). Microstructure of vegetative mycelium of macromycetes in pure culture. M. G. Kholodny Institute of Botany National Academy of Sciences of the Ukraine, University of Haifa, Kiev.
Carlile, M. J., & Friend, J. (1956). Carotenoids and reproduction in Pyronema confluens. Nature, 178, 369–370.
Claridge, A. W., Trappe, J. M., & Hansen, K. (2009). Do fungi have a role as soil stabilizers and remediators after forest fire? Forest Ecology and Management, 257, 1063–1069.
Dix, N. J., & Webster, J. (1995). Phoenicoid fungi. In: Dix, N. J., & Webster, J. (Eds.). Fungal ecology. Chapman and Hall, Cambridge. Pp. 302–321.
Dougoud, R. (2001). Clé des Discomycètes carbonicoles. Documents Mycologiques, 30, 15–29.
Dzhagan, V., Atamanchuk, A., Lytvynenko, Y., Shcherbakova, Y., & Tsvyd, N. (2020). Contribution to study of the pyrophilous fungi of Ukraine. Botanica Serbica, 44(2), 231–241.
Dzhagan, V., Dzhagan, V., Hreshchuk, O., & Taran, N. (2021). Analysis of scarlet elf cup (Sarcoscypha coccinea) carotenoids in vivo by Raman spectroscopy. Journal of Raman Spectroscopy, 52, 600–607.
El-Abyad, M. S. H., & Webster, J. (1968). Studies of pyrophilous discomycetes: I. Comparative physiological studies. Transactions of the British Mycological Society, 51, 353–367.
Filipova, N., Bulyonkova, T., & Lindemann, U. (2016). New records of two pyrophilous ascomycetes from Siberia: Pyropyxis rubra and Rhodotarzetta rosea. Ascomycete.org, 8(4), 119–126.
Fischer, M. S., Stark, F. G., Berry, T. D., Zeba, N., Whitman, T., & Traxler, M. F. (2021). Pyrolyzed substrates induce aromatic compound metabolism in the post-fire fungus, Pyronema domesticum. Frontiers in Microbiology, 12, 729289.
Hansen, K., Perry, B. A., Dranginis, A. W., & Pfister, D. H. (2013). A phylogeny of the highly diverse cup-fungus family Pyronemataceae (Pezizomycetes, Ascomycota) clarifies relationships and evolution of selected life history traits. Molecular Phylogenetics and Evolution, 67, 311–335.
Hauser, J. T. (2006). Techniques for studying Bacteria and Fungi. Carolina Biological Supply Company.
Hughes, K. W., Matheny, P. B., Miller, A. N., Petersen, R. H., Iturriaga, T. M., Johnson, K. D., Methven, A. S., Raudabaugh, D. B., Swenie, R. A., & Bruns, T. D. (2020). Pyrophilous fungi detected after wildfires in the Great Smoky Mountains National Park expand known species ranges and biodiversity estimates. Mycologia, 112(4), 677–698.
Kušan, I., Matočec, N., Mešić, A., & Tkalčec, Z. (2015). Tricharina tophiseda – a new species from Croatia, with a revision of T. japonica (Pyronemataceae, Pezizales). Phytotaxa, 221(1), 35–47.
McMullan-Fisher, S. J. M., May, T. W., Robinson, R., Bell, T. L., Lebel, T., Catcheside, P., & York, A. K. (2011). Fungi and fire in Australian ecosystems: A review of current knowledge, management implications and future directions. Australian Journal of Botany, 59, 70–90.
Merlin, J. C. (1985). Resonance Raman spectroscopy of carotenoids and carotenoid-containing systems. Pure and Applied Chemistry, 57, 785–792.
Moore, E. J. (1963). The ontogeny of the apothecia of Pyronema domesticum. American Journal of Botany, 50, 37–44.
Moore, E., & Korf, R. (1963). The genus Pyronema. Bulletin of the Torrey Botanical Club, 90, 33–42.
Moore-Landecker, E. (1975). Effect of cultural conditions on apothecial morphogenesis in Pyronema domesticum. Canadian Journal of Botany, 53, 2759–2769.
Moore-Landecker, E. (1979a). Effect of light regimens and intensities on morphogenesis of the discomycete Pyronema domesticum. Mycologia, 71, 699–712.
Moore-Landecker, E. (1979b). Effect of culture age and a single photoperiod on morphogenesis of the discomycete Pyronema domesticum. Canadian Journal of Botany, 57, 1541–1549.
Moore-Landecker, E. (1981). Histochemical observations on apothecia, permanently sterile hyphae, and sclerotia of Pyronema domesticum with special reference to light. Canadian Journal of Botany, 59, 1726–1737.
Moore-Landecker, E. (1984). Effects of ultraviolet A radiation and inhibitory volatile substances on the discomycete, Pyronema domesticum. Mycologia, 76, 820–829.
Moore-Landecker, E. (1987). Effects of medium composition and light on formation of apothecia and sclerotia by Pyronema domesticum. Canadian Journal of Botany, 65(11), 2276–2279.
Moore-Landecker, E., & Shropshire Jr., W. (1982). Effects of aeration and light on apothecia, sclerotia, and mycelial growth in the discomycete Pyronema domesticum. Mycologia, 74, 1000–1013.
Oliveira, V. E. de, Castro, H. V., Edwards, G. M., & Oliveira, F. C. de (2010). Carotenes and carotenoids in natural biological samples: A Raman spectroscopic analysis. Journal of Raman Spectroscopy, 41, 642–650.
Osterrothová, K., Culka, A., Němečková, K., Nedbalová, L., Procházková, L., & Jehlička, J. (2019). Analyzing carotenoids of snow algae by Raman microspectroscopy and high-performance liquid chromatography. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, 212, 262–271.
Petersen, P. M. (1970). Danish fireplace fungi – an ecological investigation on fungi on burns. Dansk Botanisk Arkiv, 27, 1–97.
Raudabaugh, D. B., Matheny, P. B., Hughes, K. W., Iturriaga, T., Sargent, M., & Miller, A. N. (2020). Where are they hiding? Testing the body snatchers hypothesis in pyrophilous fungi. Fungal Ecology, 43(2), 100870.
Reszczynska, E., Welc, R., Grudzinski, W., Trebacz, K., & Gruszecki, W. I. (2015). Carotenoid binding to proteins: Modeling pigment transport to lipid membranes. Archives of Biochemistry and Biophysics, 584, 125–133.
Robinson, W. (1926). The conditions of growth and development of Pyronema confluens, Tul. (P. omphaloides, (Bull.) Fuckel). Annals of Botany, 40(1), 245–272.
Rosinski, M. A. (1956). Development of the ascocarp of Anthracobia melaloma. Mycologia, 48, 506–533.
Roxon, J. E., & Batra, L. R. (1973). Anthracobia, Ascodesmis, Pyronema, and Trichophaea in culture. Mycologia, 65(5), 1036–1043.
Sajid, S., & Akbar, N. (2018). Applications of fungal pigments in biotechnology. Pure and Applied Biology, 7(3), 922–930.
Seaver, F. T. (1909). Studies in pyrophilous fungi: I. The occurrence and cultivation of Pyronema. Mycologia, 1(4), 131–139.
Senanayake, I. C., Rathnayaka, A. R., Marasinghe, D. S., Calabon, M. S., Gentekaki, E., Lee, H. B., Hurdeal, V. G., Pem, D., Dissanayake, L. S.,Wijesinghe, S. N., Bundhun, D., Nguyen, T. T., Goonasekara, I. D., Abeywickrama, P. D., Bhunjun, C. S., Jayawardena, R. S., Wanasinghe, D. N., Jeewon, R., Bhat, D. J., & Xiang, M. M. (2020). Morphological approaches in studying fungi: Collection, examination, isolation, sporulation and preservation. Mycosphere, 11(1), 2678–2754.
Šimonovičová, A., Nováková, A., Pangallo, D., Hnátová, V., & Hubka, V. (2014). The occurrence of heat-resistant species of Trichophaea abundans in different types of soil in Slovakia and Czech Republic. Biologia, 69(2), 168–172.
Stalpers, J. A. (1978). Identification of wood-inhabiting Aphyllophorales in pure culture. Studies in Mycology, 16, 248.
Turnau, K. (1983). Scanning ultrastructural ontogeny of apothecia in the operculate discomycete Trichophaea abundans. Canadian Journal of Botany, 61, 476–481.
Valadon, L. R. G., Mummery, R. S., Eijk, G. W. van, Roeymans, H. J., & Britton, G. (2013). Taxonomic implications of the carotenoids of Iodophanus carneus. Transactions of the British Mycological Society, 74(1), 187–190.
Van Vooren, N., Lindemann, U., & Healy, R. (2017). Emendation of the genus Tricharina (Pezizales) based on phylogenetic, morphological and ecological data. Ascomycete.org, 9(4), 101–123.
Verscheure, M., Lognay, G., & Marlier, M. (2002). Revue bibliographique: Les méthodes chimiques d’identification et de classification des champignons. Biotechnologie, Agronomie, Société et Environnement, 6(3), 131–142.
Weesie, R. J., Merlin, J. C., De Groot, H. J., Britton, G., Lugtenburg, J., Jansen, F. J., & Cornard, J. P. (1999). Resonance Raman spectroscopy and quantum chemical modeling studies of protein-astaxanthin interactions in α-crustacyanin (major blue carotenoprotein complex in carapace of lobster, Homarus gammarus). Biospectroscopy, 5, 358–370.
Yang, C. S., & Korf, R. P. (1985a). Ascorhizoctonia gen. nov. and complexipes emend., two genera of anamorphs of species assigned to Tricharina (Discomycetes). Mycotaxon, 23, 457–481.
Yang, C. S., & Korf, R. P. (1985b). A monograph of the genus Tricharina and of a new, segregate genus, Wilcoxina (Pezizales). Mycotaxon, 24, 467–431.
Yang, C. S., & Wilcox, H. E. (1984). An e-strain ectendomycorrhiza formed by a new species, Tricharina mikolae. Mycologia, 76(4), 675–684.
Bisko, N. A., Babitskaia, V. G., Buchalo, A. S., Krupodorova, T. A., Lomberg, M. L., Mykchaylova, O. B., Puchkova, T. A., Solomko, E. F., & Scherba, V. V. (2012). Biologicheskie osobennosti lekarstvennyh makromicetov v kulture. Tom 2 [Biological features of medicinal macromycetes in culture. Vol. 2]. M. G. Kholodny Institute of Botany, National Academy of Sciences of Ukraine, Kiev (in Russian).
Bruns, T. D., Chung. J. A., Carver. A. A., & Glassman. S. I. (2020). A simple pyrocosm for studying soil microbial response to fire reveals a rapid, massive response by Pyronema species. PLoS One, 15(3), e0222691.
Buchalo, A., Mykchaylova, O., Lomberg, M., & Vasser, S. P. (2009). Microstructure of vegetative mycelium of macromycetes in pure culture. M. G. Kholodny Institute of Botany National Academy of Sciences of the Ukraine, University of Haifa, Kiev.
Carlile, M. J., & Friend, J. (1956). Carotenoids and reproduction in Pyronema confluens. Nature, 178, 369–370.
Claridge, A. W., Trappe, J. M., & Hansen, K. (2009). Do fungi have a role as soil stabilizers and remediators after forest fire? Forest Ecology and Management, 257, 1063–1069.
Dix, N. J., & Webster, J. (1995). Phoenicoid fungi. In: Dix, N. J., & Webster, J. (Eds.). Fungal ecology. Chapman and Hall, Cambridge. Pp. 302–321.
Dougoud, R. (2001). Clé des Discomycètes carbonicoles. Documents Mycologiques, 30, 15–29.
Dzhagan, V., Atamanchuk, A., Lytvynenko, Y., Shcherbakova, Y., & Tsvyd, N. (2020). Contribution to study of the pyrophilous fungi of Ukraine. Botanica Serbica, 44(2), 231–241.
Dzhagan, V., Dzhagan, V., Hreshchuk, O., & Taran, N. (2021). Analysis of scarlet elf cup (Sarcoscypha coccinea) carotenoids in vivo by Raman spectroscopy. Journal of Raman Spectroscopy, 52, 600–607.
El-Abyad, M. S. H., & Webster, J. (1968). Studies of pyrophilous discomycetes: I. Comparative physiological studies. Transactions of the British Mycological Society, 51, 353–367.
Filipova, N., Bulyonkova, T., & Lindemann, U. (2016). New records of two pyrophilous ascomycetes from Siberia: Pyropyxis rubra and Rhodotarzetta rosea. Ascomycete.org, 8(4), 119–126.
Fischer, M. S., Stark, F. G., Berry, T. D., Zeba, N., Whitman, T., & Traxler, M. F. (2021). Pyrolyzed substrates induce aromatic compound metabolism in the post-fire fungus, Pyronema domesticum. Frontiers in Microbiology, 12, 729289.
Hansen, K., Perry, B. A., Dranginis, A. W., & Pfister, D. H. (2013). A phylogeny of the highly diverse cup-fungus family Pyronemataceae (Pezizomycetes, Ascomycota) clarifies relationships and evolution of selected life history traits. Molecular Phylogenetics and Evolution, 67, 311–335.
Hauser, J. T. (2006). Techniques for studying Bacteria and Fungi. Carolina Biological Supply Company.
Hughes, K. W., Matheny, P. B., Miller, A. N., Petersen, R. H., Iturriaga, T. M., Johnson, K. D., Methven, A. S., Raudabaugh, D. B., Swenie, R. A., & Bruns, T. D. (2020). Pyrophilous fungi detected after wildfires in the Great Smoky Mountains National Park expand known species ranges and biodiversity estimates. Mycologia, 112(4), 677–698.
Kušan, I., Matočec, N., Mešić, A., & Tkalčec, Z. (2015). Tricharina tophiseda – a new species from Croatia, with a revision of T. japonica (Pyronemataceae, Pezizales). Phytotaxa, 221(1), 35–47.
McMullan-Fisher, S. J. M., May, T. W., Robinson, R., Bell, T. L., Lebel, T., Catcheside, P., & York, A. K. (2011). Fungi and fire in Australian ecosystems: A review of current knowledge, management implications and future directions. Australian Journal of Botany, 59, 70–90.
Merlin, J. C. (1985). Resonance Raman spectroscopy of carotenoids and carotenoid-containing systems. Pure and Applied Chemistry, 57, 785–792.
Moore, E. J. (1963). The ontogeny of the apothecia of Pyronema domesticum. American Journal of Botany, 50, 37–44.
Moore, E., & Korf, R. (1963). The genus Pyronema. Bulletin of the Torrey Botanical Club, 90, 33–42.
Moore-Landecker, E. (1975). Effect of cultural conditions on apothecial morphogenesis in Pyronema domesticum. Canadian Journal of Botany, 53, 2759–2769.
Moore-Landecker, E. (1979a). Effect of light regimens and intensities on morphogenesis of the discomycete Pyronema domesticum. Mycologia, 71, 699–712.
Moore-Landecker, E. (1979b). Effect of culture age and a single photoperiod on morphogenesis of the discomycete Pyronema domesticum. Canadian Journal of Botany, 57, 1541–1549.
Moore-Landecker, E. (1981). Histochemical observations on apothecia, permanently sterile hyphae, and sclerotia of Pyronema domesticum with special reference to light. Canadian Journal of Botany, 59, 1726–1737.
Moore-Landecker, E. (1984). Effects of ultraviolet A radiation and inhibitory volatile substances on the discomycete, Pyronema domesticum. Mycologia, 76, 820–829.
Moore-Landecker, E. (1987). Effects of medium composition and light on formation of apothecia and sclerotia by Pyronema domesticum. Canadian Journal of Botany, 65(11), 2276–2279.
Moore-Landecker, E., & Shropshire Jr., W. (1982). Effects of aeration and light on apothecia, sclerotia, and mycelial growth in the discomycete Pyronema domesticum. Mycologia, 74, 1000–1013.
Oliveira, V. E. de, Castro, H. V., Edwards, G. M., & Oliveira, F. C. de (2010). Carotenes and carotenoids in natural biological samples: A Raman spectroscopic analysis. Journal of Raman Spectroscopy, 41, 642–650.
Osterrothová, K., Culka, A., Němečková, K., Nedbalová, L., Procházková, L., & Jehlička, J. (2019). Analyzing carotenoids of snow algae by Raman microspectroscopy and high-performance liquid chromatography. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, 212, 262–271.
Petersen, P. M. (1970). Danish fireplace fungi – an ecological investigation on fungi on burns. Dansk Botanisk Arkiv, 27, 1–97.
Raudabaugh, D. B., Matheny, P. B., Hughes, K. W., Iturriaga, T., Sargent, M., & Miller, A. N. (2020). Where are they hiding? Testing the body snatchers hypothesis in pyrophilous fungi. Fungal Ecology, 43(2), 100870.
Reszczynska, E., Welc, R., Grudzinski, W., Trebacz, K., & Gruszecki, W. I. (2015). Carotenoid binding to proteins: Modeling pigment transport to lipid membranes. Archives of Biochemistry and Biophysics, 584, 125–133.
Robinson, W. (1926). The conditions of growth and development of Pyronema confluens, Tul. (P. omphaloides, (Bull.) Fuckel). Annals of Botany, 40(1), 245–272.
Rosinski, M. A. (1956). Development of the ascocarp of Anthracobia melaloma. Mycologia, 48, 506–533.
Roxon, J. E., & Batra, L. R. (1973). Anthracobia, Ascodesmis, Pyronema, and Trichophaea in culture. Mycologia, 65(5), 1036–1043.
Sajid, S., & Akbar, N. (2018). Applications of fungal pigments in biotechnology. Pure and Applied Biology, 7(3), 922–930.
Seaver, F. T. (1909). Studies in pyrophilous fungi: I. The occurrence and cultivation of Pyronema. Mycologia, 1(4), 131–139.
Senanayake, I. C., Rathnayaka, A. R., Marasinghe, D. S., Calabon, M. S., Gentekaki, E., Lee, H. B., Hurdeal, V. G., Pem, D., Dissanayake, L. S.,Wijesinghe, S. N., Bundhun, D., Nguyen, T. T., Goonasekara, I. D., Abeywickrama, P. D., Bhunjun, C. S., Jayawardena, R. S., Wanasinghe, D. N., Jeewon, R., Bhat, D. J., & Xiang, M. M. (2020). Morphological approaches in studying fungi: Collection, examination, isolation, sporulation and preservation. Mycosphere, 11(1), 2678–2754.
Šimonovičová, A., Nováková, A., Pangallo, D., Hnátová, V., & Hubka, V. (2014). The occurrence of heat-resistant species of Trichophaea abundans in different types of soil in Slovakia and Czech Republic. Biologia, 69(2), 168–172.
Stalpers, J. A. (1978). Identification of wood-inhabiting Aphyllophorales in pure culture. Studies in Mycology, 16, 248.
Turnau, K. (1983). Scanning ultrastructural ontogeny of apothecia in the operculate discomycete Trichophaea abundans. Canadian Journal of Botany, 61, 476–481.
Valadon, L. R. G., Mummery, R. S., Eijk, G. W. van, Roeymans, H. J., & Britton, G. (2013). Taxonomic implications of the carotenoids of Iodophanus carneus. Transactions of the British Mycological Society, 74(1), 187–190.
Van Vooren, N., Lindemann, U., & Healy, R. (2017). Emendation of the genus Tricharina (Pezizales) based on phylogenetic, morphological and ecological data. Ascomycete.org, 9(4), 101–123.
Verscheure, M., Lognay, G., & Marlier, M. (2002). Revue bibliographique: Les méthodes chimiques d’identification et de classification des champignons. Biotechnologie, Agronomie, Société et Environnement, 6(3), 131–142.
Weesie, R. J., Merlin, J. C., De Groot, H. J., Britton, G., Lugtenburg, J., Jansen, F. J., & Cornard, J. P. (1999). Resonance Raman spectroscopy and quantum chemical modeling studies of protein-astaxanthin interactions in α-crustacyanin (major blue carotenoprotein complex in carapace of lobster, Homarus gammarus). Biospectroscopy, 5, 358–370.
Yang, C. S., & Korf, R. P. (1985a). Ascorhizoctonia gen. nov. and complexipes emend., two genera of anamorphs of species assigned to Tricharina (Discomycetes). Mycotaxon, 23, 457–481.
Yang, C. S., & Korf, R. P. (1985b). A monograph of the genus Tricharina and of a new, segregate genus, Wilcoxina (Pezizales). Mycotaxon, 24, 467–431.
Yang, C. S., & Wilcox, H. E. (1984). An e-strain ectendomycorrhiza formed by a new species, Tricharina mikolae. Mycologia, 76(4), 675–684.
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