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First carnivorous fungus from Santonian Taimyr amber

Published online by Cambridge University Press:  13 June 2023

Maryna M. SUKHOMLYN*
Affiliation:
Institute for Evolutionary Ecology of NAS of Ukraine, Kyiv, 03143, Ukraine.
Evgeny E. PERKOVSKY
Affiliation:
Schmalhausen Institute of Zoology of NAS of Ukraine, Kyiv, 01030, Ukraine. Natural History Museum of Denmark, Universitetsparken 15, 2100 Copenhagen, Denmark.
*
*Corresponding author. E-mail: suhmary@ukr.net

Abstract

Mycelium from the Yantardakh Lagerstätte (Santonian of Taimyr) is reported. Its hyphae are arranged mostly parallel, weakly branched and septated. The clamp connections indicate the Basidiomycota affinity. Two types of outgrowths are formed on the mycelium, located perpendicular to the parent hypha: the former rather long and common; and the latter are short peg-shaped, formed with a lower frequency. Arthroconidia and large spherical structures, looking like exudate drops are observed upon hyphae. Hyphae rings similar to the trapping loops of extant Basidiomycota have been found. Altogether, these rings, numerous drops and peg-like hyphal outgrowths may be interpreted as this mycelium belongs to nematophagous fungus of Agaricomycetes. Thus, this is the first finding of mycelium putatively nematophagous Basidiomycota from the Cretaceous of North Asia, which also implies the presence of nematodes in the Taimyr amber forest.

Type
Spontaneous Article
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press on behalf of The Royal Society of Edinburgh

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References

9. References

Abramova, L. N. 1983. Late Cretaceous flora of the Khatanga River basin. In Bondarev, V. I. (ed.) Paleontological rationale for the subdivision of the Paleozoic and Mesozoic of the Arctic regions of the USSR, 118–27. Leningrad: PGO Sevmorgeologiya. [In Russian.]Google Scholar
Ascaso, C., Wierzchos, J., Speranza, M., Gutiérrez, J. C., González, A. M., de los Ríos, A. & Alonso, J. 2005. Fossil protists and fungi in amber and rock substrates. Micropaleontology 51, 5972.CrossRefGoogle Scholar
Askary, T. H. 1996. Studies on some nematophagous fungi in agriculture soil of Pusa Farm, Samastipur, Bihar. M.Sc. (Ag.) Thesis, Department of Nematology, Rajendra Agricultural University, Pusa, Bihar, India.Google Scholar
Azar, D. & Maksoud, S. 2020. New psychodid flies from the Upper Cretaceous Yantardakh amber and Eocene Sakhalin amber (Diptera: Psychodidae: Psychodinae). Palaeoentomology 3, 500–12.CrossRefGoogle Scholar
Balaeș, T. & Tănase, C. 2016. Basidiomycetes as potential biocontrol agents against nematodes. Romanian Biotechnological Letters 21, 11185–93.Google Scholar
Barron, G. L. 1992. Lignolytic and cellulolytic fungi as predators and parasites. In Carroll, G. C. & Wicklow, D. T. (eds) The fungal community, its organization and role in the ecosystems, 311–26. New York: Marcel Dekker.Google Scholar
Barron, G. L. 2003. Predatory fungi, wood decay, and the carbon cycle. Biodiversity 4, 39.CrossRefGoogle Scholar
Barron, G. L. & Thorn, R. G. 1987. Destruction of nematodes by species of Pleurotus. Canadian Journal of Botany 65, 774–8.CrossRefGoogle Scholar
Baxter, A. P., Rong, I. H. & Schutte, A. L. 1995. Amylostereum areolatum (AphyIlophorales: Stereaceae) in South Africa. South African Journal of Botany 61, 352–4.CrossRefGoogle Scholar
Blagoderov, V. A. & Grimaldi, D. A. 2004. Fossil Sciaroidea (Diptera) in Cretaceous ambers, exclusive of Cecidomyiidae, Sciaridae, and Keroplatidae. American Museum Novitates 3433, 176.2.0.CO;2>CrossRefGoogle Scholar
Boidin, J. 1958. Hétérobasidiomycètes saprophytes et homobasidiomycètes résupinés. V. Essai sur le genre Stereum Pers. ex S. F. Gray [Saprophytic heterobasidiomycetes and resupinated homobasidiomycetes. V. Essay on the genus Stereum Pers. ex S. F. Gray]. Revue de Mycologie (Paris) 23, 318–46. [In French.]Google Scholar
Borhani, A., Badalyan, S. M., Garibyan, N. N., Mosazadeh, S. A. & Yasari, E. 2011. Flammulina velutipes (Curt.: Fr.) Singer: an edible mushroom in northern forest of Iran and its antagonistic activity against selected plant pathogenic fungi. International Journal of Biology 3, 162–7.CrossRefGoogle Scholar
Buchalo, A. S. 1988. Higher edible Basidiomycetes in pure culture. Kyiv: Naukova dumka, 144 pp. [In Russian.]Google Scholar
Cai, C., Leschen, R., Hibbett, D., Xia, F. & Huang, D. 2017. Mycophagous rove beetles highlight diverse mushrooms in the Cretaceous. Nature Communications 8, 14894.CrossRefGoogle ScholarPubMed
Dackman, C., Jansson, H. B. & Nordbring–Hertz, B. 1992. Nematophagous fungi and their activities in soil. In Stotzky, G. & Bollag, J. M. (eds) Soil biochemistry, Vol. 7, 95103. New York, Basel, Hong Kong: Marcel Dekker.Google Scholar
de Soares, F. E. F., Nakajima, V. M., Sufiate, B. L., Satiro, L. A. S., Gomes, E. H., Froes, F. V., Sena, F. P., Braga, F. R. & Queiroz, J. H. 2019. Proteolytic and nematicidal potential of the compost colonized by Hypsizygus marmoreus. Experimental Parasitology 197, 16–9.CrossRefGoogle Scholar
de Soares, F. E. F., Sufiate, B. L. & Queiroz, J. H. 2018. Nematophagous fungi: far beyond the endoparasite, predator and ovicidal groups. Agriculture and Natural Resources 52, 18.CrossRefGoogle Scholar
Devi, G. 2018. Utilization of nematode destroying fungi for management of plant-parasitic nematodes – a review. Biosciences Biotechnology Research Asia 15, 377–96.CrossRefGoogle Scholar
Dörfelt, H. & Schäfer, U. 1998. Fossile Pilze im Bernstein der alpischen Trias [Fossil fungi in Alpine Triassic amber]. Zeitschrift für Mykologie 64, 141–51. [In German.]Google Scholar
Drechsler, C. 1941. Some hyphomycetes parasitic on free-living terricolous nematodes. Phytopathology 31, 773802.Google Scholar
Drechsler, C. 1949. A nematode-capturing fungus with anastomosing clamp-bearing hyphae. Mycologia 41, 369–87.CrossRefGoogle Scholar
Fedotova, Z. A. & Perkovsky, E. E. 2020. Mesozoic gall midges (Diptera, Cecidomyoidea) with a description of a new genus and species from the Santonian amber of Taimyr (Ugolyak). Paleontological Journal 54, 1400–9.CrossRefGoogle Scholar
Ferreira, J. M., Carreira, D. N., Braga, F. R. & Soares, F. E. D. F. 2019. First report of the nematicidal activity of Flammulina velutipes, its spent mushroom compost and metabolites. 3 Biotech 9, 410.CrossRefGoogle ScholarPubMed
Giłka, W., Zakrzewska, M., Lukashevich, E. D. Vorontsov, D. D., Soszyńska-Maj, A., Skibińska, K. & Cranston, P.S. 2022. Wanted, tracked down and identified: Mesozoic non-biting midges of the subfamily Chironominae (Chironomidae, Diptera). Zoological Journal of the Linnean Society 194, 874–92.CrossRefGoogle Scholar
Golovneva, L. B. 2012. The Late Cretaceous flora of the Khatanga depression (Northern Siberia). Paleobotany 3, 3161. [In Russian, English summary.]Google Scholar
Gumovsky, A., Perkovsky, E. & Rasnitsyn, A. 2018. Laurasian ancestors and “Gondwanan” descendants of Rotoitidae (Hymenoptera: Chalcidoidea): what a review of Late Cretaceous Baeomorpha revealed. Cretaceous Research 84, 286322.CrossRefGoogle Scholar
Hahn, M. H., De Mio, L. L. M., Kuhn, O. J. & Duarte, H. D. S. 2019. Nematophagous mushrooms can be an alternative to control Meloidogyne javanica. Biological Control 138, 104024.CrossRefGoogle Scholar
Hakim, M., Huang, D–Y. & Azar, D. 2021. New fossil psocids from Cretaceous Siberian ambers (Psocodea: Trogiomorpha: Atropetae). Palaeoentomology 4, 186–98.CrossRefGoogle Scholar
Hibbett, D. S., Grimaldi, D. A. & Donoghue, M. J. 1997. Fossil mushrooms from Miocene and Cretaceous ambers and the evolution of homobasidiomycetes. American Journal of Botany 84, 981–91.CrossRefGoogle ScholarPubMed
Hjortstam, K. & Ryvarden, L. 1980. Studies in tropical Corticiaceae (Basidiomycetes) I. Mycotaxon 10, 269–87.Google Scholar
Hutchison, L. J., Madzia, S. E. & Barron, G. L. 1996. The presence and antifeedant function of toxin-producing secretory cells on hyphae of the lawn-inhabiting agaric Conocybe lactea. Canadian Journal of Botany 74, 431–4.CrossRefGoogle Scholar
Ignatov, M. S., Heinrichs, J., Schäfer-Verwimp, A. & Perkovsky, E. E. 2016. The first record of a bryophyte in Upper Cretaceous amber from Taimyr, northern Siberia: Taimyrobryum martynoviorum gen. et sp. nov. (Bryopsida). Cretaceous Research 65, 2531.CrossRefGoogle Scholar
Imai, S. 1933. On the taxonomy of nameko-fungus in Japan. The Botanical Magazine (Tokyo) 47, 384–9.CrossRefGoogle Scholar
Ishizaki, T., Nomura, N. & Watanabe, K. 2015. Screening of mushrooms for nematophagous activity against the pinewood nematode, Bursaphelenchus xylophilus. Nematological Research 45, 1925.CrossRefGoogle Scholar
Jansson, H-B., Tunlid, A. & Nordbring-Hertz, B. 1997. Biological control: nematodes. In Anke, T. (ed.) Fungal biotechnology, 3850. Weinheim: Chapman and Hall.Google Scholar
Karakas, M. 2020. Nematode-destroying fungi: infection structures, interaction mechanisms and biocontrol. Communications Faculty of Sciences University of Ankara Series C 29, 176201.Google Scholar
Karsten, P. A. 1879. Symbolae ad mycologiam fennicam. VI. Meddelanden af Societas pro Fauna et Flora Fennica 5, 1546.Google Scholar
Karsten, P. A. 1881a. Enumeratio Boletinearum et Polyporearum Fennicarum, systemate novo dispositarum [Enumeration of the mushrooms and polypores of Finland, arranged in a new system]. Revue Mycologique Toulouse 3, 16–9. [In Latin.]Google Scholar
Karsten, P. A. 1881b. Enumeratio Hydnearum Fr. Fennicarum, systemate novo dispositarum [Enumeration of Hydnearum Fr. of Finland, arranged in a new system]. Revue Mycologique Toulouse 3, 1921. [In Latin.]Google Scholar
Kerry, B. R. 2000. Rhizosphere interactions and the exploitation of microbial agents for the biological control of plant-parasitic nematodes. Annual Review of Phytopathology 38, 423–41.CrossRefGoogle ScholarPubMed
Kirk, P. M., Cannon, P. F., Minter, D. W. & Stalpers, J. A. 2008. Dictionary of the fungi. 10th edition. Wallingford, UK: CAB International, 640 pp.Google Scholar
Kolibáč, J. & Perkovsky, E. E. 2020. A reclassification of Acanthocnemoides sukatshevae Zherikhin, 1977 from the mid-Cretaceous Taimyr amber (Coleoptera). Cretaceous Research 115, 104548.CrossRefGoogle Scholar
Koziak, A. T. E., Cheng, K. C. & Thorn, R. G. 2007. Phylogenetic analyses of Nematoctonus and Hohenbuehelia (Pleurotaceae). Canadian Journal of Botany 85, 762–73.CrossRefGoogle Scholar
Kummer, P. 1871. Der Führer in die Pilzkunde [The guide to mycology]. Zerbst: C. Luppe, 146 pp. [In German.]Google Scholar
Kwok, O. C. H., Plattner, R., Weisleder, D. & Wicklow, D. T. 1992. A nematicidal toxin from Pleurotus ostreatus NRRL 3526. Journal of Chemycal Ecology 18, 127–36.CrossRefGoogle Scholar
Larsson, K. H. 2007. Molecular phylogeny of Hyphoderma and the reinstatement of Peniophorella. Mycological Research 111, 185–95.CrossRefGoogle ScholarPubMed
Li, J., Zou, C., Xu, J., Ji, X., Niu, X., Yang, J., Huang, X. & Zhang, K. Q. 2015. Molecular mechanisms of nematode–nematophagous microbe interactions: basis for biological control of plant-parasitic nematodes. Annual Review of Phytopathology 53, 6795.CrossRefGoogle ScholarPubMed
Liou, J. Y. & Tzean, S. S. 1992. Stephanocysts as nematode-trapping and infecting propagules. Mycologia 84, 786–90.CrossRefGoogle Scholar
Liu, X., Xiang, M. & Che, Y. 2009. The living strategy of nematophagous fungi. Mycoscience 50, 20–5.CrossRefGoogle Scholar
Lopez-Llorca, L. V. & Jansson, H. B. 2006. Fungal parasites of invertebrates: multimodal biocontrol agents. In Robson, G. D., West, P. V. & Gadd, G. M. (eds) Exploitation of fungi, 310–35. Cambridge, UK: Cambridge University Press.Google Scholar
Luo, H., Li, X., Li, G., Pan, Y. & Zhang, K. 2006. Acanthocytes of Stropharia rugosoannulata function as a nematode-attacking device. Applied and Environmental Microbiology 72, 2982–7.CrossRefGoogle ScholarPubMed
Luo, H., Liu, Y., Fang, L., Li, X., Tang, N. & Zhang, K. 2007. Coprinus comatus damages nematode cuticles mechanically with spiny balls and produces potent toxins to immobilize nematodes. Applied and Environmental Microbiology 73, 3916–23.CrossRefGoogle ScholarPubMed
Luo, H., Mo, M., Huang, X., Li, X. & Zhang, K. 2004. Coprinus comatus: a basidiomycete fungus forms novel spiny structures and infects nematode. Mycologia 96, 1218–25.CrossRefGoogle ScholarPubMed
Maire, R. 1933. Fungi Catalaunici: contributions à l’étude de la flore mycologique de la Catalogne [Catalan fungi: contributions to the study of the mycological flora of Catalonia]. In Treballs del Museu de Ciències Naturals Barcelona. Serie Botanica, XV, 2, 1–120. Barcelona: Museu de Cienciec Naturales. [In French.]Google Scholar
Makarov, K. V. & Perkovsky, E. E. 2020. Smallest and oldest false skin beetle: Paleobiphyllus ponomarenkoi gen. et sp. nov. (Coleoptera: Cleroidea: Biphyllidae) from Santonian Taimyr amber, northern Russia. Cretaceous Research 106, 104238.CrossRefGoogle Scholar
Mamiya, Y., Hiratsuka, M. & Murata, M. 2005. Ability of wood-decay fungi to prey on the pinewood nematode, Bursaphelenchus xylophilus (Steiner and Buhrer) Nickle. Japanese Journal of Nematology 35, 2130.Google Scholar
Maslova, N. P., Tobias, A. V. & Kodrul, T. M. 2021. Recent studies of co-evolutionary relationships of fossil plants and fungi: success, problems, prospects. Paleontologicheskii Zhurnal 2021, 321. [In Russian. English translation: Paleontological Journal 55, 1–17.]Google Scholar
Melnitsky, S. I. & Ivanov, V. D. 2021. Two new species of the genus Archaeopolycentra (Trichoptera: Polycentropodidae) from Cretaceous Taimyr amber. Far Eastern Entomologist 444, 17.CrossRefGoogle Scholar
Métrod, G. 1940. Description de Galera [Description of Galera]. Bulletin Trimestriel de la Société Mycologique de France 56, 4656. [In French.]Google Scholar
Miller, O. K. 1969. A new species of Pleurotus with a coremioid imperfect stage. Mycologia 61, 887–93.CrossRefGoogle Scholar
Murrill, W. A. 1922. Dark-spored agarics - II. Gomphidius ands Stropharia. Mycologia 14, 121–42.CrossRefGoogle Scholar
Neda, H. 2004. Type studies of Pleurotus reported from Japan. Mycoscience 45, 181–7.CrossRefGoogle Scholar
Ogłaza, B., Perkovsky, E. E. & Wegierek, P. 2022a. Khatangaphis sibirica Kononova, 1975 (Hemiptera: Sternorrhyncha: Tajmyraphididae) redescription. Palaeoentomology 5, 6670.CrossRefGoogle Scholar
Ogłaza, B., Perkovsky, E. E. & Wegierek, P. 2022b. Canadaphis mordvilkoi, Kononova 1976 (Hemiptera: Sternorrhyncha: Canadaphididae) – redescription and neotype designation. Zootaxa 5183, 98103.CrossRefGoogle Scholar
Pegler, D. N. 1975. The classification of the genus Lentinus Fr. (Basidiomycota). Kavaka 3, 1120.Google Scholar
Peris, D. 2020. Coleoptera in amber from Cretaceous resiniferous forests. Cretaceous Research 113, 104484. https://doi.org/10.1016/j.cretres.2020.104484CrossRefGoogle Scholar
Perkovsky, E. E. 2022. Two different Cretaceous worlds: Taimyr and Kachin amber trichopterofaunas. Zoodiversity 56, 51–6.CrossRefGoogle Scholar
Perkovsky, E. E., Sukhomlin, E. B. & Zelenkov, N. V. 2018. An unexpectedly abundant new genus of black flies (Diptera, Simuliidae) from Upper Cretaceous Taimyr amber of Ugolyak, with discussion of the early evolution of birds at high latitudes. Cretaceous Research 90, 80–9.CrossRefGoogle Scholar
Perkovsky, E. E. & Vasilenko, D. V. 2019. A summary of recent results in the study of Taimyr amber. Paleontological Journal 53, 984–93.CrossRefGoogle Scholar
Perkovsky, E. E. & Wegierek, P. 2017. Oldest amber species of Palaeoaphididae (Hemiptera) from Baikura (Taimyr amber). Cretaceous Research 80, 5660. https://doi.org/10.1016/j.cretres.2017.08.013CrossRefGoogle Scholar
Persoon, C. H. 1797. Tentamen Dispositionis Methodice Fungorum in Classes Ordines Genera et Familias. Cum supplemento adjecta [An Attempt at the Methodical Arrangement of Fungi into Classes, Orders, Genera and Families. With supplement added]. Lipsiae [Leipzig]: Wolf, 92 pp. [In Latin.]Google Scholar
Poinar, G. Jr. 2016. Fossil fleshy fungi ("mushrooms") in amber. Fungal Genomics & Biology 6, 142.CrossRefGoogle Scholar
Poinar, G. O. Jr. & Brown, A. E. 2003. A non-gilled hymenomycete in Cretaceous amber. Mycological Research 17, 763–8.CrossRefGoogle Scholar
Poinar, G. O. Jr., da Silva, A. D. & Baseia, I. G. 2014. A gasteroid fungus, Palaeogaster micromorpha gen. & sp. nov. (Boletales) in Cretaceous Myanmar amber. Journal of the Botanical Research Institute of Texas 8, 139–43.Google Scholar
Quélet, L. 1872. Les champignons du Jura et des Vosges [Mushrooms from Jura and Vosges]. Mémoires de la Société d'Émulation de Montbéliard 5, 43332. [In French.]Google Scholar
Rasnitsyn, A. P., Bashkuev, A. S., Kopylov, D. S., Lukashevich, E. D., Ponomarenko, A. G., Popov, Yu. A., Rasnitsyn, D. A., Ryzhkova, O. V., Sidorchuk, E. A., Sukatsheva, I. D. & Vorontsov, D. D. 2016. Sequence and scale of changes in the terrestrial biota during the Cretaceous (based on materials from fossil resins). Cretaceous Research 61, 234–55.CrossRefGoogle Scholar
Redhead, S. A. & Ginns, J.H. 1985. A reappraisal of agaric genera associated with brown rots of wood. Transactions of the Mycological Society of Japan 26, 349–81.Google Scholar
Reshetnikov, S. V. 1991. Evolution of asexual reproduction in higher basidiomycetes. Kyiv: Naukova Dumka, 188 pp. [In Russian.]Google Scholar
Ryvarden, L. 1972. A critical checklist of the Polyporaceae in tropical East Africa. Norwegian Journal of Botany 19, 229–38.Google Scholar
Saks, V. N., Gramberg, I. S., Ronkina, Z. Z. & Aplonova, E. N. 1959. The Mesozoic deposits of the Khatanga depression. Trudy Nauchno-issledovatel'skogo Instituta Geologii Arktiki 99, 1246. [In Russian.]Google Scholar
Schmalhausen, J. 1890. Tertiäre Pflanzen der Insel Neusibirien [Tertiary plants of the Novaya Sibir Island]. Mémoires de l'Académie impériale des sciences de St. Pétersbourg. VII ser 37, 122. [In German.]Google Scholar
Schulzer, S., Kanitz, A. & Knapp, J. A. 1866. Die bisher bekannten pflanzen Slavoniens, ein versuch [Essay on known to date plants of Slavonia]. Verhandlungen der Zoologisch-Botanischen Gesellschaft 16, 3172. Wien: C. Czermak. [In German]Google Scholar
Shear, C. L. 1902. Mycological notes and new species. Bulletin of the Torrey Botanical Club 29, 449–57.CrossRefGoogle Scholar
Siddiqui, Z. A. & Mahmood, I. 1996. Biological control of Heterodera cajani and Fusarium udum on pigeonpea by Glomus mosseae, Trichoderma harzianum, and Verticillium chlamydosporium. Israel Journal of Plant Sciences 44, 4956.CrossRefGoogle Scholar
Singer, R. 1951. The Agaricales in modern taxonomy. Lilloa 22, 1832.Google Scholar
Stalpers, J. A. 1978. Identification of wood-inhabiting Aphyllophorales in pure culture. Studies in Mycology 16, 1248.Google Scholar
Swe, A., Li, J., Zhang, K. Q., Pointing, S. B., Jeewon, R. & Hyde, K. D. 2011. Nematode-trapping fungi. Current Research in Environmental & Applied Mycology 1, 126.Google Scholar
Tanney, J. B. & Hutchison, L. J. 2012. The production of nematode-immobilizing secretory cells by Climacodon septentrionalis. Mycoscience 53, 31–5.CrossRefGoogle Scholar
Thorn, R. G. & Barron, G. L. 1984. Carnivorous mushrooms. Science 224, 76–8.CrossRefGoogle ScholarPubMed
Thorn, R. G., Moncalvo, J.-M., Reddy, C. A. & Vilgalys, R. 2000. Phylogenetic analyses and the distribution of nematophagy support a monophyletic Pleurotaceae within the polyphyletic pleurotoid–lentinoid fungi. Mycologia 92, 241–52.CrossRefGoogle Scholar
Tian, N., Wang, Y. D., Zheng, S. & Shu, Z. 2020. White-rotting fungus with clamp-connections in a coniferous wood from the Lower Cretaceous of Heilongjiang Province, NE China. Cretaceous Research 105, 104014.CrossRefGoogle Scholar
Yang, Y., Yang, E., An, Z. & Liu, X. 2007. Evolution of nematode-trapping cells of predatory fungi of the Orbiliaceae based on evidence from rRNA-encoding DNA and multiprotein sequences. Proceedings of the National Academy of Sciences of the United States of America 104, 8379–84.CrossRefGoogle ScholarPubMed