Diversity of colacosome-interacting mycoparasites expands the understanding of the evolution and ecology of Microbotryomycetes

Abstract

Mycoparasites in Basidiomycota comprise a diverse group of fungi, both morphologically and phylogenetically. They interact with their hosts through either fusion-interaction or colacosome-interaction. Colacosomes are subcellular structures formed by the mycoparasite at the host–parasite interface, which penetrate the parasite and host cell walls. Previously, these structures were detected in 19 fungal species, usually by means of transmission electron microscopy. Most colacosome-forming species have been assigned to Microbotryomycetes (Pucciniomycotina, Basidiomycota), a highly diverse class, comprising saprobic yeasts, mycoparasites, and phytoparasites. In general, these myco- and phytoparasites are dimorphic organisms, with a parasitic filamentous morph and saprobic yeast morph. We investigated colacosome-forming mycoparasites based on fungarium material, freshly collected specimens, and cultures of yeast morphs. We characterised the micromorphology of filamentous morphs, the physiological characteristics of yeast morphs, and inferred phylogenetic relationships based on DNA sequence data from seven loci. We outline and employ an epifluorescence-based microscopic method to assess the presence and organisation of colacosomes. We describe five new species in the genus Colacogloea, the novel dimorphic mycoparasite Mycogloiocolax gerardii, and provide the first report of a sexual, mycoparasitic morph in Colacogloea philyla and in the genus Slooffia. We detected colacosomes in eight fungal species, which brings the total number of known colacosome-forming fungi to 27. Finally, we revealed three distinct types of colacosome organisation in Microbotryomycetes.

Mycoparasitism in Basidiomycota

“…A third type is recognised as a regular placement of colacosomes in parasite hyphae coiling around host hyphae. So far, this type of arrangement has only been found in Colacogloea papilionacea and Slooffia micra (Kirschner & Oberwinkler 2001, Schoutteten et al 2023. A fourth type has been observed by Bauer (2004) in a yet undescribed colacosome-interacting mycoparasite of a Tulasnella host.…”

“…However, no DNA sequence data or ultrastructural data are available and it is questionable that these species have affinity to Cystobasidiomycetes. Schoutteten et al (2023) suggested that C. sebaceum is most likely a member of the genus Slooffia (Microbotryomycetes).…”

“…At least four different types of colacosome arrangement are currently known in microbotryomycetous mycoparasites (Bauer 2004, Schoutteten et al 2023. The first type is characterised by a more or less linear placement of colacosomes, where colacosomes are formed along the contact surface of host and parasite hyphae.…”

“…The placement in Microbotryomycetes was tentative for a long time, based on the presence of colacosomes and septal pore ultrastructure. Schoutteten et al (2023) provided DNA sequence data for this species and showed that it is a member of Microbotryomycetes based on molecular phylogenetic reconstruction.…”

“…Micromorphologically, the species is characterised by transversally three-septate basidia producing ballistospores, the absence of distinct probasidia, the presence of conidiophores producing thick-walled conidia, and the presence of hyphidia and clamped hyphae. Schoutteten et al (2023) showed that C. effusa comprises a species complex, with at least six species in Europe which are associated with P. praetermissa and P. pubera. At least two distinct types of colacosome arrangement are known from this genus, i.e., colacosomes are arranged along touching hyphae of host and parasite, or in parasite-formed gall-like cells that surround host hyphae (Fig.…”