Examination of mycoparasites reveals a new type of host-parasite interface and rearranges the taxonomy of <i>Occultifur</i> and <i>Microsporomyces</i> (<i>Cystobasidiomycetes</i>, <i> Basidiomycota</i>)

The present study investigates the species boundaries, evolutionary relationships, and host-parasite interfaces of dimorphic mycoparasites that were previously assigned to <i>Achroomyces soranus</i>, <i>Occultifur internus</i>, and <i>Platygloea mycophila</i> based on morphological similarities<i>.</i> Our comparison of recently collected and cultivated samples with the type specimens of <i>A. soranus</i> and <i>P. mycophila</i> shows that both groups are species complexes, of which the taxa can be differentiated based on morphological and ecological characters. By integrating the results of a seven-locus dataset (SSU, LSU, ITS, <i>RPB1</i>, <i>RPB2</i>, <i>TEF1</i>, and mitochondrial <i>CYT-B</i>) and detailed micromorphological comparisons of the investigated specimens, we show for the first time that these three groups of mycoparasites belong to <i>Cystobasidiomycetes</i> (<i>Pucciniomycotina</i>). We applied a polyphasic species concept involving morphology, phylogeny, and ecology to delineate and circumscribe these and new genera. The genus <i>Occultifur</i> comprises six species. <i>Occultifur internus</i> and the newly proposed <i>O. cerinomycicola</i> are intrahymenial mycoparasites producing haustorial cells and establishing fusion pore interaction with their Dacrymycetous host. Based on microscopical examination, we show that <i>Achroomyces soranus</i> is a member of the genus <i>Occultifur</i>. Based on the molecular phylogenetic reconstruction, we found that three lichen-associated fungi which are only known from a yeast morph are nested within <i>Occultifur</i>, <i>i.e. Lichenozyma pisutiana</i>, <i>Microsporomyces cladoniae</i>, and <i>M. wangii</i>. The genus <i>Obvidator</i> is newly introduced for three mycoparasitic species inhabiting members of the corticioid genus <i>Peniophora</i> (<i>Russulales</i>, <i>Agaricomycetes</i>) and causing gall-like malformations of the host basidiome. Microscopic investigation shows that <i>Platygloea mycophila</i> is a member of this genus. <i>Obvidator</i> species display a yet undiscovered type of host-parasite interface, in which the mycoparasites produce short protrusions on their hyphae adjacent to the host hyphae. The lysis of the host cell wall takes place at points of contact with parasite protrusions, but no rupture of the host plasma membrane or nanometer-fusion pore formation was observed. The updated <i>Cystobasidiomycetes</i> phylogeny obtained in this study by including mycoparasites showed that the genera <i>Occultifur</i> and <i>Microsporomyces</i> as currently circumscribed are polyphyletic. To resolve this polyphyly, we introduce two new genera, <i>i.e. Cystastrum</i> and <i>Millanizyma</i>, and recombine species comprising the <i>Occultifur externus</i> clade and a clade consisting of <i>Microsporomyces bloemfonteinensis</i> and <i>M. cladoniophilus</i>, respectively. <b>Taxonomic novelties: New genera:</b> <i>Cystastrum</i> Schoutteten & Yurkov, <i>Millanizyma</i> Schoutteten & Yurkov, <i>Obvidator</i> Schoutteten<i>.</i> <b>New species:</b> <i>Obvidator incarnatae</i> Schoutteten & Yurkov, <i>Obvidator quercinae</i> Schoutteten & Yurkov, <i>Occultifur cerinomycicola</i> Schoutteten, Enzlin & Yurkov<i>.</i> <b>New combinations:</b> <i>Cystastrum brasiliense</i> (F.C.O. Gomes <i>et al.</i>) Schoutteten, <i>Cystastrum externum</i> (J.P. Samp. <i>et al.</i>) Schoutteten & Yurkov, <i>Cystastrum kilbournense</i> (Kurtzman & Robnett <i>ex</i> Denchev & T. Denchev) Schoutteten & Yurkov, <i>Cystastrum mephitis</i> (Zalar <i>et al</i>.) Schoutteten & Yurkov, <i>Cystastrum tropicale</i> (Khunnamw. <i>et al. ex</i> Denchev & T. Denchev) Schoutteten & Yurkov, <i>Cystastrum plantarum</i> (Khunnamw. <i>et al.</i>) Schoutteten & Yurkov, <i>Millanizyma bloemfonteinensis</i> (C.H. Pohl <i>et al.</i>) Schoutteten & Yurkov, <i>Millanizyma cladoniophila</i> (N.H. Nguyen <i>et al.</i>) Schoutteten & Yurkov, <i>Occultifur cladoniae</i> (Kachalkin <i>et al.</i>) Schoutteten, <i>Occultifur pisutianus</i> (Černajová & Škaloud) Schoutteten, <i>Obvidator mycophilus</i> (Burds. & Gilb.) Schoutteten, <i>Occultifur soranus</i> (Hauerslev) Schoutteten, <i>Occultifur wangii</i> (Kachalkin <i>et al.</i>) Schoutteten<i>.</i> <b>Citation:</b> Schoutteten N, Yurkov A, Spirin V, Savchenko A, Aime MC, Begerow D, Verbeken A (2024). Examination of mycoparasites reveals a new type of host-parasite interface and rearranges the taxonomy of <i>Occultifur</i> and <i>Microsporomyces</i> (<i>Cystobasidiomycetes</i>, <i>Basidiomycota</i>). <i>Studies in Mycology</i> <b>109</b>: 451-486. doi: 10.3114/sim.2024.109.07.