Aphelids are a poorly known group of parasitoids of algae that have raised considerable interest due to their pivotal phylogenetic position. Together with Cryptomycota and the highly derived Microsporidia, they have been recently re-classified as the Opisthosporidia, which constitute the sister group to the fungi within the Holomycota. Despite their huge diversity, as revealed by molecular environmental studies, and their phylogenetic interest, only three genera have been described (Aphelidium, Amoeboaphelidium, and Pseudaphelidium), from which 18S rRNA gene sequences exist only for Amoeboaphelidium and Aphelidium species. Here, we describe the life cycle and ultrastructure of a new representative of Aphelida, Paraphelidium tribonemae gen. et sp.nov., and provide the first 18S rRNA gene sequence obtained for this genus. Molecular phylogenetic analysis indicates that Paraphelidium is distantly related to both Aphelidium and Amoebaphelidium, highlighting the wide genetic diversity of aphelids. Paraphelidium tribonemae has amoeboflagellate zoospores, rhomboid mitochondrial cristae in zoospores, trophonts and plasmodia; lipid-microbody complex and dictyosomes. The amoeboid trophont uses pseudopodia to feed from the host cytoplasm. Though genetically distinct, the genus Paraphelidium is morphologically indistinguishable from other aphelid genera and has zoospores able to produce lamellipodia with subfilopodia like those of Amoeboaphelidium.

Fungi encompass, in addition to classically well-studied lineages, an ever-expanding diversity of poorly known lineages including zoosporic chytrid-like parasites. Here, we formally describe Amoeboradix gromovi gen. et sp. nov. comprising a set of closely related strains of chytrid-like parasites of the yellow-green alga Tribonema gayanum unusually endowed with amoeboid zoospores. Morphological and ultrastructural features of A. gromovi observed by light and transmission electron microscopy recall previous descriptions of Rhizophydium anatropum. A. gromovi exhibits one of the longest kinetosomes known in eukaryotes, composed of microtubular singlets or doublets. To carry out molecular phylogenetic analysis and validate the identification of different life cycle stages, we amplified 18S rRNA genes from three A. gromovi strains infecting T. gayanum cultures, single sporangia and single zoospores. Molecular phylogenetic analyses of 18S+28S rRNA concatenated genes of the type strain revealed that A. gromovi is closely related to the recently described species Sanchytrium tribonematis, another parasite of Tribonema that had been tentatively classified within Monoblepharidomycetes. However, our phylogenetic analysis with an extended taxon sampling did not show any particular affinity of Amoeboradix and Sanchytrium with described fungal taxa. Therefore, Amoeboradix gromovi and Sanchytrium tribonematis likely represent a new divergent taxon that remains incertae sedis within Fungi.

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Aphelids (Aphelida) are poorly known parasitoids of algae that have raised considerable interest because of their phylogenetic position as phagotrophic protists sister to Fungi. Together with Rozellida and Microsporidia they have been classified in the Opisthosporidia but seem to be more closely related to the Fungi rather than to the Cryptomycota and Microsporidia, the other members of the Opisthosporidia. Molecular environmental studies have revealed high genetic diversity within the aphelids, but only four genera have been described: Aphelidium, Amoeboaphelidium, Paraphelidium and Pseudaphelidium. Here, we describe the life cycle of a new species of Aphelidium, Aph. arduennense. Molecular phylogenetic analysis of its 18S rRNA indicates that Aph. arduennense is sister to Aph. tribonematis, and together with Aph. melosirae they form a monophyletic cluster. Within the aphelids, this cluster is distantly related to Paraphelidium and Amoeboaphelidium.

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The aphelids, intracellular parasitoid of algae, play significant role in the ponds communities regulating the algae blooms. They represent a large cluster of OTUs sister to Fungi at the molecular phylogenetic tree sharing a common ancestor with fungi. Their vegetative life cycle being similar to that of chytridiomycetes includes opisthokont uniflagellar zoospores, cysts, phagotrophic intracellular stage, and multinuclear plasmodium producing zoospores. The sexual part of life cycle is not known, and, as we can see now, the asexual part is also understudied. We have found in the Aphelidium insulamus and other ahelid species a new stage – big multiflagellar, or amoeboid cells, which can be considered both, the result of zoospore fusion, or the remnant of plasmodium after zoospore formation. A study of this phenomenon lead us to the conclusion, that after multicellular infection the trophic stages of different parasitoids fuse in one plasmodium having different sorts of nuclei. Some of them become the nuclei of zoospores, while the others left in the remnant of plasmodium, which becomes a monster. The families of protein encoded genes involved in the vegetative cell fusion was also discussed.

Aphelids are a holomycotan group, represented exclusively by parasitoids infecting algae. They form a sister lineage to Fungi in the phylogenetic tree and represent a key group for reconstruction of the evolution of Holomycota and for analysis of the origin of Fungi. The newly assembled genome of Aphelidium insullamus (Holomycota, Aphelida) with a total length of 18.9Mb, 7820 protein-coding genes and a GC percentage of 52.05% was obtained by a hybrid assembly based on Oxford Nanopore long reads and Illumina paired reads. In order to trace the origin and the evolution of fungal osmotrophy and its presence or absence in Aphelida, we analyzed the set of main fungal transmembrane transporters, which are proteins of the Major Facilitator superfamily (MFS), in the predicted aphelid proteomes. This search has shown an absence of a specific fungal protein family Drug:H+ antiporters-2 (DAH-2) and specific fungal orthologs of the sugar porters (SP) family, and the presence of common opisthokont's orthologs of the SP family in four aphelid genomes. The repertoire of SP orthologs in aphelids turned out to be less diverse than in free-living opisthokonts, and one of the most limited among opisthokonts. We argue that aphelids do not show signs of similarity with fungi in terms of their osmotrophic abilities, despite the sister relationships of these groups. Moreover, the osmotrophic abilities of aphelids appear to be reduced in comparison with free-living unicellular opisthokonts. Therefore, we assume that the evolution of fungi-specific traits began after the separation of fungal and aphelid lineages, and there are no essential reasons to consider aphelids as a prototype of the fungal ancestor.