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Karpov, S. A.

Publications and source records attributed to Karpov, S. A..

3 recordsLinked to original sources

A parasitic flagellate among the Nucleariae: a new perspective on the phylogeny of Holomycota (Opisthokonta)

Holomycota, together with Holozoa, represents one of the two main branches of the supergroup Opisthokonta. Fungi, as well as three basal protist lineages Nuclearida, Rosellida, and Aphelida belong to Holomycota. Surprisingly, among all these holomycotan groups, only the most basal lineage, Nuclearida, lacks any traces of flagella in its life cycle and is represented by free-living amoebae, in contrast to the obligately parasitic and flagellated Rosellida and Aphelida, which evolved later. As the earliest-branching lineage, nucleariids play a key role in understanding the origin and diversification of Opisthokonta, which is presumed to have evolved from a uniflagellated ancestor. In this study, we describe the first known nucleariid that is parasitic on algae and possesses a flagellated stage in its life cycle. We studied the life cycle, and showed the ultrastructure of main life cycle stages of this parasite. The multigene phylogenetic tree based on the newly sequenced transcriptome demonstrated its basal position among nucleariids, forming a clade of environmental OTUs. This finding together with unique ultrastructural features, parasitic style of life, and presence of flagellum allowed us to describe a new species, genus, and family in the order Nuclearidida. We emended the diagnoses of the order, class, and phylum Nuclearida. Based on the ribosomal phylogenetic tree where the Insolitus nuclearius has a basal position among the nucleariids we discussed the evolution of this group from the uniflagellated ancestor and provided new insights into the early evolution of Holomycota in a whole, revising hypotheses regarding the opisthokont ancestor.

evolutionary biology↗

Phylogenomics of a new fungal phylum reveals multiple waves of reductive evolution across Holomycota

Compared to multicellular fungi and unicellular yeasts, unicellular fungi with free-living flagellated stages (zoospores) remain poorly known and their phylogenetic position is often unresolved. Recently, rRNA gene phylogenetic analyses of two atypical parasitic fungi with amoeboid zoospores and long kinetosomes, the sanchytrids Amoeboradix gromovi and Sanchytrium tribonematis, showed that they formed a monophyletic group without close affinity with known fungal clades. Here, we sequence single-cell genomes for both species to assess their phylogenetic position and evolution. Phylogenomic analyses using different protein datasets and a comprehensive taxon sampling result in an almost fully-resolved fungal tree, with Chytridiomycota as sister to all other fungi, and sanchytrids forming a well-supported, fast-evolving clade sister to Blastocladiomycota. Comparative genomic analyses across fungi and their allies (Holomycota) reveal an atypically reduced metabolic repertoire for sanchytrids. We infer three main independent flagellum losses from the distribution of over 60 flagellum-specific proteins across Holomycota. Based on sanchytrids phylogenetic position and unique traits, we propose the designation of a novel phylum, Sanchytriomycota. In addition, our results indicate that most of the hyphal morphogenesis gene repertoire of multicellular fungi had already evolved in early holomycotan lineages.

evolutionary biology↗

The transcriptome of Paraphelidium tribonemae illuminates the ancestry of Fungi and Opisthosporidia

Aphelids constitute a group of diverse, yet poorly known, parasites of algae [1, 2]. Their life cycle and morphology resemble those of zoosporic fungi (chytrids) and rozellids (Cryptomycota/Rozellosporidia), another specious group of parasites of fungi and oomycetes [3, 4]. Unlike fungi, which are osmotrophs, aphelids and rozellids are phagotrophs, feeding on the hosts cytoplasm. Combined RNA polymerase and rRNA gene trees [5] suggested that aphelids and rozellids relate to Microsporidia, extremely reduced parasites with remnant mitochondria [6]. Accordingly, aphelids, rozellids and Microsporidia were proposed to form a monophyletic clade, called Opisthosporidia, sister to Fungi [1]. Microsporidia would have subsequently lost the ancestral opisthosporidian phagotrophy. However, the limited phylogenetic signal of those genes combined with microsporidian fast-evolving sequences have resulted in incongruent tree topologies, showing either rozellids [5, 7] or aphelids [8] as the earliest-branching lineages of Opisthosporidia. We have generated the first transcriptome data for one aphelid species, Paraphelidium tribonemae [2]. In-depth multi-gene phylogenomic analyses using various protein datasets place aphelids in a deep, pivotal position as a sister group to Fungi, making Opisthosporidia paraphyletic. We infer a rich, free-living-like proteome for P. tribonemae, which includes cellulases likely involved in algal cell-wall penetration, enzymes involved in chitin biosynthesis and several metabolic pathways that were lost in the comparatively reduced Rozella allomycis genome [9]. Our results suggest that Fungi evolved from a complex phagotrophic opisthosporidian ancestor, likely a specialized endobiotic predator, which became osmotrophic at the fungal root and evolved towards phagotrophic parasitism in the rozellid/microsporidian line.

evolutionary biology↗