The aphelid-like phagotrophic origins of fungi

Abstract

Aphelids are poorly known phagotrophic parasites of algae whose life cycle and morphology resemble those of the widely diverse parasitic rozellids (Cryptomycota, Rozellomycota). In previous phylogenetic analyses of RNA polymerase and rRNA genes, aphelids and rozellids formed a monophyletic group together with the extremely reduced parasitic Microsporidia, named Opisthosporidia, which was sister to Fungi. However, the statistical support for that group was always moderate. We generated the first transcriptome data for one aphelid species, Paraphelidium tribonemae. In-depth multi-gene phylogenomic analyses using various protein datasets place aphelids as the closest relatives of Fungi to the exclusion of rozellids and Microsporidia. In contrast with the comparatively reduced Rozella allomycis genome, we infer a rich, free-living-like aphelid proteome, including cellulases likely involved in algal cell-wall penetration, enzymes involved in chitin biosynthesis and several metabolic pathways. Our results suggest that Fungi evolved from a complex aphelid-like ancestor that lost phagotrophy and became osmotrophic.

Combined cultivation and single-cell approaches to the phylogenomics of nucleariid amoebae, close relatives of fungi

“…The last common ancestor of opisthokonts was probably phagotrophic with amoeboid polarized cell shape and a single flagellum, features that can be found in extant examples such as choanoflagellates [72], pigoraptors [73] or aphelids [9]. All known nucleariids lack flagella, suggesting that the last common ancestor of all nucleariids had already lost the ancestral flagellum.…”

“…Two distinct datasets, a dataset modified from Mikhailov et al [9,61] (dataset GBE: 264 protein alignments) and Torruella et al [9] (dataset SCPD: 74 single-copy domains) were updated with data from seven new nucleariid species. For both datasets, orthologues were identified by TBLASTN, aligned with MAFFT v7 and trimmed with TRIMAl with the automated1 option.…”

“…We also used publicly available data from two Nuclearia species [7], two Fonticula species [5,71] and Parvularia atlantis [20], adding representative members of other opisthokont lineages as outgroup. With these sequence datasets, we updated two datasets of conserved phylogenetic markers previously used to study the phylogeny of holomycotan clades [9,61]: the GBE dataset (264 proteins) and the SCPD dataset (74 single-copy protein domains-without N. pattersoni XT1 as no gene markers were retrieved for this species) (electronic supplementary material, figures S6A-D). As in the 18S rRNA gene phylogeny, all previously recognized nucleariids (Nuclearia, Fonticula and Parvularia) clustered together with Lithocolla and the two Pompholyxophrys species with maximum support in ML and BI analyses for both datasets, forming a sister clade to other Holomycota (figure 3).…”

“…They are thus part of the Holomycota (Nucletmycea), the opisthokont lineage containing fungi and its relatives [8]. The last opisthokont common ancestor probably was a phagotrophic cell with a single flagellum and polarized cell shape, a feature that is shared with the deepest-branching fungi and their aphelid [9] and rozellid [10] relatives [11].…”

Where are the basal fungi? Current status on diversity, ecology, evolution, and taxonomy

“…For instance, these groups lack chitinous cell walls in the major stages of their life cycle. Unlike most fungi, rozellids and aphelids are not osmotrophic, but use phagocytosis instead to engulf the host cytoplasm (Karpov et al 2017;Torruella et al 2017). Thus with various aspects considered including morphology and life cycle Fig.…”