Genomic survey of a hyperparasitic microsporidianAmphiamblyssp. (Metchnikovellidae)

Abstract

Metchnikovellidae are a group of unusual microsporidians that lack some of the defining ultrastructural features characteristic of derived Microsporidia and are thought to be one of their earliest-branching lineages. The basal position of metchnikovellids was never confirmed by molecular phylogeny in published research, and thus far no genomic data for this group were available. In this work, we obtain a partial genome of metchnikovellid Amphiamblys sp. using multiple displacement amplification, next-generation sequencing, and metagenomic binning approaches. The partial genome, which we estimate to be close to 90% complete, displays genome compaction on par with gene-dense microsporidian genomes, but contains an unusual repertoire of unique repeat elements. Phylogenetic analyses of multigene datasets place Amphiamblys sp. as the first branch of the microsporidian lineage following the divergence of a mitochondriate microsporidian Mitosporidium. We find evidence for a mitochondrial remnant presumably functionally equivalent to a mitosome in Amphiamblys sp. and the common enzymatic complement for microsporidian anaerobic metabolism. Comparative genomic analyses identify the conservation of components for clathrin vesicle formation as one of the key features distinguishing the metchnikovellid from its highly derived relatives. The presented data confirm the notion of Metchnikovellidae as a less derived microsporidian group, and provide an additional stepping stone for reconstruction of an evolutionary transition from the early diverging parasitic fungi to derived Microsporidia.

Clarifying the Relationships between Microsporidia and Cryptomycota

“…) and Amphiamblys (Mikhailov et al. ), but the addition of nuclear and mitochondrial genomes of Paramicrosporidium saccamoebae (Quandt et al. ) have provided several intriguing new perspectives on microsporidian evolution.…”

“…Mitosporidium , sometimes referred to as the earliest branching microsporidian (Mikhailov et al. ; Quandt et al. ), has a mitochondrion, albeit lacking Complex I of the oxidative phosphorylation pathway.…”

“…Metchnikovellids (e.g. Amphiamblys, Amphiacantha) have traditionally been referred to as atypical, "primitive" microsporidians, but share many characters with LB-Microsporidia, and were recently shown to branch as sisters to them (Mikhailov et al 2017).…”

“…These three genera clearly share some features with classical LB-Microsporidia, including forms of polar filaments (not necessarily functional as extrusion apparatus), unwalled intracellular meront stages, and nonflagellated spores; but in other respects, they are dissimilar, Nucleophaga and Paramicrosporidium being the least structurally similar to LB-Microsporidia. Mitosporidium, sometimes referred to as the earliest branching microsporidian (Mikhailov et al 2017;Quandt et al 2017), has a mitochondrion, albeit lacking Complex I of the oxidative phosphorylation pathway. Paramicrosporidium has a canonical fungal mitochondrial genome, and shares more gene content with distantly related fungi than with its closest relatives (Quandt et al 2017).…”

Metchnikovella Dogieli Sp. N. (Microsporidia: Metchnikovellida), a Parasite of Archigregarines Selenidium Sp. From Polychaetes Pygospio Elegans

“…Based on unusual spore morphology and unusual life cycle without merogonial proliferation, metchnikovellids have been regarded as a monotypic taxon (Class Rudimicrosporea with a single family Metchnikovellidae) (Sprague, 1977). Basal position of metch-nikovellids in relation to other taxa of microsporidia was suggested by SSU rDNA-inferred phylogeny (Simdianov et al, 2009;Nassonova et al, 2015) and confirmed by phylogenomic analyses (Mikhailov et al, 2016;Nassonova et al, 2016). It is very hard to find and study metchnikovellids, because of their hyperparasitic life style, small size and occasional occurrence in the environment.…”