Genome-scale phylogenetic analyses confirm Olpidium as the closest living zoosporic fungus to the non-flagellated, terrestrial fungi

Abstract

The zoosporic obligate endoparasites, Olpidium, hold a pivotal position to the reconstruction of the flagellum loss in fungi, one of the key morphological transitions associated with the colonization of land by the early fungi. We generated genome and transcriptome data from non-axenic zoospores of Olpidium bornovanus and used a metagenome approach to extract phylogenetically informative fungal markers. Our phylogenetic reconstruction strongly supported Olpidium as the closest zoosporic relative of the non-flagellated terrestrial fungi. Super-alignment analyses resolved Olpidium as sister to the non-flagellated terrestrial fungi, whereas a super-tree approach recovered different placements of Olpidium, but without strong support. Further investigations detected little conflicting signal among the sampled markers but revealed a potential polytomy in early fungal evolution associated with the branching order among Olpidium, Zoopagomycota and Mucoromycota. The branches defining the evolutionary relationships of these lineages were characterized by short branch lengths and low phylogenetic content and received equivocal support for alternative phylogenetic hypotheses from individual markers. These nodes were marked by important morphological innovations, including the transition to hyphal growth and the loss of flagellum, which enabled early fungi to explore new niches and resulted in rapid and temporally concurrent Precambrian diversifications of the ancestors of several phyla of fungi.

Cryogenian glacial habitats as a plant terrestrialisation cradle – the origin of the anydrophytes and Zygnematophyceae split

“…(iv) Intermittent conditions favoured the development of resistant resting spores" (Naranjo-Ortiz and Gabaldon 2019b). Here we further elaborate their hypothesis and indicate that as loss of flagella and sex by conjugation of zygomycetous fungi coincides with the Cryogenian glaciations (Taylor and Berbee, 2006;Lutzoni et al, 2018;Naranjo -Ortiz and Gabaldon 2019a;Chang et al, 2021) so the split of Zygnematophyceae from Anydrophytes happened under the same selective pressure of Cryogenian glaciations. Sexuality based on mere conjugation without flagellated gametes possibly facilitated in zygomycetous fungi and Zygnematophycea in a more effective and therefore evolutionarily more adaptive lifecycle as compared to flagellated gametes mediated sexuality of other Cryogenian land-inhabiting organisms.…”

“…sexual process) optimised for cold and dry conditions. It is accepted in the same period zygomycetous fungi (originally Zygomycota) also lost the flagella and evolved conjugation as a mechanism of sexual reproduction (Liu et al, 2006;Taylor and Berbee, 2006;Lutzoni et al, 2018;Naranjo -Ortiz and Gabaldon 2019;Chang et al, 2021). The hypothesis the same selective pressure of dry land stress conditions resulted in an independent evolution of conjugation in algae and fungi was originally proposed by Stebbins and Hill (1980).…”

“…Already Stebbins and Hill (1980) argued the same evolutionary constraint of dry land drove the convergent evolution of Zygnematophyceae and zygomycetous fungi (including Mucoromycota; former Zygomycota -Naranjo-Ortiz and Gabaldon 2019b; Chang et al, 2021) -loss of flagella and sexuality by conjugation. "'Zygomycetous' refers to a paraphyletic phylum (Zygomycota), and this in turn to a sexual structure, the zygospore, that is common to most lineages ascribed to it" (Naranjo-Ortiz and Gabaldon 2019b).…”

Early-diverging fungal phyla: taxonomy, species concept, ecology, distribution, anthropogenic impact, and novel phylogenetic proposals

“…The fifth clade of the chytrids consists of the genus Olpidium , which comprises unicellular, obligate parasites of plants that reproduce with flagellate, swimming zoospores (Voigt et al 2013 ). This genus remains a distinct clade at present, though Olpidium was postulated to form a monophyletic group with taxa traditionally classified in the Zygomycota (Sekimoto et al 2011 ; Chang et al 2021 ). Topology tests rejected all alternative trees that constrained the species of Olpidium to cluster with other groups of flagellate fungi.…”

“…Nevertheless, the deep-level phylogenetic relationships among the basal lineage fungi remained unsatisfactorily resolved when an oligogenic approach was used for phylogenetic reconstruction. In an endeavour to increase the phylogenetic signal by augmentation of the number of informative characters phylogenomic studies arose, which applied a multitude of orthologous genes and proteins to resolve the deep branches in the fungal tree (Spatafora et al 2016 ; Chang et al 2021 ).…”