Genome-scale phylogenetic analyses confirmOlpidiumas 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.

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

“…However, C. protostelioides branched in our multi-gene phylogenies within Chytridiomycota with maximum support, confirming that ultrastructural similarity most likely reflects convergent evolution. All our results concur to confirm that Olpidium constitutes a new phylum-level fungal linage (Olpidiomycota) sister to the non-flagellated fungi, in agreement with recent unpublished work by Chang et al 65 .…”

“…Likewise, if radiation characterized early fungal evolution 22 , the accumulation of enough sequence substitutions during diversification would have been limited. This would explain the difficulty to resolve the deepest branches of the fungal tree, the fact that Chytridiomycota and Blastocladiomycota have alternatively been recovered as sisters of all other fungi 21,26,27,39,65 and the low support and discrepancies observed for the split between Glomeromycota and Mucoromycota (with additional constraints related to their symbiotic adaptation to land plants 24,67,68 ). The solid position of the root of the fungal tree on the chytrid branch revealed by our phylogenomic analyses with a richer dataset is additionally consistent with the distribution of so-considered derived characters in Blastocladiomycota, including sporic meiosis, relatively small numbers of carbohydrate metabolism genes and, in some species, hyphal-like apical growing structures (Allomyces) and narrow sporangia exit tubes (e.g.…”

“…Likewise, if radiation characterized early fungal evolution 22 , the accumulation of enough sequence substitutions during diversification would have been limited. This would explain the difficulty to resolve the deepest branches of the fungal tree, the fact that Chytridiomycota and Blastocladiomycota have alternatively been recovered as sisters of all other fungi 21,26,27,39,65 and the low support and discrepancies observed for the split between Glomeromycota and (which was not certified by peer review) is the author/funder. All rights reserved.…”

Evolution of zygomycete secretomes and the origins of terrestrial fungal ecologies

“…The monophyly of each zygomycete subphyla (Glomeromycotina, Mortierellomycotina, Mucoromycotina, Entomophthoromycotina, Kickxellomycotina, and Zoopagomycotina) was well supported. The ''rogue'' genus Basidiobolus (Chang et al, 2021;Li et al, 2021) was resolved as part of Entomophthoromycotina and thus included in the subphylum in the subsequent analyses.…”

“…Zygomycete fungi comprise the first diverging lineages of Kingdom Fungi to emerge after the loss of the flagellum and the origin of the filamentous fungal thallus (Kiss et al, 2019). The two phylum level clades, Mucoromycota and Zoopagomycota, have been resolved as a paraphyletic grade (Chang et al, 2021;Spatafora et al, 2016) or sister groups (Li et al, 2021), depending on taxon sampling and the molecular markers employed. Zygomycetes are ubiquitous in nature and with diverse ecologies.…”