Taxonomic vs genomic fungi: contrasting evolutionary loss of protistan genomic heritage and emergence of fungal novelties

Abstract

Fungi are among the most ecologically important heterotrophs that have radiated into most niches on Earth and fulfil key ecological services. However, despite intense interest in their origins, major genomic trends characterising the evolutionary route from a unicellular opisthokont ancestor to derived multicellular fungi remain poorly known. Here, we reconstructed gene family evolution across 123 genomes of fungi and relatives and show that a dominant trend in early fungal evolution has been the gradual shedding of protist genes and highly episodic innovation via gene duplication. We find that the gene content of early-diverging fungi is protist-like in many respects, owing to the conservation of protist genes in early fungi. While gene loss has been constant and gradual during early fungal evolution, our reconstructions show that gene innovation showed two peaks. Gene groups with the largest contribution to genomic change included extracellular proteins, transcription factors, as well as ones linked to the coordination of nutrient uptake with growth, highlighting the transition to a sessile osmotrophic feeding strategy and subsequent lifestyle evolution as important elements of early fungal evolution. Taken together, this work provided a highly resolved genome-wide catalogue of gene family changes across fungal evolution. This suggests that the genome of pre-fungal ancestors may have been transformed into the archetypal fungal genome by a combination of gradual gene loss, turnover and two large duplication events rather than by abrupt changes, and consequently, that the taxonomically defined fungal kingdom does not represent a genomically uniform assemblage of extant species characterized by diagnostic synapomorphies.

To the Origin of Fungi. Analysis of MFS Transporters of First Assembled Aphelidium Genome Highlights Dissimilarity of Osmotrophic Abilities between Aphelida and Fungi

“…Thus, there are about 6-11 specific fungal SP orthogroups. This fact agrees well with the tendency to the enhanced evolution of metabolic genes shown in fungi [20,44].…”

“…Hence, ideas about the morphology and lifestyle of the common ancestor of aphelids and fungi become vaguer than just the assumption that it was aphelid-like. Recently, a number of common genes have been discovered in fungi and aphelids [6,8,9,20] and some metabolitic features of their common ancestor have been identified [8]. However, if we consider separately each of the common features of fungi and aphelids, they do not allow us to reconstruct a precise image of their common ancestor.…”

“…MFS transporters in fungi are numerous and diverse because fungi, as obligate osmotrophic organisms, must transport all types of nutrient substrates across the membrane [19][20][21]. MFS proteins in fungi are represented both by families common to all organisms, such as Sugar Porters (SPs), and by fungal-specific families, such as Drug:H + Antiporters-2 (DHA-2) [18,19,[22][23][24].…”

Niche and ecosystem preference of earliest diverging fungi in soils

“…There are some concerns about the correct taxon names of EDF (Tedersoo et al 2018 ). Additionally, there are conflicting views on whether Aphelida, Microsporida, Rozellida, and related lineages belong in “Fungi” (Ocaña-Pallarès et al 2022 ; Merényi et al 2022 , preprint). This study ignored the controversy and treated EDF as fungi for convenience.…”