Diploid-dominant life cycles characterize the early evolution of Fungi

Abstract

Most of the described species in kingdom Fungi are contained in two phyla, the Ascomycota and the Basidiomycota (subkingdom Dikarya). As a result, our understanding of the biology of the kingdom is heavily influenced by traits observed in Dikarya, such as aerial spore dispersal and life cycles dominated by mitosis of haploid nuclei. We now appreciate that Fungi comprises numerous phylum-level lineages in addition to those of Dikarya, but the phylogeny and genetic characteristics of most of these lineages are poorly understood due to limited genome sampling. Here, we addressed major evolutionary trends in the non-Dikarya fungi by phylogenomic analysis of 69 newly generated draft genome sequences of the zoosporic (flagellated) lineages of true fungi. Our phylogeny indicated five lineages of zoosporic fungi and placed Blastocladiomycota, which has an alternation of haploid and diploid generations, as branching closer to the Dikarya than to the Chytridiomyceta. Our estimates of heterozygosity based on genome sequence data indicate that the zoosporic lineages plus the Zoopagomycota are frequently characterized by diploid-dominant life cycles. We mapped additional traits, such as ancestral cell-cycle regulators, cell-membrane– and cell-wall–associated genes, and the use of the amino acid selenocysteine on the phylogeny and found that these ancestral traits that are shared with Metazoa have been subject to extensive parallel loss across zoosporic lineages. Together, our results indicate a gradual transition in the genetics and cell biology of fungi from their ancestor and caution against assuming that traits measured in Dikarya are typical of other fungal lineages.

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

“…1). Our phylogeny is highly supported and is largely congruent with phylogenies from recent studies 9,15,17–19 .…”

“…Reconstructions of the last universal fungal ancestor (LUFA) became more and more nuanced with the inclusion of newly discovered and/or classified early diverging lineages 8,10,[12][13][14][15][16] . These results contributed to our current understanding of LUFA as a unicellular phagotrophic parasite of microalgae, possessing motile cell stages with amoeboid and flagellar motility and a chitinous cell wall, at least in part of its life cycle 9,15 . In contrast, derived fungi (i.e., Dikarya) are sessile terrestrial osmotrophs that grow septate hyphae, and their cells are covered by a rigid cell wall throughout their life cycle.…”

“…They not only exhibit an extreme diversity in morphological traits, but also in ecological functions, which make them key players in the ecosystem as symbionts, parasites or saprobes, among others. Kingdom Fungi, defined in the broad sense to include Rozellomycota and Microsporidia (also known as Opisthosporidia) and Aphelidomycota 8 , encompasses at least 10 phylum-level clades, with most of its phylogenetic diversity found in early-diverging fungi (EDF), an informal group comprising Rozello-, Aphelido-, Chytridio-, Sanchytrio-, Blastocladio-, Olpidio-, Zoopago- and Mucoromycota as well as Microsporidia 9,10 . Irrespective of significant flux in the taxonomic definition of Fungi 11 , how the earliest fungal ancestors are characterised and how they evolved from a unicellular opisthokont ancestor has been the subject of intense research.…”

A Genome Sequence Assembly of the Phototactic and Optogenetic Model Fungus Blastocladiella emersonii Reveals a Diversified Nucleotide-Cyclase Repertoire

“…of bases: 2,196,251,798). After some manual refinement to remove duplicated contigs, this process resulted in an assembly of 34.27 Mb, smaller in size than published Blastocladiomycota species (see supplementary table S1, Supplementary Material online) for example; Allomyces macrogynus (NCBI: PRJNA20563; 57.06 Mb) and Catenaria anguillulae (NCBI: PRJNA330705; 41.34 Mb) ( Ruiz-Trillo et al 2007 ; Mondo et al 2017 ; Amses et al 2022 ). The B. emersonii genome assembly has an N50 of 2.02 Mb (see fig.…”

“…The earliest branches of the fungi include two major zoosporic radiations, the Blastocladiomycota and Sanchytriomycota forming one clade, and the Chytridiomycota forming the other ( Galindo et al 2021 ). Genomic studies of Blastocladiomycota and Chytridiomycota species are limited, with a few key genome data sets across diverse taxa ( Ruiz-Trillo et al 2007 ; Mondo et al 2017 ; Amses et al 2022 ). Blastocladiella emersonii has been found in soil and freshwater, with the American Type Culture Collection (ATCC) 22665 strain isolated from pond water in Pennsylvania (USA) over 70 years ago ( Cantino 1951 ).…”