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

Abstract

Compared to multicellular fungi and unicellular yeasts, unicellular fungi with free-living flagellated stages (zoospores) remain poorly known and their phylogenetic position is often unresolved. Recently, rRNA gene phylogenetic analyses of two atypical parasitic fungi with amoeboid zoospores and long kinetosomes, the sanchytrids Amoeboradix gromovi and Sanchytrium tribonematis, showed that they formed a monophyletic group without close affinity with known fungal clades. Here, we sequence single-cell genomes for both species to assess their phylogenetic position and evolution. Phylogenomic analyses using different protein datasets and a comprehensive taxon sampling result in an almost fully-resolved fungal tree, with Chytridiomycota as sister to all other fungi, and sanchytrids forming a well-supported, fast-evolving clade sister to Blastocladiomycota. Comparative genomic analyses across fungi and their allies (Holomycota) reveal an atypically reduced metabolic repertoire for sanchytrids. We infer three main independent flagellum losses from the distribution of over 60 flagellum-specific proteins across Holomycota. Based on sanchytrids’ phylogenetic position and unique traits, we propose the designation of a novel phylum, Sanchytriomycota. In addition, our results indicate that most of the hyphal morphogenesis gene repertoire of multicellular fungi had already evolved in early holomycotan lineages.

The cellular slime mold Fonticula alba forms a dynamic, multicellular collective while feeding on bacteria

“…Recent evidence suggests hyphal morphogenesis genes predate fungal multicellularity, and an aggregative origin to hyphae could explain this occurrence. 18 Multinuclear states are common in many protists. 34 Perhaps similar multinuclear and invasive evolutionary routes occurred in other protist branches such as myxomycetes and oomycetes.…”

“…Chytrids and other primitive fungi retain single cellular flagellate and amoeboid states, and emerging evidence suggests that rhizoid organizations common in chytrids may not predate hyphal arrangements. 18 , 17

Figure 1 F. alba invades virgin bacterial sources collectively (A) Tree approximating F. alb a location in eukaryotic evolution (for a more detailed tree, see Galindo et al. 18 and Brown et al.

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“… 18 , 17

Figure 1 F. alba invades virgin bacterial sources collectively (A) Tree approximating F. alb a location in eukaryotic evolution (for a more detailed tree, see Galindo et al. 18 and Brown et al. 19 ).

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“… (A) Tree approximating F. alb a location in eukaryotic evolution (for a more detailed tree, see Galindo et al. 18 and Brown et al. 19 ).…”

The taxonomy of the Trichophyton rubrum complex: a phylogenomic approach

“…Phylogenomics has been used in the past to elucidate evolutionary history in fungi [38–40], but to our knowledge, this is the first phylogenomic study conducted on the T. rubrum complex. The clarification of the relationships in the T. rubrum complex is important for correct identifications in clinical settings and to better understand the epidemiology of these pathogens.…”