A conserved minimal core and modular extensions make the fungal flagellum

Flagellated fungi are pivotal for understanding the evolution of eukaryotic motility, yet knowledge of their flagellar proteins remains fragmentary. We assembled a cross-phyla atlas by mapping 394 reference flagellar proteins on 184 fungal proteomes. Out of 394 orthogroups, 342 orthogroups have fungal homologs, of which 210 orthogroups are specific to flagellated fungi. From these, we propose a 184-orthogroup minimal flagellum encompassing proteins shared by flagellated fungi. This minimal toolkit retains the axonemal core (tubulins, dynein arms), beat regulators (nexin-dynein regulatory complex, radial spokes), intraflagellar transport (IFT-B, IFT-A, IFT kinesin, dynein), basal-body and trafficking (exocyst/TRAPP). Genes specific to the flagellum preferentially express during flagellated life cycle stages; but conserved flagellar genes show no such expression specificity, regardless of whether the species is flagellated. Fungal lineages differ in the composition of flagellar modules. Neocallimastigomycota stand out as the most diverged among flagellated lineages with the broadest flagellar toolkit, including a complete BBSome, yet reduced centriole-associated modules. We delineate a conserved engine for fungal motility and a modular, lineage-specific set of proteins that broadens regulation and sensory capacity. The conservation of flagellar proteins between fungi and animals opens up possibilities of experimental functional validation in models simpler than animals.