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Much of the diversity of microbes from natural habitats, such as soil and freshwater, comprise species and lineages that have never been isolated into pure culture. In part, this stems from a bias of culturing in favor of saprotrophic microbes over the myriad symbiotic ones that include parasitic and mutualistic relationships with other taxa. In the present study, we aimed to shed light on the ecological function and morphology of the many undescribed lineages of aquatic fungi by individually isolating and sequencing molecular barcodes from 127 cells of host-associated fungi using single-cell sequencing. By adding these sequences and their photographs into the fungal tree, we were able to understand the morphology of reproductive and vegetative structures of these novel fungi and to provide a hypothesized ecological function for them. These individual host-fungal cells revealed themselves to be complex environments despite their small size; numerous samples were hyper-parasitized with other zoosporic fungal lineages such as Rozellomycota. 

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. 

Most empirical research on biological shortfalls has focused on vertebrate taxa. This is important given many species in poorly studied groups such as invertebrates, plants, and fungi are predicted to possess high conservation risk. Here, we focus on Laboulbeniomycetes: a class of microfungi that are understudied. We examined four shortfalls: Linnean (knowledge gaps in species diversity), Wallacean (knowledge gaps in distributions), Latimerian (knowledge gaps in species persistence), and the newly introduced Scottian (knowledge gaps in species conservation assessments) shortfalls. The Linnean shortfall in Laboulbeniomycetes is hard to predict due to inconsistent species description rates. Analysis of distribution patterns indicates Laboulbeniomycetes are likely to experience an extremely high Wallacean shortfall, with many species having highly disjunct known distributions. Latimerian shortfall analysis shows over half (51%) of Laboulbeniomycetes have not been recorded in >50 years, while the group has a collective Scottian shortfall of 100%, given none of the 2454 described species have received an IUCN threat assessment. We suggest continued study of natural history collections, expanded citizen science programmes, and machine‐learning identification approaches as important tools for reducing knowledge shortfalls in both Laboulbeniomycetes and poorly studied taxa more generally.