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We report on the isolation and characterization of three isolates of anaerobic gut fungi from a cattle faecal sample obtained in Stillwater, OK, USA. The isolates produced polycentric thalli with nucleated rhizomycelia, lobed appressorium-like structures, intercalary sporangia and constricted sausage-like hyphae. These morphological features are characteristic of members of the genusAnaeromyces. No zoospore production was observed during the isolation process or thereafter. The strains seemed to have propagated solely through their nucleated hyphae post initial enrichment. Phylogenetic analysis of the D1/D2 region of the large ribosomal subunit (D1/D2 LSU) rRNA, the ribosomal intergenic spacer region 1 (ITS1), RNA polymerase II large subunit (RPB1) and comparative average amino acid identity using transcriptomic datasets further confirmed the position of the type strain as a distinct member of the genusAnaeromyces, familyAnaeromycetaceaeand phylumNeocallimastigomycota. We propose to accommodate these isolates into a new species (Anaeromyces corallioides) within the genusAnaeromyces. The type strain is EE.1. 

Abstract Anaerobic gut fungi (AGF,Neocallimastigomycota) reside in the alimentary tract of herbivores. While their presence in mammals is well documented, evidence for their occurrence in non-mammalian hosts is currently sparse. Culture-independent surveys of AGF in tortoises identified a unique community, with three novel deep-branching genera representing >90% of sequences in most samples. Representatives of all genera were successfully isolated under strict anaerobic conditions. Transcriptomics-enabled phylogenomic and molecular dating analyses indicated an ancient, deep-branching position in the AGF tree for these genera, with an evolutionary divergence time estimate of 104-112 million years ago (Mya). Such estimates push the establishment of animal-Neocallimastigomycotasymbiosis from the late to the early Cretaceous. Further, tortoise-associated isolates (T-AGF) exhibited limited capacity for plant polysaccharides metabolism and lacked genes encoding several carbohydrate-active enzyme (CAZyme) families. Finally, we demonstrate that the observed curtailed degradation capacities and reduced CAZyme repertoire is driven by the paucity of horizontal gene transfer (HGT) in T-AGF genomes, compared to their mammalian counterparts. This reduced capacity was reflected in an altered cellulosomal production capacity in T-AGF. Our findings provide insights into the phylogenetic diversity, ecological distribution, evolutionary history, evolution of fungal-host nutritional symbiosis, and dynamics of genes acquisition inNeocallimastigomycota.