Anaerobic fungi in the tortoise alimentary tract illuminate early stages of host-fungal symbiosis and Neocallimastigomycota evolution

Carrie J. Pratt, Casey H. Meili, Adrienne L. Jones, Darian K. Jackson, Emma E. England, Yan Wang, Steve Hartson, Janet Rogers, Mostafa S. Elshahed and Noha H. Youssef ()
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Carrie J. Pratt: Oklahoma State University
Casey H. Meili: Oklahoma State University
Adrienne L. Jones: Oklahoma State University
Darian K. Jackson: Oklahoma State University
Emma E. England: Oklahoma State University
Yan Wang: University of Toronto Scarborough
Steve Hartson: Oklahoma State University
Janet Rogers: Oklahoma State University
Mostafa S. Elshahed: Oklahoma State University
Noha H. Youssef: Oklahoma State University

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: 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-Neocallimastigomycota symbiosis 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 in Neocallimastigomycota.

Date: 2024
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DOI: 10.1038/s41467-024-47047-4

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