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Wild herbivorous mammals (genus Neotoma) host a diverse but transient assemblage of fungi

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Abstract

Fungi are often overlooked in microbiome research and, as a result, little is known about the mammalian mycobiome. Although frequently detected in vertebrate guts and known to contribute to digestion in some herbivores, whether these eukaryotes are a persistent part of the mammalian gut microbiome remains contentious. To address this question, we sampled fungi from wild woodrats (Neotoma spp.) collected from 25 populations across the southwestern United States. For each animal, we collected a fecal sample in the wild, and then re-sampled the same individual after a month in captivity on a controlled diet. We characterized and quantified fungi using three techniques: ITS metabarcoding, shotgun metagenomics and qPCR. Wild individuals contained diverse fungal assemblages dominated by plant pathogens, widespread molds, and coprophilous taxa primarily in Ascomycota and Mucoromycota. Fungal abundance, diversity and composition differed between individuals, and was primarily influenced by animal geographic origin. Fungal abundance and diversity significantly declined in captivity, indicating that most fungi in wild hosts came from diet and environmental exposure. While this suggests that these mammals lack a persistent gut mycobiome, natural fungal exposure may still impact fungal dispersal and animal health.

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Data and code availability

Sequencing data can be found on the SRA under BioProjects PRJNA824056 and PRJNA722312. Code is available on GitHub at https://github.com/SBWeinstein/Neotoma_fungi.

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Acknowledgements

We thank Rodolfo Martínez-Mota, Tess E. Stapleton, Dylan M. Klure, Teri J. Orr, Kaylene Yamada, James Patton, James Malcolm, Madeline Nelson, and Margaret Doolin for assistance with sample collection and animal husbandry, and Bryn Dentinger and Alexander Bradshaw for discussions on fungal ecology and access to reference databases.

Funding

Support was provided by NSF Dimensions DEB 1342615, NSF IOS 1656497, and Ruth L. Kirschstein National Research Service Award NIH T32AI055434. ITS amplicon sequencing was performed at the University of Utah’s High-Throughput Genomics facility which is supported by NIH award number P30CA042014.

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    Authors and Affiliations

    1. School of Biological Sciences, University of Utah, Salt Lake City, UT, USA

      Sara B. Weinstein, Robert Greenhalgh & M. Denise Dearing

    2. Department of Pathology, Division of Microbiology and Immunology, University of Utah School of Medicine, Salt Lake City, UT, USA

      W. Zac Stephens & June L. Round

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    2. W. Zac Stephens
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    3. Robert Greenhalgh
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    4. June L. Round
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    Correspondence to Sara B. Weinstein.

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    Animal use was approved by the University of Utah IACUC (16-02011) and conducted under permits from CA (SC-8123), UT (1COLL5194-1,2), NV (333663), and AZ (SP773078).

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    Sara B. Weinstein and W. Zac Stephens are equally contributing lead authors.

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    Weinstein, S.B., Stephens, W.Z., Greenhalgh, R. et al. Wild herbivorous mammals (genus Neotoma) host a diverse but transient assemblage of fungi. Symbiosis 87, 45–58 (2022). https://doi.org/10.1007/s13199-022-00853-0

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