Fungal symbiont transmitted by free-living mice promotes type 2 immunity

Yun Liao, Iris H. Gao, Takato Kusakabe, Woan-Yu Lin, Alexander Grier, Xiangyu Pan, Olga Morzhanaeva, Terrance P. Shea, Hiroshi Yano, Danielle Karo-Atar, Kaitlin A. Olsen, Ji Hoon Oh, Kurt J. Vandegrift, Irah L. King, Christina A. Cuomo, David Artis, Barbara Rehermann, Neil Lipman and Iliyan D. Iliev ()
Additional contact information
Yun Liao: Cornell University
Iris H. Gao: Cornell University
Takato Kusakabe: Cornell University
Woan-Yu Lin: Cornell University
Alexander Grier: Cornell University
Xiangyu Pan: Cornell University
Olga Morzhanaeva: Cornell University
Terrance P. Shea: Broad Institute of MIT and Harvard
Hiroshi Yano: Cornell University
Danielle Karo-Atar: Research Institute of the McGill University Health Centre
Kaitlin A. Olsen: Research Institute of the McGill University Health Centre
Ji Hoon Oh: DHHS
Kurt J. Vandegrift: The Pennsylvania State University
Irah L. King: Research Institute of the McGill University Health Centre
Christina A. Cuomo: Broad Institute of MIT and Harvard
David Artis: Cornell University
Barbara Rehermann: DHHS
Neil Lipman: Memorial Sloan Kettering Cancer Center and Weill Cornell Medicine
Iliyan D. Iliev: Cornell University

Nature, 2024, vol. 636, issue 8043, 697-704

Abstract: Abstract The gut mycobiota is crucial for intestinal homeostasis and immune function1. Yet its variability and inconsistent fungal colonization of laboratory mice hinders the study of the evolutionary and immune processes that underpin commensalism2,3. Here, we show that Kazachstania pintolopesii is a fungal commensal in wild urban and rural mice, with an exceptional ability to colonize the mouse gastrointestinal tract and dominate the gut mycobiome. Kazachstania pintolopesii colonization occurs in a bacteria-independent manner, results in enhanced colonization resistance to other fungi and is shielded from host immune surveillance, allowing commensal presence. Following changes in the mucosal environment, K. pintolopesii colonization triggers a type 2 immune response in mice and induces gastrointestinal eosinophilia. Mechanistically, we determined that K. pintolopesii activates type 2 immunity via the induction of epithelial IL-33 and downstream IL-33–ST2 signalling during mucus fluctuations. Kazachstania pintolopesii-induced type 2 immunity enhanced resistance to helminth infections or aggravated gastrointestinal allergy in a context-dependent manner. Our findings indicate that K. pintolopesii is a mouse commensal and serves as a valuable model organism for studying gut fungal commensalism and immunity in its native host. Its unnoticed presence in mouse facilities highlights the need to evaluate its influence on experimental outcomes and phenotypes.

Date: 2024
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DOI: 10.1038/s41586-024-08213-2

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