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Adaptive immunity induces mutualism between commensal eukaryotes

Author

Listed:
  • Kyla S. Ost

    (University of Utah School of Medicine
    University of Utah)

  • Teresa R. O’Meara

    (University of Michigan Medical School)

  • W. Zac Stephens

    (University of Utah School of Medicine
    University of Utah)

  • Tyson Chiaro

    (University of Utah School of Medicine
    University of Utah)

  • Haoyang Zhou

    (University of Utah School of Medicine
    University of Utah)

  • Jourdan Penman

    (University of Utah School of Medicine
    University of Utah)

  • Rickesha Bell

    (University of Utah School of Medicine
    University of Utah)

  • Jason R. Catanzaro

    (Yale University School of Medicine)

  • Deguang Song

    (Yale University School of Medicine)

  • Shakti Singh

    (Harbor–UCLA Medical Center)

  • Daniel H. Call

    (Brigham Young University)

  • Elizabeth Hwang-Wong

    (Johns Hopkins University School of Medicine)

  • Kimberly E. Hanson

    (University of Utah)

  • John F. Valentine

    (University of Utah School of Medicine)

  • Kenneth A. Christensen

    (Brigham Young University)

  • Ryan M. O’Connell

    (University of Utah School of Medicine
    University of Utah)

  • Brendan Cormack

    (Johns Hopkins University School of Medicine)

  • Ashraf S. Ibrahim

    (Harbor–UCLA Medical Center
    David Geffen School of Medicine at UCLA)

  • Noah W. Palm

    (Yale University School of Medicine)

  • Suzanne M. Noble

    (UCSF School of Medicine)

  • June L. Round

    (University of Utah School of Medicine
    University of Utah)

Abstract

Pathogenic fungi reside in the intestinal microbiota but rarely cause disease. Little is known about the interactions between fungi and the immune system that promote commensalism. Here we investigate the role of adaptive immunity in promoting mutual interactions between fungi and host. We find that potentially pathogenic Candida species induce and are targeted by intestinal immunoglobulin A (IgA) responses. Focused studies on Candida albicans reveal that the pathogenic hyphal morphotype, which is specialized for adhesion and invasion, is preferentially targeted and suppressed by intestinal IgA responses. IgA from mice and humans directly targets hyphal-enriched cell-surface adhesins. Although typically required for pathogenesis, C. albicans hyphae are less fit for gut colonization1,2 and we show that immune selection against hyphae improves the competitive fitness of C. albicans. C. albicans exacerbates intestinal colitis3 and we demonstrate that hyphae and an IgA-targeted adhesin exacerbate intestinal damage. Finally, using a clinically relevant vaccine to induce an adhesin-specific immune response protects mice from C. albicans-associated damage during colitis. Together, our findings show that adaptive immunity suppresses harmful fungal effectors, with benefits to both C. albicans and its host. Thus, IgA uniquely uncouples colonization from pathogenesis in commensal fungi to promote homeostasis.

Suggested Citation

  • Kyla S. Ost & Teresa R. O’Meara & W. Zac Stephens & Tyson Chiaro & Haoyang Zhou & Jourdan Penman & Rickesha Bell & Jason R. Catanzaro & Deguang Song & Shakti Singh & Daniel H. Call & Elizabeth Hwang-W, 2021. "Adaptive immunity induces mutualism between commensal eukaryotes," Nature, Nature, vol. 596(7870), pages 114-118, August.
  • Handle: RePEc:nat:nature:v:596:y:2021:i:7870:d:10.1038_s41586-021-03722-w
    DOI: 10.1038/s41586-021-03722-w
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    Cited by:

    1. Raquel Alonso-Roman & Antonia Last & Mohammad H. Mirhakkak & Jakob L. Sprague & Lars Möller & Peter Großmann & Katja Graf & Rena Gratz & Selene Mogavero & Slavena Vylkova & Gianni Panagiotou & Sascha , 2022. "Lactobacillus rhamnosus colonisation antagonizes Candida albicans by forcing metabolic adaptations that compromise pathogenicity," Nature Communications, Nature, vol. 13(1), pages 1-15, December.

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