Journal
SCIENCE IMMUNOLOGY
Volume 5, Issue 44, Pages -Publisher
AMER ASSOC ADVANCEMENT SCIENCE
DOI: 10.1126/sciimmunol.aay3254
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Funding
- NSF [NSF-IOS-1457282]
- U.S. Department of Agriculture [USDA-NIFA-2016-09400]
- NIH [NIH 2R01GM085207-09, NIH P20GM103452]
- National Natural Science Foundation of China [31879045]
- Japan Society for the Promotion of Science (JSPS) KAKENHI [JP19K21158]
- JSPS Overseas Research Fellowships
- University of New Mexico's Initiative for Maximizing Student Development (IMSD) Program
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Although mammalian secretory immunoglobulin A (sIgA) targets mucosal pathogens for elimination, its interaction with the microbiota also enables commensal colonization and homeostasis. This paradoxical requirement in the control of pathogens versus microbiota raised the question of whether mucosal (secretory) Igs (sIgs) evolved primarily to protect mucosal surfaces from pathogens or to maintain microbiome homeostasis. To address this central question, we used a primitive vertebrate species (rainbow trout) in which we temporarily depleted its mucosal Ig (sIgT). Fish devoid of sIgT became highly susceptible to a mucosal parasite and failed to develop compensatory IgM responses against it. IgT depletion also induced a profound dysbiosis marked by the loss of sIgT-coated beneficial taxa, expansion of pathobionts, tissue damage, and inflammation. Restitution of sIgT levels in IgT-depleted fish led to a reversal of microbial translocation and tissue damage, as well as to restoration of microbiome homeostasis. Our findings indicate that specialization of sIgs in pathogen and microbiota control occurred concurrently early in evolution, thus revealing primordially conserved principles under which primitive and modern sIgs operate in the control of microbes at mucosal surfaces.
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