BackgroundSecretory IgA (SIgA) is the first line of defense in protecting the intestinal epithelium against pathogenic bacteria, regulating gut microbiota composition, and maintaining intestinal homeostasis. Early weaning strategies may disrupt SIgA levels in piglet intestines, causing a decline in immune response and early weaning stress. However, the specific microbial mechanisms modulating SIgA in early-weaned piglets are not well understood. ObjectivesWe hypothesized that Akkermansia muciniphila increases intestinal SIgA production in the early-weaned piglets. MethodsFecal SIgA levels, SIgA-coated bacteria abundance, and fecal metagenomes were compared between 6 Huanjiang miniature (HM) and 6 Duroc×Landrace×Yorkshire (DLY) early-weaned piglets to identify bacterial species involved in SIgA modulation. Four bacterial species were investigated using 5 groups (Control, A. muciniphila, L. amylovorus, L. crispatus, and L. acidophilus) of male specific pathogen-free C57BL/6J mice, weaned 3 wk postbirth (n = 8/group). Subsequently, 10-d-old Landrace×Yorkshire (LY) piglets were randomly assigned to 3 groups (Control, 109A. muciniphila, and 108A. muciniphila) (n = 10/group) to evaluate the effect of orally administered A. muciniphila on intestinal SIgA production and microbial composition. ResultsHM early-weaned piglets showed significantly higher SIgA levels [7.59 μg/mg, 95% confidence interval (CI): 3.2, 12, P = 0.002] and SIgA-coated bacteria abundance (8.64%, 95% CI: 3.2, 14, P = 0.014) than DLY piglets. In the mouse model, the administration of A. muciniphila significantly increased SIgA levels (3.50 μg/mg, 95% CI: 0.59, 6.4, P = 0.018), SIgA-coated bacteria abundance (9.06%, 95% CI: 4, 14, P = 0.018), and IgA+ plasma cell counts (6.1%, 95% CI: 4.3, 8, P = 0.005). In the pig experiments, the oral administration of A. muciniphila to LY piglets significantly enhanced intestinal SIgA concentrations (4.22 μg/mg, 95% CI: 0.37, 8.5, P = 0.034) and altered the SIgA-coated bacterial landscape. ConclusionsEarly intervention with A. muciniphila in nursing piglets can increases intestinal SIgA production and alter the reactivity toward commensal bacteria upon early weaning.
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