Jiang Qin, Zhu Xiaoyan, Sun Lingling, Xie Chunlin, Wang Xinkai, Ma Libao, Yan Xianghua
National Key Laboratory of Agricultural Microbiology, Frontiers Science Center for Animal Breeding and Sustainable Production, Hubei Hongshan Laboratory, College of Animal Sciences and Technology, Huazhong Agricultural University, Wuhan, Hubei, China; Yazhouwan National Laboratory (YNL), Sanya, China.
National Key Laboratory of Agricultural Microbiology, Frontiers Science Center for Animal Breeding and Sustainable Production, Hubei Hongshan Laboratory, College of Animal Sciences and Technology, Huazhong Agricultural University, Wuhan, Hubei, China.
J Nutr. 2025 Jan;155(1):52-65. doi: 10.1016/j.tjnut.2024.11.002. Epub 2024 Nov 10.
Secretory 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.
We hypothesized that Akkermansia muciniphila increases intestinal SIgA production in the early-weaned piglets.
Fecal 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, 10A. muciniphila, and 10A. muciniphila) (n = 10/group) to evaluate the effect of orally administered A. muciniphila on intestinal SIgA production and microbial composition.
HM 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.
Early intervention with A. muciniphila in nursing piglets can increases intestinal SIgA production and alter the reactivity toward commensal bacteria upon early weaning.
分泌型免疫球蛋白A（SIgA）是保护肠道上皮免受病原菌侵害、调节肠道微生物群组成和维持肠道内环境稳定的第一道防线。早期断奶策略可能会破坏仔猪肠道中的SIgA水平，导致免疫反应下降和早期断奶应激。然而，调节早期断奶仔猪SIgA的具体微生物机制尚不清楚。
我们假设嗜黏蛋白阿克曼氏菌可增加早期断奶仔猪肠道SIgA的产生。
比较6只环江微型猪（HM）和6只杜洛克×长白×大白（DLY）早期断奶仔猪的粪便SIgA水平、SIgA包被细菌丰度和粪便宏基因组，以确定参与SIgA调节的细菌种类。使用5组（对照组、嗜黏蛋白阿克曼氏菌、解淀粉乳杆菌、卷曲乳杆菌和嗜酸乳杆菌）出生后3周断奶的雄性无特定病原体C57BL/6J小鼠（每组n = 8）对4种细菌进行了研究。随后，将10日龄的长白×大白（LY）仔猪随机分为3组（对照组、10⁸嗜黏蛋白阿克曼氏菌组和10⁹嗜黏蛋白阿克曼氏菌组）（每组n = 10），以评估口服嗜黏蛋白阿克曼氏菌对肠道SIgA产生和微生物组成的影响。
HM早期断奶仔猪的SIgA水平[7.59μg/mg，95%置信区间（CI）：3.2，12，P = 0.002]和SIgA包被细菌丰度（8.64%，95%CI：3.2，14，P = 0.014）显著高于DLY仔猪。在小鼠模型中，给予嗜黏蛋白阿克曼氏菌显著提高了SIgA水平（3.50μg/mg，95%CI：0.59，6.4，P = 0.018）、SIgA包被细菌丰度（9.06%，95%CI：4，14，P = 0.018）和IgA浆细胞计数（6.1%，95%CI：4.3，8，P = 0.005）。在仔猪实验中，给LY仔猪口服嗜黏蛋白阿克曼氏菌显著提高了肠道SIgA浓度（4.22μg/mg，95%CI：0.37，8.5，P = 0.034），并改变了SIgA包被细菌的格局。
对哺乳仔猪进行嗜黏蛋白阿克曼氏菌早期干预可增加肠道SIgA的产生，并改变早期断奶时对共生细菌的反应性。
