Exploring the Arctic Charr Intestinal Glycome: Evidence of Increased N‑Glycolylneuraminic Acid Levels and Changed Host–Pathogen Interactions in Response to Inflammation

Disease outbreaks are a limiting factor for the sustainable development of the aquaculture industry. The intestinal tract is covered by a mucus layer mainly comprised by highly glycosylated proteins called mucins. Mucins regulate pathogen adhesion, growth, and virulence, and the glycans are vital for these functions. We analyzed intestinal mucin O-glycans on mucins from control and full-fat extruded soy-bean-fed (known to cause enteritis) Arctic charr using liquid chromatography–tandem mass spectrometry. In total, 56 glycans were identified on Arctic charr intestinal mucins, with a high prevalence of core-5-type and sialylated O-glycans. Disialic-acid-epitope-containing structures including NeuAcα2,8NeuAc, NeuAc­(Gc)­α2,8NeuGc­(Ac), and NeuGcα2,8NeuGc were the hallmark of Arctic charr intestinal mucin glycosylation. Arctic charr fed with soy bean meal diet had lower (i) number of structures detected, (ii) interindividual variation, and (iii) N-glycolylneuraminic-acid-containing glycans compared with control Arctic charr. Furthermore, Aeromonas salmonicida grew less in response to mucins from inflamed Arctic charr than from the control group. The Arctic charr glycan repertoire differed from that of Atlantic salmon. In conclusion, the loss of N-glycolylneuraminic acid may be a biomarker for inflammation in Arctic char, and inflammation-induced glycosylation changes affect host–pathogen interactions.病害暴发是制约水产养殖业可持续发展的关键限制因素。肠道表面覆盖有一层以黏蛋白（mucins）为主要组成的黏液层，黏蛋白属于高度糖基化蛋白。黏蛋白可调控病原菌的黏附、增殖与毒力，而其表面的聚糖对这些功能的发挥至关重要。本研究采用液相色谱-串联质谱技术，对对照组以及饲喂可诱发肠炎的挤压膨化全脂大豆日粮的北极红点鲑（Arctic charr）的肠道黏蛋白O-聚糖进行了分析。共计在北极红点鲑肠道黏蛋白上鉴定出56种聚糖，其中核心5型（core-5-type）唾液酸化O-聚糖占比极高。包含NeuAcα2,8NeuAc、NeuAc(Gc)α2,8NeuGc(Ac)以及NeuGcα2,8NeuGc在内的双唾液酸表位结构，是北极红点鲑肠道黏蛋白糖基化的标志性特征。与对照组北极红点鲑相比，饲喂大豆粕日粮的北极红点鲑在三方面表现更低：（1）检测到的聚糖结构数量；（2）个体间变异程度；（3）含N-羟乙酰神经氨酸（N-glycolylneuraminic acid）的聚糖占比。此外，杀鲑气单胞菌（Aeromonas salmonicida）在接触发炎北极红点鲑的黏蛋白时，其增殖水平显著低于接触对照组黏蛋白时的水平。北极红点鲑的聚糖谱与大西洋鲑存在显著差异。综上，N-羟乙酰神经氨酸的缺失可作为北极红点鲑肠炎炎症的潜在生物标志物，而炎症诱导的糖基化改变会影响宿主-病原菌互作。