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Research article2019Peer reviewedOpen access

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

Venkatakrishnan, Vignesh; Karlsson, Niclas G.; Linden, Sara K.; Padra, Janos T.; Sundh, Henrik; Sundell, Kristina; Jin, Chunsheng; Langeland, Markus; Carlberg, Hanna; Vidakovic, Aleksander; Lundh, Torbjorn

Abstract

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-S-type and sialylated O-glycans. Disialic-acid-epitope-containing structures including NeuAc alpha 2,8NeuAc, NeuAc(Gc)alpha 2,8NeuGc(Ac), and NeuGca2,8NeuGc 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.

Keywords

Arctic charr; Atlantic salmon; core-5 O-glycans; disialic acids; distal intestine; liquid-chromatography tandem mass spectrometry; mucin O-glycans; NeuGc; sialic acid; soybean diet

Published in

Journal of Proteome Research
2019, Volume: 18, number: 4, pages: 1760-1773