High-mannose N-glycosylation increases in gill mucus from Sparicotyle chrysophrii infected gilthead seabream (Sparus aurata) and correlates with expression of the mannosyltransferase alg11 and microbial opportunistic pathogens

Gilthead seabream (Sparus aurata) is an important fish in the aquaculture industry frequently suffering from Sparicotylosis caused by infection with the parasite Sparicotyle chrysophrii. The seabream gills are coated by a mucus layer containing a large abundance of O- and N-glycans. The glycan repertoire is important for homeostasis, host-microbiota interactions and infection as it influences microbial growth, quorum sensing, virulence and adhesion. Here, the mucus glycome from gills with and without experimental S. chrysophrii infection was analyzed using liquid chromatography mass spectrometry. Infection did not induce overall shifts in either terminal moieties or core structures among the 57 O-glycans identified. The proportion of the detected glycans (N + O-glycans) that were N-glycans was 54 % (median) in non-infected gill mucus, while it was 28 % in mucus from S. chrysophrii infected gills. Eight N-glycans were detected and the relative abundance of high mannose N-glycans was increased more than threefold in gill mucus from infected fish. By leveraging gill transcriptomic data, nine transcripts were found differentially expressed in S. chrysophrii infected fish. Notably, the expression of asparagine-linked glycosylation protein 11 (alg11), which codes for a mannosyltransferase that transfers mannose in an α1-2 linkage in the dolichol-linked oligosaccharide pathway correlated with the relative abundance of high-mannose N-glycans. The abundance of high mannose N-glycans also correlated with the number of S. chrysophrii parasites and the abundance of the bacterium 2013Ark19i (Candidatus Ichthyocystis sparus), proposed as the causing agent of epitheliocystis.