Gill Mucus and Gill Mucin O-glycosylation in Healthy and Amebic Gill Disease-Affected Atlantic Salmon

Abstract

Amoebic gill disease (AGD) causes poor performance and death in salmonids. Mucins are mainly comprised by carbohydrates and are main components of the mucus covering the gill. Since glycans regulate pathogen binding and growth, glycosylation changes may affect susceptibility to primary and secondary infections. We investigated gill mucin O-glycosylation from Atlantic salmon with and without AGD using liquid chromatography–mass spectrometry. Gill mucin glycans were larger and more complex, diverse and fucosylated than skin mucins. Confocal microscopy revealed that fucosylated mucus coated sialylated mucus strands in ex vivo gill mucus. Terminal HexNAcs were more abundant among O-glycans from AGD-affected Atlantic salmon, whereas core 1 structures and structures with acidic moieties such as N-acetylneuraminic acid (NeuAc) and sulfate groups were less abundant compared to non-infected fish. The fucosylated and NeuAc-containing O-glycans were inversely proportional, with infected fish on the lower scale of NeuAc abundance and high on fucosylated structures. The fucosylated epitopes were of three types: Fuc-HexNAc-R, Gal-[Fuc-]HexNAc-R and HexNAc-[Fuc-]HexNAc-R. These blood group-like structures could be an avenue to diversify the glycan repertoire to limit infection in the exposed gills. Furthermore, care must be taken when using skin mucus as proxy for gill mucus, as gill mucins are distinctly different from skin mucins.

Host-Parasite Interaction of Atlantic salmon (Salmo salar) and the Ectoparasite Neoparamoeba perurans in Amoebic Gill Disease

“…A total of 18 metalloproteinases were identified in the enriched GO term 'metallopeptidase activity' which included stromelysin-3-like (144). Mucus production and wound healing metabolic processes are also upregulated in the gill, particularly transferases associated with glycoprotein production, a key component of mucus (145). Differential gene expression of mucins in AGD has previously been reported in proximity to gill lesions in AGD in Atlantic salmon (16).…”

Experimental Challenge Models and In Vitro Models to Investigate Efficacy of Treatments and Vaccines against Amoebic Gill Disease

“…Fish origin, size, age, health status should be reported. Atlantic salmon farmed at different geographical locations differ, for example geographical origin of Atlantic salmon affects mucus characteristics [ 69 ] which are important in AGD [ 70 ]. AGD resistant families are increasingly available and while they have to be tested as the commercial target for a vaccine or treatment, they may require higher concentrations of the amoebae, longer challenge times or different environmental conditions.…”

Fatty acid and lipid class composition in cutaneous mucus of Atlantic salmon,Salmo salar(L.)

“…Other fatty acids were at <5% abundance (Table 2), and variations between samples from the nine individuals in the same tank were relatively low. Comparison of the fatty acids in the total lipids of the salmon samples to similar studies is complicated by the influence of intrinsic and extrinsic factors, which affect the composition of the mucus, such as diet (Benktander et al, 2020; Ekman et al, 2015; Jung et al, 2012; van der Marel et al, 2010; Torrecillas et al, 2019). Nevertheless, the most abundant fatty acid constituents of cutaneous mucus of fish in earlier reports are C18:1n‐9, C16:0 and C18:0, which is consistent with this present study (Table 3).…”