In Atlantic salmon skin infested with salmon lice, elevated seawater temperatures change gene expression and mucus glycosylation, which promotes pathogen binding

Abstract

Skin barrier function is paramount for fish health and is likely affected by the predicted increases in seawater temperature. Salmonid skin produces a mucus layer mainly composed of mucins. Mucin glycans regulate interactions with pathogens, including binding to host cells, quorum sensing and regulation of virulence genes. In this work, the objective was to elucidate the Atlantic salmon (Salmo salar) skin mucosal responses to temperature in the presence of salmon lice (Lepeophtheirus salmonis) to mimic salmon louse pressure at sea. A simultaneous louse and temperature challenge trial was performed, at low (5 °C), medium (10 °C), and high (17 °C) temperatures, using a protocol resulting in lice at the same development stage and density in all groups. Temperature affected skin morphology, with a thinner outer epidermal layer with fewer mucous cells at 17 °C than at 5 °C. Liquid chromatography–mass spectrometry demonstrated that the skin mucin O-glycome changed with temperature: the most pronounced glycan changes were a decrease of the disaccharide Sialyl-Tn and an increase of the tetrasaccharide NeuAcα2-3Galβ1-3[NeuAcα2-6]GalNAcol and sulfated glycans at 17 °C. Principal component analysis of gene expression data clustered samples according to temperature treatments, and changes in expression of homologues of human sialyl-, core 1-, Gal, and GalNAc transferase genes were proposed to be linked to the glycan changes observed by mass spectrometry. Finally, Aeromonas salmonicida had a higher ability to bind mucins from fish kept at 17 °C than at 5 °C, demonstrating effects of temperature related glycosylation changes on host-pathogen interactions.