Stress Impairs Skin Barrier Function and Induces α2-3 Linked N-Acetylneuraminic Acid and Core 1 O-Glycans on Skin Mucins in Atlantic Salmon, Salmo salar.

John Benktander,Abarna V M Murugan,Sara K Lindén,Bendik Fyhn Terjesen,Jelena Kolarevic,Vignesh Venkatakrishnan,János Tamás Padra,Kristina Sundell,Henrik Sundh,Marnix Gorissen

doi:10.3390/ijms22031488

John Benktander, Abarna V M Murugan + Show 8 more

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https://doi.org/10.3390/ijms22031488

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Abstract

The skin barrier consists of mucus, primarily comprising highly glycosylated mucins, and the epithelium. Host mucin glycosylation governs interactions with pathogens and stress is associated with impaired epithelial barrier function. We characterized Atlantic salmon skin barrier function during chronic stress (high density) and mucin O-glycosylation changes in response to acute and chronic stress. Fish held at low (LD: 14–30 kg/m3) and high densities (HD: 50-80 kg/m3) were subjected to acute stress 24 h before sampling at 17 and 21 weeks after start of the experiment. Blood parameters indicated primary and secondary stress responses at both sampling points. At the second sampling, skin barrier function towards molecules was reduced in the HD compared to the LD group (Papp mannitol; p < 0.01). Liquid chromatography–mass spectrometry revealed 81 O-glycan structures from the skin. Fish subjected to both chronic and acute stress had an increased proportion of large O-glycan structures. Overall, four of the O-glycan changes have potential as indicators of stress, especially for the combined chronic and acute stress. Stress thus impairs skin barrier function and induces glycosylation changes, which have potential to both affect interactions with pathogens and serve as stress indicators.

Highlights

Atlantic salmon aquaculture has grown tremendously the last decades and the yearly world production has exceeded 2 million tonnes since 2012 [1]
Plasma cortisol levels and glucose were assessed as indicators of a primary stress response, while plasma sodium levels was used as indicator for osmoregulatory status
The observed reduction in skin barrier function in the high densities (HD) group at S2 suggest that this environment was stressful to the fish, even though no significant differences were observed in plasma cortisol or glucose levels

Summary

Introduction

Atlantic salmon aquaculture has grown tremendously the last decades and the yearly world production has exceeded 2 million tonnes since 2012 [1]. Upon recognition of a stressor, the central nervous system elicits a series of behavioral and physiological responses in order to restore homeostasis [9] In this primary response, the hypothalamic-pituitary gland-interrenal (HPI) axis is activated and leads to increased circulating levels of the glucocorticoid cortisol [9]. A conserved response to acute and chronic stress in vertebrates is impaired intestinal barrier function manifested as increased translocation of luminal content (e.g., ions, larger molecules and pathogens) and intestinal inflammation [16]. It is currently not known if acute or chronic stress affects skin barrier function of fish

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