Fish pathogen binding to mucins from Atlantic salmon and Arctic char differs in avidity and specificity and is modulated by fluid velocity

Abstract

Disease outbreaks are limiting factors for an ethical and economically sustainable aquaculture industry. The first point of contact between a pathogen and a host occurs in the mucus, which covers the epithelial surfaces of the skin, gills and gastrointestinal tract. Increased knowledge on host-pathogen interactions at these primary barriers may contribute to development of disease prevention strategies. The mucus layer is built of highly glycosylated mucins, and mucin glycosylation differs between these epithelial sites. We have previously shown that A . salmonicida binds to Atlantic salmon mucins. Here we demonstrate binding of four additional bacteria, A . hydrophila , V . harveyi , M . viscosa and Y . ruckeri , to mucins from Atlantic salmon and Arctic char. No specific binding could be observed for V . salmonicida to any of the mucin groups. Mucin binding avidity was highest for A . hydrophila and A . salmonicida , followed by V . harveyi , M . viscosa and Y . ruckeri in decreasing order. Four of the pathogens showed highest binding to either gills or intestinal mucins, whereas none of the pathogens had preference for binding to skin mucins. Fluid velocity enhanced binding of intestinal mucins to A . hydrophila and A . salmonicida at 1.5 and 2 cm/s, whereas a velocity of 2 cm/s for skin mucins increased binding of A . salmonicida and decreased binding of A . hydrophila . Binding avidity, specificity and the effect of fluid velocity on binding thus differ between salmonid pathogens and with mucin origin. The results are in line with a model where the short skin mucin glycans contribute to contact with pathogens whereas pathogen binding to mucins with complex glycans aid the removal of pathogens from internal epithelial surfaces.

Dietary Chitosan Nanoparticles: Potential Role in Modulation of Rainbow Trout (Oncorhynchus mykiss) Antibacterial Defense and Intestinal Immunity against Enteric Redmouth Disease

“…The most predominant contents of fish intestinal mucus are the viscous glycoproteins, mucins, which have different types according to their glycosylation degree, and consider the main site of mucus interaction with the surroundings in addition to granting its antimicrobial characteristics [ 49 , 50 ]. The intestinal mucins contain complex glycans can act for pathogens elevation from the internal epithelium [ 51 ]. However, the commensal intestinal bacteria produce proteases that can rapidly degrade the immune elements of the intestinal mucus after being secreted in the lumen hindering their accurate quantification [ 49 ].…”

Mechanical induced wounds in fish – a review on models and healing mechanisms

“…Weak binding of bacteria to the mucus can be beneficial to ‘wash off’ bacteria and prevent colonization (Easy & Ross 2010; Padra et al . 2019) . In addition, extracellular proteins, such as enzymes, antimicrobial peptides and immunoglobulins, are active in the mucus gel, protecting the underlying epithelia, reviewed by multiple authors (Esteban 2012; Rakers et al .…”

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

“…Among the glycosylation changes identified, the increased proportion of large glycan structures suggests a decreased mucin production [ 46 ], which may contribute to the increased susceptibility to disease of stressed fish. The structural changes also have potential to affect host pathogen interactions [ 22 , 25 , 26 , 31 , 32 , 52 ]. Finally, the relative abundance of O -glycan structures Galß1-3(NeuAcα2-6)GalNacol, NeuAcα2-3Galß1-3(NeuAcα2-6)GalNAcol and core type 1 structures as well as the proportion of sialylation in the form of NeuAcα2-3 has potential as biomarkers for stress in fish, especially for the accumulative chronic and AS, as this was not apparent in any of the other stress markers.…”

“…The fish pathogen Aeromonas salmonicida binds to sialic acids on salmon mucins, and terminal N -Acetylhexosamine (HexNAc) on intestinal mucins promotes A. salmonicida growth [ 30 , 31 ]. A. hydrophila , Vibrio harveyi , Moritella viscosa , and Yersinia ruckeri , also bind to mucins from Atlantic salmon and Arctic char, although the structures they adhere to are currently not identified [ 32 ]. The glycan structures on mucins can thus greatly affect the interaction with pathogens [ 21 ].…”