Date Published: May 24, 2019
Publisher: Public Library of Science
Author(s): János Tamás Padra, Abarna V. M. Murugan, Kristina Sundell, Henrik Sundh, John Benktander, Sara K. Lindén, Peng Xu.
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.
In fish aquaculture, disease outbreaks limit the development of the industry because of associated ethical and economic issues. Current remedies by vaccination and/or antibiotic treatment are far from ideal: vaccines do not provide the ultimate solution to the problem due to severe side effects and limited efficacy for some pathogens . Use of antibiotics adds to the spreading of antibiotic resistant bacteria and genes into our environment . To increase fish welfare and aquaculture productivity, an improved understanding of host-pathogen interactions is necessary.
In this study, we demonstrated that A. hydrophila, V. harveyi, M. viscosa and Y. ruckeri bound to mucins from Atlantic salmon and Arctic char, whereas we did not detect specific binding of V. salmonicida to mucins from any of the epithelial sites. Binding specificity and avidity to mucins from different Atlantic salmon epithelial sites (skin, gills, pyloric ceca, proximal intestine and distal intestine) differed between pathogens. Mucin binding avidity was highest for A. hydrophila, then V. harveyi, M. viscosa and Y. ruckeri followed in decreasing order. M. viscosa and Y. ruckeri bound preferentially to intestinal mucins, A. hydrophila to gills and V. harveyi bound equally to mucins from all epithelial sites. Finally, we demonstrated that the effect of fluid velocity on binding to mucins differs between pathogens and mucin origin.