Abstract
Fish have to face various environmental challenges that may compromise the efficacy of the immune response in mucosal surfaces. Since the effect of acute stress on mucosal barriers in fish has still not been fully elucidated, we aimed to compare the short-term mucosal stress and immune transcriptomic responses in a freshwater (rainbow trout, Oncorhynchus mykiss) and a marine fish (gilthead seabream, Sparus aurata) to bacterial immersion (Vibrio anguillarum bacterin vaccine) and air exposure stress in skin, gills, and intestine. Air exposure and combined (vaccine + air) stressors exposure were found to be inducers of the cortisol secretion in plasma and skin mucus on both species in a time-dependent manner, while V. anguillarum bacterin exposure induced cortisol release in trout skin mucus only. This was coincident with a marked differential increase in transcriptomic patterns of stress- and immune-related gene expression profiles. Particularly in seabream skin, the expression of cytokines was markedly enhanced, whereas in gills the response was mainly suppressed. In rainbow trout gut, both air exposure and vaccine stimulated the transcriptomic response, whereas in seabream, stress and immune responses were mainly induced by air exposure. Therefore, our comparative survey on the transcriptomic mucosal responses demonstrates that skin and gut were generally more reactive in both species. However, the upregulation of immune transcripts was more pronounced in gills and gut of vaccinated trout, whereas seabream appeared to be more stress-prone and less responsive to V. anguillarum bacterin in gills and gut. When fish were subjected to both treatments no definite pattern was observed. Overall, the results indicate that (1) the immune response was not homogeneous among mucosae (2), it was greatly influenced by the specific traits of each stressor in each surface and (3) was highly species-specific, probably as a result of the adaptive life story of each species to the microbial load and environmental characteristics of their respective natural habitats.
Highlights
Fish are living in a microbial-loaded environment involving an intense interaction of their mucosal surfaces with microbiota and various immune responses in these surfaces
In order to evaluate whether the application of air exposure, V. anguillarum bacterin, or the combination of both stressors induce a stress response systemic and local, cortisol levels were evaluated
Our findings illustrate the implication and importance of the mucosal immunity in response to different stressors and provide comparative data on the transcriptomic responses of several immunomodulators in mucosal-associated lymphoid tissues (MALTs) tissues. In species such as trout and seabream acclimated to their adaptive thermoneutral environments and confronted to V. anguillarum bacterin, our results show a higher responsiveness of skin and gills immune transcripts to the biotic stressor in trout than in seabream
Summary
Fish are living in a microbial-loaded environment involving an intense interaction of their mucosal surfaces with microbiota and various immune responses in these surfaces. When interacting with mucosal interfaces, exogenous bacteria and viruses skew the immune responsiveness depending on each surface Pathogens, such as Vibrio anguillarum, are able to adhere preferentially to fish integument [7], modifying the thickness, quality, and secretory pattern of skin immune defenses which, in turn, vary depending on the interspecific susceptibility to diseases, pathogen virulence, and environmental toxicity [8]. Common features of these MALTs resemble those of mammals and include the following: (i) a copious mucus layer that actively barriers pathogen adherence and agglutinates [9]; (ii) secreted antimicrobial proteins (such as lysozyme, lectins, complement proteins, histones, and defensins), antibodies (igm and igt/z isotypes), immune mediators (cytokines and chemokines), and enzymatic disruptors (mainly proteases, peroxidases, and phosphatases); and (iii) interposed myeloid and lymphoid immune cells (including mast cells, dendritic-like cells, macrophages, neutrophils, and B and T lymphocyte families), natural killer cells (NK/ NCC-like), epithelial phagocytic cells, and immune-associated cells such as thrombocytes and erythrocytes [6, 8, 10,11,12]
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