Crowding reshapes the mucosal but not the systemic response repertoires of Atlantic salmon to peracetic acid

Abstract

Knowledge of the impact of aquaculture chemotherapeutants on fish physiology is scarce. This is particularly relevant for peracetic acid (PAA), a widely used oxidative disinfectant in aquaculture. The chemical behaviour in water is well studied but knowledge about the physiological consequences for fish is limited. The present study investigated the transcriptomics, morphology, and physiology of Atlantic salmon (Salmo salar) responses to PAA and explored how crowding prior to exposure influenced these responses. Post-smolts were subjected to crowding by reducing the water volume thereby increasing the density for 1 h before they were exposed to 4.8 ppm PAA for 30 minutes. The exposed fish were allowed to recover for 2 weeks (w), with samplings carried out at 4 h and 2 w postexposure (p.e.). There were four treatment groups in total: no crowding/control; no crowding/PAA; crowding/control; and crowding/PAA. The physiological changes were documented at the mucosal (i.e., skin and gills) and systemic (i.e., plasma) levels. The overall external welfare score was in good status in all experimental groups. The treatments did not dramatically affect the number of mucous cells in both the skin and the gills. Branchial histomorphology was in a fairly good condition, despite the increased occurrence of epithelial lifting in the crowded groups at 2 w p.e. The gill transcriptome was affected by crowding, PAA, and their combinations more than the skin, as manifested by the number of differentially expressed genes (DEG) in the former. In general, individual stimuli and their combinations elicited strong transcriptional responses in the gills at 4 h p.e. and a marked recovery was observed 2 w thereafter. Crowding altered the dynamics of transcriptional response to PAA especially at 4 h p.e. and the two mucosal tissues demonstrated a contrasting profilea higher number of DEGs in the gills without crowding history, while higher skin DEGs were observed in the group subjected to crowding prior to exposure. Plasma metabolomics identified 639 compounds, and the metabolomic changes were affected mainly by crowding and sampling time, and not by PAA exposure. The results revealed the ability of salmon to mobilise physiological countermeasures to PAA exposure that were differentially influenced by crowding, and that such an effect was remarkably exhibited at the mucosa rather than in the circulating metabolome.

Oxidative Chemical Stressors Alter the Physiological State of the Nasal Olfactory Mucosa of Atlantic Salmon

“…Besides the activation of several effector molecules that provide an interconnected response to oxidant-triggered oxidative stress, it is compelling to observe that several genes for molecules for cytostructural and extracellular matrix were represented in the list of upregulated genes. Previous studies using this oxidant found histostructural changes, though minimal, in the gill and skin mucosa [4,27,42]. We can speculate that the upregulation observed here may play a role in maintaining the structural integrity and barrier functionality under oxidative challenge.…”

“…Thereafter, the oxidant (Divosan Forte™, Lilleborg AS, Olso, Norway) was added to the water column to achieve a final concentration of 10 ppm. This concentration was 2x higher than the concentration we earlier tested and reported [4]. Aeration was supplied to enable mixing and to maintain the oxygen level.…”

“…This mode of application was patterned on a previous PAA experiment conducted in rainbow trout, a closely related species of salmon [ 26 ]. Moreover, the concentration is within the range safe for use in salmon [ 4 , 28 ]. It was ensured that the application of PAA on each occasion was between 0900 and 1000 to avoid temporal effects.…”

“…The integrated antioxidant systems, which include enzymatic and nonenzymatic antioxidants, are at the forefront of blocking the harmful effects of ROS [ 1 ]. Redox imbalance associated with oxidative stress promotes genetic instability, changes in gene expression patterns, alterations in cellular signalling cascades/cell metabolism, and disruption of the cell cycle, leading to several pathophysiological conditions [ 4 , 5 ].…”

“…We employed both in vivo and in vitro strategies to unravel the molecular changes in the nasal olfactory mucosa when challenged with exogenous oxidants relevant in fish farming. In this study, we employed peracetic acid (PAA) as the main oxidant, as it is currently being developed as a chemotherapeutant (i.e., for amoebic gill disease—AGD) and disinfectant in recirculating aquaculture systems for salmon [ 4 , 26 ], and the results here are expected to help underline its potential for use. Both in vivo trials were designed to simulate the prospective use of PAA as either a routine disinfectant (Trial 1) or a treatment for a parasitic infection (Trial 2).…”