Intermittent administration of peracetic acid is a mild environmental stressor that elicits mucosal and systemic adaptive responses from Atlantic salmon post-smolts

Abstract

Background Fish encounter oxidative stress several times during their lifetime, and it has a pervasive influence on their health and welfare. One of the triggers of oxidative stress in fish farming is the use of oxidative disinfectants to improve rearing conditions, especially in production systems employing recirculation technology. Here we report the physiological and morphological adaptive responses of Atlantic salmon (Salmo salar L.) post-smolts to intermittent exposure to a potent oxidative agent peracetic acid (PAA). Fish reared in semi-commercial scale brackish water recirculating aquaculture system (RAS) were exposed to 1 ppm PAA every 3 days over 6 weeks. Mucosal and systemic responses were profiled before exposure, 22 and 45 days during the intermittent PAA administration. Results Oxidative stress was likely triggered as plasma antioxidant capacity increased significantly during the exposure period. Adaptive stress response to the periodic oxidant challenge was likewise demonstrated in the changes in plasma glucose and lactate levels. PAA-induced alterations in the transcription of antioxidants, cytokines, heat shock proteins and mucin genes showed a tissue-specific pattern: downregulation was observed in the gills and olfactory rosette, upregulation occurred in the skin, and no substantial changes in the liver. Further, PAA exposure resulted in histological changes in key mucosal organs (i.e. olfactory rosette, skin and gills); pathological alterations were predominant in the gills where cases of epithelial lifting, hypertrophy and clubbing were prevalent. In addition, intermittent PAA administration resulted in an apparent overproduction of mucus in the nasal mucosa. Lastly, PAA did not dramatically alter the ability of salmon to mount a physiological stress response in the presence of a secondary stressor, though some subtle interference was documented in the kinetics and magnitude of plasma cortisol and glucose response post-stress. Conclusions The present study collectively demonstrated that intermittent oxidant exposure was a mild environmental stressor that salmon could mount strong adaptive responses at systemic and mucosal levels. The results will be valuable in optimising the rearing conditions of post-smolts in RAS, especially in adopting water treatment strategies that do not considerably interfere with fish health and welfare.

Mode of Application of Peracetic Acid-Based Disinfectants has a Minimal Influence on the Antioxidant Defences and Mucosal Structures of Atlantic Salmon (Salmo salar) Parr

“…The modulation of antioxidant defence genes in the gills, skin, and olfactory organs in this study) demonstrated that PAA could be a potential environmental stressor ( Figures 1 – 3 , however, the impact collectively suggests that the risk was minimal at least in terms of the biomarkers analysed here. This corroborates a recent study of salmon smolts where PAA addition in brackish water RAS was identified as a mild environmental stressor that triggered local and systemic oxidative stress ( Osório et al, 2022 ). In earlier studies, the gills of salmon smolts were the most responsive to PAA-induced oxidative stress although we could not establish such a striking profile here.…”

“…Pulse delivery of PAA had a significant impact on gpx expression in the skin ( Figure 2 ). Such PAA-induced modulation in the skin had not been observed in earlier studies of salmon smolts ( Soleng et al, 2019 ; Osório et al, 2022 ). Our results suggest that the antioxidant function of gpx against PAA is likely influenced by the life stage of salmon; it might be crucial during the parr stage.…”

“…Therefore, exploring its application as a disinfectant in RAS must be supported by data on its health impacts on fish. Current evidence on the health effects on salmon are seen during the smolt stage ( Lazado et al, 2020a ; Lazado et al, 2021a ; Lazado et al, 2021b ; Osório et al, 2022 ). Existing work often assumes that PAA will have the same impacts on parr, but such assumptions are tenuous due to immense physiological differences between parr and smolts.…”

“…Earlier studies of salmon smolts showed that PAA could trigger oxidative stress at the systemic level ( Soleng et al, 2019 ; Lazado et al, 2020a ; Osório et al, 2022 ). This was documented either by an increase in plasmatic TAC or regulation of metabolites with known function in the antioxidant-oxidant homeostasis.…”

“…The mobilisation of antioxidants both at the systemic and mucosal levels could be both spontaneous and latent depending on the dose and mode of delivery. We previously reported that the application of PAA in brackish water salmon RAS could be a mild environmental stressor; nonetheless, the fish could mount strong adaptive responses to routine application ( Osório et al, 2022 ).…”