Oxidant-induced modifications in the mucosal transcriptome and circulating metabolome of Atlantic salmon
Carlo C Lazado1, Lars-Flemming Pedersen2, Katrine H Kirste1
1Nofima, Norwegian Institute of Food Fisheries and Aquaculture Research, 1433, Ås, Norway.
Abstract:
Here we report the molecular networks associated with the mucosal and systemic responses to peracetic acid (PAA), a candidate oxidative chemotherapeutic in Atlantic salmon (Salmo salar). Smolts were exposed to different therapeutic doses (0, 0.6 and 2.4 mg/L) of PAA for 5 min, followed by a re-exposure to the same concentrations for 30 min 2 weeks later. PAA-exposed groups have higher external welfare score alterations, especially 2 weeks after the re-exposure. Cases of fin damage and scale loss were prevalent in the PAA-exposed groups. Transcriptomic profiling of mucosal tissues revealed that the skin had 12.5 % more differentially regulated genes (DEGs) than the gills following PAA exposure. The largest cluster of DEGs, both in the skin and gills, were involved in tissue extracellular matrix and metabolism. There were 22 DEGs common to both mucosal tissues, which were represented primarily by genes involved in the biophysical integrity of the mucosal barrier, including cadherin, collagen I α 2 chain, mucin-2 and spondin 1a. The absence of significant clustering in the plasma metabolomes amongst the three treatment groups indicates that PAA treatment did not induce any global metabolomic disturbances. Nonetheless, five metabolites with known functions during oxidative stress were remarkably affected by PAA treatments such as citrulline, histidine, tryptophan, methionine and trans-4-hydroxyproline. Collectively, these results indicate that salmon were able to mount mucosal and systemic adaptive responses to therapeutic doses of PAA and that the molecules identified are potential markers for assessing the health and welfare consequences of oxidant exposure.
Insights
Atlantic salmon exposed to peracetic acid (PAA) showed adaptive mucosal and systemic responses. Identified genes and metabolites may serve as biomarkers for oxidant exposure and welfare in fish health management.
Area of Science:
- Aquatic animal health
- Fish immunology
- Oxidative stress research
Background:
- Peracetic acid (PAA) is an oxidative chemotherapeutic agent used in aquaculture.
- Understanding PAA's molecular effects on fish is crucial for optimizing its therapeutic application and ensuring fish welfare.
- Atlantic salmon (Salmo salar) are a key species in aquaculture, making them a relevant model for studying chemotherapeutic responses.
Purpose of the Study:
- To investigate the molecular networks associated with mucosal and systemic responses to PAA in Atlantic salmon.
- To identify potential biomarkers for assessing the health and welfare impacts of PAA exposure.
- To evaluate the adaptive capacity of salmon to therapeutic doses of PAA.
Main Methods:
- Atlantic salmon smolts were exposed to varying therapeutic doses of PAA (0, 0.6, 2.4 mg/L).
- Transcriptomic profiling of skin and gill tissues was performed to identify differentially expressed genes (DEGs).
- Plasma metabolomic analysis was conducted to assess systemic metabolic changes.
Main Results:
- PAA exposure led to increased external welfare score alterations, fin damage, and scale loss.
- Skin tissue exhibited a higher percentage of DEGs compared to gills, with major clusters related to extracellular matrix and metabolism.
- Common DEGs in mucosal tissues were linked to mucosal barrier integrity, while plasma metabolomics revealed specific metabolite alterations related to oxidative stress.
Conclusions:
- Atlantic salmon demonstrate adaptive mucosal and systemic responses to therapeutic PAA doses.
- Specific genes and metabolites are identified as potential indicators of PAA-induced stress and welfare changes.
- The findings provide molecular insights into salmon's resilience to oxidative chemotherapeutics.
