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. 2022 Aug 30;11(9):1708.
doi: 10.3390/antiox11091708.

Impact of Antioxidant Feed and Growth Manipulation on the Redox Regulation of Atlantic Salmon Smolts

Peng Yin  1   2 , Björn Thrandur Björnsson  3 , Per Gunnar Fjelldal  4 , Takaya Saito  1 , Sofie Charlotte Remø  1 , Rolf Brudvik Edvardsen  1 , Tom Hansen  4 , Sandeep Sharma  5 , Rolf Erik Olsen  6 , Kristin Hamre  1
Affiliations

Impact of Antioxidant Feed and Growth Manipulation on the Redox Regulation of Atlantic Salmon Smolts

Peng Yin et al. Antioxidants (Basel). .

Abstract

Accumulating evidence indicates a close relationship between oxidative stress and growth rate in fish. However, the underlying mechanisms of this relationship remain unclear. This study evaluated the combined effect of dietary antioxidants and growth hormone (GH) on the liver and the muscle redox status of Atlantic salmon. There were two sequential experimental phases (EP) termed EP1 and EP2, each lasting for 6 weeks. In EP1, Atlantic salmon were fed either low-(L, 230 mg/kg ascorbic acid (Asc), 120 mg/kg α-tocopherol (α-TOH)), or high-(H, 380 mg/kg Asc, 210 mg/kg α-TOH)vitamin diets. The vitamins were supplemented as stable forms and the feeding was continued in EP2. In EP2, half of the fish were implanted with 3 μL per g body weight of recombinant bovine GH (Posilac®, 1 mg rbGH g BW-1) suspended in sesame oil, while the other half were held in different tanks and sham-implanted with similar volumes of the sesame oil vehicle. Here, we show that increasing high levels of vitamin C and E (diet H) increased their content in muscle and liver during EP1. GH implantation decreased vitamin C and E levels in both liver and muscle but increased malondialdehyde (MDA) levels only in the liver. GH also affected many genes and pathways of antioxidant enzymes and the redox balance. Among the most consistent were the upregulation of genes coding for the NADPH oxidase family (NOXs) and downregulation of the oxidative stress response transcription factor, nuclear factor-erythroid 2-related factor 2 (nrf2), and its downstream target genes in the liver. We verified that GH increases the growth rate until the end of the trail and induces an oxidative effect in the liver and muscle of Atlantic salmon. Dietary antioxidants do lower oxidative stress but have no effect on the growth rate. The present study is intended as a starting point to understand the potential interactions between growth and redox signaling in fish.

Keywords: antioxidant nutrients; fish; growth hormone; oxidative stress; redox; transcriptional regulation.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
General flow chart of the experimental design of Atlantic salmon during EP1 and EP2.
Figure 2
Figure 2
Specific growth rate in Atlantic salmon in response to dietary vitamins and growth hormone (GH) implantation or sham implantation over EP1 and EP2. The specific growth rate is calculated over the EP1 from 0 to 42 days, EP2 from 42 to 60 days as well as 61 to 86 days. Data presented as means ± SD. p-values obtained from two-way ANOVA on the main effects of diet, GH, and interaction are provided in insets. * Significant effect of treatment (p < 0.05, two-way ANOVA).
Figure 3
Figure 3
Cataract score, lens histidine, and lens N-acetyl L-histidine (NAH) in Atlantic salmon. Cataract score was only detected in the EP2. Data presented as means ± SD. p-values obtained from two-way ANOVA on the main effects of diet, GH, and interaction are provided in insets. **; significant effect of treatment (p < 0.01, two-way ANOVA).
Figure 4
Figure 4
Tissue concentrations (mg kg−1 wet weight) of redox-dependent micronutrients in Atlantic salmon in response to dietary vitamins and GH implantation or sham implantation over EP1 and EP2. Data presented as means ± SD. P-values obtained from two-way ANOVA on the main effects of diet, GH, and interaction are provided in insets. *, **, ***; significant effect of treatment (p < 0.05, p < 0.01, p < 0.001, two-way ANOVA). Small letters are the result of post-hoc after significant interaction (two-way ANOVA with Tukey HSD post-hoc).
Figure 5
Figure 5
Tissues reduced and oxidized glutathione (GSH and GSSG, μmoles kg−1 wet weight) and the GSH-based redox potential (mV) in Atlantic salmon in response to dietary vitamins and GH implantation or sham implantation over EP1 and EP2. Data presented as means ± SD. p-values obtained from two-way ANOVA on the main effects of diet, GH, and interaction are provided in insets. **; significant effect of treatment (p < 0.01, two-way ANOVA).
Figure 6
Figure 6
Changes in specific antioxidant enzyme activity in response to dietary vitamins and GH implantation or shame implantation over EP1 and EP2. Data presented as means ± SD. P-values obtained from two-way ANOVA on the main effects of diet, GH, and interaction are provided in insets. *, **, ***; significant effect of treatment (p ≤ 0.05, p ≤ 0.01, p ≤ 0.001, two-way ANOVA). Different l letters denote significant effect between groups in the EP1, small letters are the result of post-hoc after significant interactions (two-way ANOVA with Tukey HSD post-hoc) in the EP2.
Figure 7
Figure 7
PCA biplots on specific antioxidant enzyme activity grouped by GH (A,B) or dietary vitamins C and E feeding (C,D) measured in liver and muscle, respectively. Arrows represent the 5 most contributing variables to the model, respectively (Cat, catalase; Sod, superoxide dismutase; Gst, glutathione S-transferase; Gpx, total glutathione peroxidase). Ellipses represent the 95% confidence intervals around a center of 9 rearing tanks (pool of 3 individuals).
Figure 8
Figure 8
Expression of genes involved in redox system affected by dietary vitamins and GH implantation. Heat map of the expression of genes associated with the redox system over EP1 and EP2. Normalization genes was performed using size factors calculated by DESeq2, followed by log2 fold-change (LFC) and adjusted p-value estimates between sample group; red and blue indicate upregulated and downregulated expression, respectively, while the symbol *, •, and ⸰ indicate p-values lower than 0.001, 0.01, and 0.1, respectively.
Figure 9
Figure 9
Effect of GH and vitamin C and E nutrition on the redox system in liver (A) and muscle (B) of Atlantic salmon during the EP2. The systemic overview of redox regulation was raised based on the results in this study. Arrows in blue color represent the regulation of antioxidants by GH, in pink color represent the regulation of antioxidants by dietary vitamin C and E. Arrows in red and green color represent the regulation of redox relative gene expression of the comparisons of L-GH vs. L-Sham and H-GH vs. H-Sham, respectively.
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