Modulation of gut microbiota, blood metabolites, and disease resistance by dietary β-glucan in rainbow trout (Oncorhynchus mykiss)

Abstract

Background: Prebiotics are known to have a positive impact on fish health and growth rate, and β-glucans are among the most used prebiotics on the market. In this study, rainbow trout (Oncorhynchus mykiss) were treated with a β-1,3;1,6-glucan dietary supplement (at a dose of 0 g, 1 g, 10 g, and 50 g β-glucan per kg of feed). After 6 weeks, the effect of the β-glucan was evaluated by determining the changes in the microbiota and the blood serum metabolites in the fish. The impact of β-glucan on the immune system was evaluated through a challenge experiment with the bacterial fish pathogen Yersinia ruckeri.

Results: The microbiota showed a significant change in terms of composition following β-glucan treatment, notably an increase in the relative abundance of members of the genus Aurantimicrobium, associated with a decreased abundance of the genera Carnobacterium and Deefgea. Furthermore, analysis of more than 200 metabolites revealed that the relative levels of 53 metabolites, in particular compounds related to phosphatidylcholines, were up- or downregulated in response to the dietary supplementation, this included the amino acid alanine that was significantly upregulated in the fish that had received the highest dose of β-glucan. Meanwhile, no strong effect could be detected on the resistance of the fish to the bacterial infection.

Conclusions: The present study illustrates the ability of β-glucans to modify the gut microbiota of fish, resulting in alteration of the metabolome and affecting fish health through the lipidome of rainbow trout.

Keywords: Gut microbiota; Metabolite response; Oncorhynchus mykiss; Prebiotic; β-glucan.

Fig. 1

Alpha diversity measured in Chao1. W0: Diversity for control week 0. W6: Diversity for control week 6. 0.1%: Diversity for microbiota treated with 0.1% β-glucan. 1.0%: Diversity for microbiota treated with 1.0% β-glucan. 5.0%: Diversity for microbiota treated with 5.0% β-glucan

Fig. 2

Heatmap showing the relative abundance in term of sequence reads for the 20 most abundant bacterial genera in the intestines of the fish receiving the different concentration of β-glucan and the control groups. Individual numbers on the heatmap indicate the relative abundance of each genus

Fig. 3

Redundancy analysis plot illustrating the composition of the microbiota in the intestine of the fish at week 6, constrained based on the concentration of β-glucan in the diet. Percentages in the axis indicate the percentage of the total variation explained by the treatment group; followed by the effect of this axis on the total variation between samples

Fig. 4

Heatmap showing the relative abundance of the serum’s metabolites compared to the control at week 6 (W6- 0.0% β-glucan) using pairwise Wilcoxon rank sum tests. Only samples that are significantly different from the control are shown and the colour of the square indicates the intensity of the change. A: LC samples. B: FIA samples

Fig. 5

Clearance of Y. ruckeri among experimentally infected fish shown as the prevalence of Y. ruckeri among the groups. Sampling size (n) was 10, 20, 20, 30 fish per group at 3, 14, 21, and 28 days p.i., respectively