Dataset Information

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.

SUBMITTER: Menanteau-Ledouble S

PROVIDER: S-EPMC9677660 | biostudies-literature | 2022 Nov

REPOSITORIES: biostudies-literature

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Publications

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

Menanteau-Ledouble Simon S Skov Jakob J Lukassen Mie Bech MB Rolle-Kampczyk Ulrike U Haange Sven-Bastiaan SB Dalsgaard Inger I von Bergen Martin M Nielsen Jeppe Lund JL

Animal microbiome 20221120 1

<h4>Background</h4>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-gluc ...[more]

PMID: 36404315

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Project description:Emerging evidence confirms using probiotics in promoting growth and immunity of farmed fish. However, the molecular mechanisms underlying the host-microbiome interactions mediated by probiotics are not fully understood. In this study, we used rainbow trout (Oncorhynchus mykiss) as a model to investigate the internal mechanisms of host-microbiome interactions influenced by two probiotic bacteria, Bacillus velezensis and Lactobacillus sakei. We carried out experiments, including intestinal histology, serum physiology, and transcriptome and combined intestinal microbiome and metabolite profiling. Our results showed that both probiotics had a positive effect on growth, immunity, serum enzyme activity, the gut microbiome, and resistance to Aeromonas salmonicida in rainbow trout. Moreover, the intestinal microbial structure was reshaped with increased relative abundance of potential beneficial bacteria, such as Ruminococcus, Lachnospiraceae ucg-004, Leptotrichia, Bacillus coagulans, Porphyromonadaceae, Anaerococcus, and Photobacterium in the B. velezensis group and Paenibacillaceae and Eubacterium hallii in the L. sakei group. Metabolomic profiling and transcriptome analysis revealed upregulated metabolites as biomarkers, i.e., sucrose and l-malic acid in the B. velezensis group, and N-acetyl-l-phenylalanine, N-acetylneuraminic acid, and hydroxyproline in the L. sakei group. Additionally, a multiomics combined analysis illustrated significant positive correlations between the relative abundance of microflora, metabolites, and gene expression associated with immunity and growth. This study highlights the significant role of probiotics as effectors of intestinal microbial activity and shows that different probiotics can have a species-specific effect on the physiological regulation of the host. These findings contribute to a better understanding of the complex host-microbiome interactions in rainbow trout and may have implications for the use of probiotics in aquaculture. IMPORTANCE Probiotics are kinds of beneficial live microbes that impart beneficial effects on the host. Recent studies have proven that when given supplementation with probiotics, farmed fish showed improved disease prevention and growth promotion. However, the underlying metabolic functions regarding their involvement in regulating growth phenotypes, nutrient utilization, and immune response are not yet well understood in the aquaculture field. Given the active interactions between the gut microbiota and fish immune and growth performance, we conducted the supplementation experiments with the probiotics Bacillus velezensis and Lactobacillus sakei. The results showed that probiotics mediated intestinal microbiome- and microbiota-derived metabolites regulating the growth and immunity of fish, and different probiotics participated in the species-specific physiological regulation of the host. This study contributed to a better understanding of the functional interactions associated with host health and gut microbiota species.

Project description:BACKGROUND:Diverse microbial communities colonizing the intestine of fish contribute to their growth, digestion, nutrition, and immune function. We hypothesized that fecal samples representing the gut microbiota of rainbow trout could be associated with differential growth rates observed in fish breeding programs. If true, harnessing the functionality of this microbiota can improve the profitability of aquaculture. The first objective of this study was to test this hypothesis if gut microbiota is associated with fish growth rate (body weight). Four full-sibling families were stocked in the same tank and fed an identical diet. Two fast-growing and two slow-growing fish were selected from each family for 16S rRNA microbiota profiling. Microbiota diversity varies with different DNA extraction methods. The second objective of this study was to compare the effects of five commonly used DNA extraction methods on the microbiota profiling and to determine the most appropriate extraction method for this study. These methods were Promega-Maxwell, Phenol-chloroform, MO-BIO, Qiagen-Blood/Tissue, and Qiagen-Stool. Methods were compared according to DNA integrity, cost, feasibility and inter-sample variation based on non-metric multidimensional scaling ordination (nMDS) clusters. RESULTS:Differences in DNA extraction methods resulted in significant variation in the identification of bacteria that compose the gut microbiota. Promega-Maxwell had the lowest inter-sample variation and was therefore used for the subsequent analyses. Beta diversity of the bacterial communities showed significant variation between breeding families but not between the fast- and slow-growing fish. However, an indicator analysis determined that cellulose, amylose degrading and amino acid fermenting bacteria (Clostridium, Leptotrichia, and Peptostreptococcus) are indicator taxa of the fast-growing fish. In contrary, pathogenic bacteria (Corynebacterium and Paeniclostridium) were identified as indicator taxa for the slow-growing fish. CONCLUSION:DNA extraction methodology should be carefully considered for accurate profiling of the gut microbiota. Although the microbiota was not significantly different between the fast- and slow-growing fish groups, some bacterial taxa with functional implications were indicative of fish growth rate. Further studies are warranted to explore how bacteria are transmitted and potential usage of the indicator bacteria of fast-growing fish for development of probiotics that may improve fish health and growth.

Dataset Information

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

Background

Results

Conclusions

Publications

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

Similar Datasets

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