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. 2023 Sep 6:14:1254569.
doi: 10.3389/fmicb.2023.1254569. eCollection 2023.

Genetic assessment of the effect of red yeast (Sporidiobolus pararoseus) as a feed additive on mycotoxin toxicity in laying hens

Shahrbanou Hosseini  1   2 , Bertram Brenig  1   2 , Sunattinee Winitchakorn  3 , Chanidapha Kanmanee  3 , Orranee Srinual  3   4 , Wanaporn Tapingkae  3   4 , Kesinee Gatphayak  3   4
Affiliations

Genetic assessment of the effect of red yeast (Sporidiobolus pararoseus) as a feed additive on mycotoxin toxicity in laying hens

Shahrbanou Hosseini et al. Front Microbiol. .

Abstract

Toxic fungal species produce hazardous substances known as mycotoxins. Consumption of mycotoxin contaminated feed and food causes a variety of dangerous diseases and can even lead to death of animals and humans, raising global concerns for adverse health effects. To date, several strategies have been developed to counteract with mycotoxin contamination. Red yeast as a novel biological dietary agent is a promising strategy to eliminate mycotoxicity in living organisms. Poultry are most susceptible animals to mycotoxin contamination, as they are fed a mixture of grains and are at higher risk of co-exposure to multiple toxic fungal substances. Therefore, this study investigated the genetic mechanism underlying long-term feeding with red yeast supplementation in interaction with multiple mycotoxins using transcriptome profiling (RNA_Seq) in the liver of laying hens. The results showed a high number of significantly differentially expressed genes in liver of chicken fed with a diet contaminated with mycotoxins, whereas the number of Significantly expressed genes was considerably reduced when the diet was supplemented with red yeast. The expression of genes involved in the phase I (CYP1A1, CYP1A2) and phase II (GSTA2, GSTA3, MGST1) detoxification process was downregulated in animals fed with mycotoxins contaminated diet, indicating suppression of the detoxification mechanisms. However, genes involved in antioxidant defense (GSTO1), apoptosis process (DUSP8), and tumor suppressor (KIAA1324, FBXO47, NME6) were upregulated in mycotoxins-exposed animals, suggesting activation of the antioxidant defense in response to mycotoxicity. Similarly, none of the detoxification genes were upregulated in hens fed with red yeast supplemented diet. However, neither genes involved in antioxidant defense nor tumor suppressor genes were expressed in the animals exposed to the red yeast supplemented feed, suggesting decreases the adsorption of biologically active mycotoxins in the liver of laying hens. We conclude that red yeast can act as a mycotoxin binder to decrease the adsorption of mycotoxins in the liver of laying hens and can be used as an effective strategy in the poultry feed industry to eliminate the adverse effects of mycotoxins for animals and increase food safety for human consumers.

Keywords: RNA sequencing; detoxification; feed additive; gene expression; laying hens; mycotoxin; red yeast.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Overall distribution of differentially expressed genes (DEGs) in the liver of laying hens. The volcano plots illustrate significant DEGs in different experimental groups: (A) red yeast versus control (RY vs. CON), (B) mycotoxins versus control (MT vs. CON), (C) red yeast + mycotoxins versus control (RY + MT vs. CON). Each dot in the plots represent a gene with its corresponding log2 (fold change) on the x-axis and -log10 p-value on the y-axis. The significant expression differences are shown at the significant threshold (padj < 0.05).
Figure 2
Figure 2
Venn diagram of significantly differentially expressed genes. The Venn diagram shows the number of uniquely expressed genes (upregulated↑ and downregulated↓) comparing mycotoxins versus control (MT vs. CON) and red yeast + mycotoxins versus control (RY + MT vs. CON) groups, with the overlapping region illustrating the number of genes co-expressed in both experimental groups.
Figure 3
Figure 3
Top significantly differentially expressed genes (DEGs). The radar plots represent the top significantly upregulated and downregulated genes (padj < 0.01, −2 < log2 fold change >2) in different experimental groups: (A) mycotoxins versus control (MT vs. CON), (B) in both mycotoxins versus control (MT vs. CON) and red yeast + mycotoxins versus control (RY + MT vs. CON) groups (common genes), (C) red yeast + mycotoxins versus control (RY + MT vs. CON). The identified candidate genes expressed at the top significant level are marked with an asterisk (*) in the figure.
Figure 4
Figure 4
Differential expression of candidate genes. The bar charts illustrate upregulation and downregulation of candidate genes involved in mycotoxin toxicity at the significant threshold (padj < 0.05) in different experimental groups: (A) uniquely expressed candidate genes in mycotoxins versus control (MT vs. CON), (B) common candidate genes expressed in both mycotoxins versus control (MT vs. CON) and in red yeast + mycotoxins versus control (RY + MT vs. CON), (C) uniquely expressed candidate genes in red yeast + mycotoxins versus control (RY + MT vs. CON). The x-axis represents the differences in mean fold change (log2) per gene.
Figure 5
Figure 5
Significantly enriched terms in gene ontology (GO) analysis. The bar charts illustrate the annotation of GO categories in biological process in mycotoxins versus control (MT vs. CON) and in red yeast + mycotoxins versus control (RY + MT vs. CON). The vertical axis represents the top 20 significant enriched GOs (padj < 0.05) and the horizontal axis represents the number of genes in each GO term. The second horizontal axis indicates the significant level of each GO term -log10 (padj < 0.05).
Figure 6
Figure 6
Significantly enriched pathways in the KEGG pathway analysis. The scatter plot illustrates the significantly enriched pathways (padj < 0.05) in mycotoxins versus control (MT vs. CON) group. The vertical axis represents the enriched pathway categories and the horizontal axis represents the gene ratio (the ratio of differentially expressed genes enriched in each pathway to the total number of genes in the pathway). The size and colour of dots indicate gene number and the range of padj-value, respectively. The enriched detoxification and lipid metabolism pathways are marked with an asterisk (*) in the scatter plot and their significantly up- and down-regulated genes are represented in the figure.
Figure 7
Figure 7
Significantly enriched pathways in the KEGG pathway analysis. The scatter plot illustrates the significantly enriched pathways (padj < 0.05) in red yeast + mycotoxins versus control (RY + MT vs. CON) group. The vertical axis represents the enriched pathway categories and the horizontal axis represents the gene ratio (the ratio of differentially expressed genes enriched in each pathway to the total number of genes in the pathway). The size and colour of dots indicate gene number and the range of padj-value, respectively. The enriched lipid metabolism and essential amino acids related pathways are marked with an asterisk (*) in the scatter plot and their significantly up-and down-regulated genes are represented in the figure.
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