An integrated transcriptome and microbial community analysis reveals potential mechanisms for increased immune responses when replacing silybum marianum meal with soybean meal in growing lambs
Silybum marianum meal is a by-product that remains silymarin complex and is perceived as a potential-protein source. The potential and its mechanism of silybum marianum meal as a protein supplement in ruminants were evaluated by testing the growth performance, biochemical parameters, cytokine levels...
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Frontiers Media S.A.
2023-03-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1093129/full |
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| author | Tianxi Zhang Tianxi Zhang Yanbo Ren Yanbo Ren Chao Yang Chao Yang Kefyalew Gebeyew Kefyalew Gebeyew Min Gao Zhixiong He Zhixiong He Zhiliang Tan Zhiliang Tan |
| author_facet | Tianxi Zhang Tianxi Zhang Yanbo Ren Yanbo Ren Chao Yang Chao Yang Kefyalew Gebeyew Kefyalew Gebeyew Min Gao Zhixiong He Zhixiong He Zhiliang Tan Zhiliang Tan |
| author_sort | Tianxi Zhang |
| collection | DOAJ |
| description | Silybum marianum meal is a by-product that remains silymarin complex and is perceived as a potential-protein source. The potential and its mechanism of silybum marianum meal as a protein supplement in ruminants were evaluated by testing the growth performance, biochemical parameters, cytokine levels, gut transcriptome and microbial community profiles. Forty-two male Hulunbeier growing lambs (aged about 3-month-old; averaged body weight of 21.55 kg) were randomly divided into the CON (with 10% soybean meal) and SIL groups (with 10% silybum marianum meal). There was no significant difference in growth performance, feed intakes, or serum biochemical parameters between CON and SIL. The serum levels of IL-1β, TNF-α, TGF-β, HGF, and VEGF were all increased (p < 0.05) in the SIL group as compared with the CON group. Transcriptome gene set enrichment analysis (GSEA) revealed that the core genes in the rumen from SIL group were enriched with fructose and mannose metabolism, while the core genes in the ileum were enriched for three biological process, including digestive tract development, positive regulation of MAPK cascade, and regulation of I-kappaB kinase/NF-kappaB signaling. The 16S rDNA results showed that the relative abundance of Bacteroidetes, Firmicutes, Synergistetes, and Verrucomicrobia in the rumen from SIL group was significantly higher than that in CON group (p < 0.05), whereas Proteobacteria was significantly lower than that in CON group (p < 0.05). The LEfSe analysis showed that the genera Pyramidobacter, Saccharofermentans, Anaerovibrio, Oscillibacter and Barnesiella were enriched in the rumen from SIL group, whereas Sharpea was enriched in the CON group (LDA > 2). In the ileum, there were no significant differences in the phylum-level classification of microbes observed. At the genus level, the relative abundances of Bifidobacterium and Ruminococcus in the ileum from SIL group were significantly higher than that in the CON group (p < 0.05), whereas the relative abundance of Clostridium_XI was lower (p < 0.05). Correlation analysis showed that Clostridium_XI was negatively correlated with VEGF, TGF-β, TNF-α and HGF (p < 0.05). Core genes BMP4 and CD4 were negatively correlated with Clostridium_XI (p < 0.05). Our results indicated that supplementing silybum marianum meal as a replacement for soybean meal resulted in increased cytokines production without affecting growth performance in growing lambs, and the enrichment of immune-related genes and altered microbial community in the ileum were contributed to the increased immune responses. |
| first_indexed | 2024-04-10T06:16:10Z |
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| last_indexed | 2024-04-10T06:16:10Z |
| publishDate | 2023-03-01 |
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| spelling | doaj.art-6647f1c2d9ff49039105d0cc9e89fcff2023-03-02T07:08:42ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-03-011410.3389/fmicb.2023.10931291093129An integrated transcriptome and microbial community analysis reveals potential mechanisms for increased immune responses when replacing silybum marianum meal with soybean meal in growing lambsTianxi Zhang0Tianxi Zhang1Yanbo Ren2Yanbo Ren3Chao Yang4Chao Yang5Kefyalew Gebeyew6Kefyalew Gebeyew7Min Gao8Zhixiong He9Zhixiong He10Zhiliang Tan11Zhiliang Tan12CAS Key Laboratory for Agro-Ecological Processes in Subtropical Region, National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Hunan Provincial Key Laboratory of Animal Nutritional Physiology and Metabolic Process, Institute of Subtropical Agriculture, The Chinese Academy of Sciences, Changsha, ChinaUniversity of Chinese Academy of Science, Beijing, ChinaCAS Key Laboratory for Agro-Ecological Processes in Subtropical Region, National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Hunan Provincial Key Laboratory of Animal Nutritional Physiology and Metabolic Process, Institute of Subtropical Agriculture, The Chinese Academy of Sciences, Changsha, ChinaSchool of Animal Science, Inner Mongolia Agricultural University, Hohhot, ChinaCAS Key Laboratory for Agro-Ecological Processes in Subtropical Region, National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Hunan Provincial Key Laboratory of Animal Nutritional Physiology and Metabolic Process, Institute of Subtropical Agriculture, The Chinese Academy of Sciences, Changsha, ChinaUniversity of Chinese Academy of Science, Beijing, ChinaCAS Key Laboratory for Agro-Ecological Processes in Subtropical Region, National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Hunan Provincial Key Laboratory of Animal Nutritional Physiology and Metabolic Process, Institute of Subtropical Agriculture, The Chinese Academy of Sciences, Changsha, ChinaUniversity of Chinese Academy of Science, Beijing, ChinaInner Mongolia Academy of Agricultural and Animal Husbandry Sciences, Hohhot, ChinaCAS Key Laboratory for Agro-Ecological Processes in Subtropical Region, National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Hunan Provincial Key Laboratory of Animal Nutritional Physiology and Metabolic Process, Institute of Subtropical Agriculture, The Chinese Academy of Sciences, Changsha, ChinaUniversity of Chinese Academy of Science, Beijing, ChinaCAS Key Laboratory for Agro-Ecological Processes in Subtropical Region, National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Hunan Provincial Key Laboratory of Animal Nutritional Physiology and Metabolic Process, Institute of Subtropical Agriculture, The Chinese Academy of Sciences, Changsha, ChinaUniversity of Chinese Academy of Science, Beijing, ChinaSilybum marianum meal is a by-product that remains silymarin complex and is perceived as a potential-protein source. The potential and its mechanism of silybum marianum meal as a protein supplement in ruminants were evaluated by testing the growth performance, biochemical parameters, cytokine levels, gut transcriptome and microbial community profiles. Forty-two male Hulunbeier growing lambs (aged about 3-month-old; averaged body weight of 21.55 kg) were randomly divided into the CON (with 10% soybean meal) and SIL groups (with 10% silybum marianum meal). There was no significant difference in growth performance, feed intakes, or serum biochemical parameters between CON and SIL. The serum levels of IL-1β, TNF-α, TGF-β, HGF, and VEGF were all increased (p < 0.05) in the SIL group as compared with the CON group. Transcriptome gene set enrichment analysis (GSEA) revealed that the core genes in the rumen from SIL group were enriched with fructose and mannose metabolism, while the core genes in the ileum were enriched for three biological process, including digestive tract development, positive regulation of MAPK cascade, and regulation of I-kappaB kinase/NF-kappaB signaling. The 16S rDNA results showed that the relative abundance of Bacteroidetes, Firmicutes, Synergistetes, and Verrucomicrobia in the rumen from SIL group was significantly higher than that in CON group (p < 0.05), whereas Proteobacteria was significantly lower than that in CON group (p < 0.05). The LEfSe analysis showed that the genera Pyramidobacter, Saccharofermentans, Anaerovibrio, Oscillibacter and Barnesiella were enriched in the rumen from SIL group, whereas Sharpea was enriched in the CON group (LDA > 2). In the ileum, there were no significant differences in the phylum-level classification of microbes observed. At the genus level, the relative abundances of Bifidobacterium and Ruminococcus in the ileum from SIL group were significantly higher than that in the CON group (p < 0.05), whereas the relative abundance of Clostridium_XI was lower (p < 0.05). Correlation analysis showed that Clostridium_XI was negatively correlated with VEGF, TGF-β, TNF-α and HGF (p < 0.05). Core genes BMP4 and CD4 were negatively correlated with Clostridium_XI (p < 0.05). Our results indicated that supplementing silybum marianum meal as a replacement for soybean meal resulted in increased cytokines production without affecting growth performance in growing lambs, and the enrichment of immune-related genes and altered microbial community in the ileum were contributed to the increased immune responses.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1093129/fullsilybum marianum mealsoybean meallambscytokinesmicrobial communitytranscriptome |
| spellingShingle | Tianxi Zhang Tianxi Zhang Yanbo Ren Yanbo Ren Chao Yang Chao Yang Kefyalew Gebeyew Kefyalew Gebeyew Min Gao Zhixiong He Zhixiong He Zhiliang Tan Zhiliang Tan An integrated transcriptome and microbial community analysis reveals potential mechanisms for increased immune responses when replacing silybum marianum meal with soybean meal in growing lambs Frontiers in Microbiology silybum marianum meal soybean meal lambs cytokines microbial community transcriptome |
| title | An integrated transcriptome and microbial community analysis reveals potential mechanisms for increased immune responses when replacing silybum marianum meal with soybean meal in growing lambs |
| title_full | An integrated transcriptome and microbial community analysis reveals potential mechanisms for increased immune responses when replacing silybum marianum meal with soybean meal in growing lambs |
| title_fullStr | An integrated transcriptome and microbial community analysis reveals potential mechanisms for increased immune responses when replacing silybum marianum meal with soybean meal in growing lambs |
| title_full_unstemmed | An integrated transcriptome and microbial community analysis reveals potential mechanisms for increased immune responses when replacing silybum marianum meal with soybean meal in growing lambs |
| title_short | An integrated transcriptome and microbial community analysis reveals potential mechanisms for increased immune responses when replacing silybum marianum meal with soybean meal in growing lambs |
| title_sort | integrated transcriptome and microbial community analysis reveals potential mechanisms for increased immune responses when replacing silybum marianum meal with soybean meal in growing lambs |
| topic | silybum marianum meal soybean meal lambs cytokines microbial community transcriptome |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1093129/full |
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