Oregano Essential Oils Mediated Intestinal Microbiota and Metabolites and Improved Growth Performance and Intestinal Barrier Function in Sheep
With the increased demand for safe and sustainable alternatives to growth promoting antibiotics in the livestock industry, oregano essential oils (OEO) and Lactobacillus reuteri (LR) have been examined as alternatives to antibiotics for growth promotion and to improve animal health and performance....
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-07-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2022.908015/full |
| _version_ | 1811224619826282496 |
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| author | Li Jia Jianping Wu Yu Lei Fanyun Kong Rui Zhang Jianxiang Sun Liao Wang Zemin Li Jinping Shi Ying Wang Yubing Wei Ke Zhang Zhaomin Lei |
| author_facet | Li Jia Jianping Wu Yu Lei Fanyun Kong Rui Zhang Jianxiang Sun Liao Wang Zemin Li Jinping Shi Ying Wang Yubing Wei Ke Zhang Zhaomin Lei |
| author_sort | Li Jia |
| collection | DOAJ |
| description | With the increased demand for safe and sustainable alternatives to growth promoting antibiotics in the livestock industry, oregano essential oils (OEO) and Lactobacillus reuteri (LR) have been examined as alternatives to antibiotics for growth promotion and to improve animal health and performance. However, the mechanism underlying the OEO and LR mediation of sheep growth remains unknown. In this study, 16S rRNA gene sequencing and untargeted metabolomics were used to determine the role of the gut microbiota in the growth improvements observed. The potential modulating roles of intestinal microbial metabolites of OEO and LR to intestinal health were systematically explored as well. It was observed that both OEO and LR had greater average daily gain (ADG) and lower F/G ratio. Furthermore, OEO also appeared to have produced a greater amylase enzyme activity and mucin gene expression in the jejunal mucosa. It was also observed that OEO reduced serum IL-2 and TNF-β as well as mRNA levels of NF-κB p65, toll-like receptor-4 (TLR-4), and IL-6 in the jejunal mucosa. Moreover, dietary OEO supplementation increased the abundances of Ruminococcus, Bifidobacterium and Enterococcus, while the relative abundances of Succiniclasticum, Marvinbryantia and Streptococcus were enriched in LR group. Spearman’s correlation analysis revealed that the abundances of Bifidobacterium, Ruminococcus and Enterococcus were positively correlated with the mRNA expression of mucins. Moreover, the relative abundance of Enterococcus was positively correlated with amylase activity. Metabolomics analysis indicated that OEO and LR increased the levels of indole acetaldehyde and indole-3-acetic acid through the tryptophan metabolism pathway. It was observed that LR also decreased the inflammatory metabolites including tryptamine and 5-hydroxyindole-3-acetic acid. Collectively, these results suggested that OEO exerted a beneficial effect on growth performance and the mucosal barrier, affected tryptophan metabolism and improved the intestinal microbiota of sheep. |
| first_indexed | 2024-04-12T08:50:59Z |
| format | Article |
| id | doaj.art-c8dd9547f3214422b444063f056982fa |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-04-12T08:50:59Z |
| publishDate | 2022-07-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-c8dd9547f3214422b444063f056982fa2022-12-22T03:39:34ZengFrontiers Media S.A.Frontiers in Immunology1664-32242022-07-011310.3389/fimmu.2022.908015908015Oregano Essential Oils Mediated Intestinal Microbiota and Metabolites and Improved Growth Performance and Intestinal Barrier Function in SheepLi Jia0Jianping Wu1Yu Lei2Fanyun Kong3Rui Zhang4Jianxiang Sun5Liao Wang6Zemin Li7Jinping Shi8Ying Wang9Yubing Wei10Ke Zhang11Zhaomin Lei12College of Animal Science and Technology, Gansu Agricultural University, Lanzhou, ChinaInstitute of Rural Development, Northwest Normal University, Lanzhou, ChinaKey Laboratory of Animal Genetics, Breeding and Reproduction of Shanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, ChinaCollege of Animal Science and Technology, Gansu Agricultural University, Lanzhou, ChinaCollege of Animal Science and Technology, Gansu Agricultural University, Lanzhou, ChinaCollege of Animal Science and Technology, Gansu Agricultural University, Lanzhou, ChinaCollege of Animal Science and Technology, Gansu Agricultural University, Lanzhou, ChinaCollege of Animal Science and Technology, Gansu Agricultural University, Lanzhou, ChinaCollege of Animal Science and Technology, Gansu Agricultural University, Lanzhou, ChinaCollege of Animal Science and Technology, Gansu Agricultural University, Lanzhou, ChinaThe Animal Husbandry and Veterinary Station in Pingshan Lake Mongolian Township of Ganzhou District, Zhangye, ChinaKey Laboratory of Animal Genetics, Breeding and Reproduction of Shanxi Province, College of Animal Science and Technology, Northwest A&F University, Yangling, ChinaCollege of Animal Science and Technology, Gansu Agricultural University, Lanzhou, ChinaWith the increased demand for safe and sustainable alternatives to growth promoting antibiotics in the livestock industry, oregano essential oils (OEO) and Lactobacillus reuteri (LR) have been examined as alternatives to antibiotics for growth promotion and to improve animal health and performance. However, the mechanism underlying the OEO and LR mediation of sheep growth remains unknown. In this study, 16S rRNA gene sequencing and untargeted metabolomics were used to determine the role of the gut microbiota in the growth improvements observed. The potential modulating roles of intestinal microbial metabolites of OEO and LR to intestinal health were systematically explored as well. It was observed that both OEO and LR had greater average daily gain (ADG) and lower F/G ratio. Furthermore, OEO also appeared to have produced a greater amylase enzyme activity and mucin gene expression in the jejunal mucosa. It was also observed that OEO reduced serum IL-2 and TNF-β as well as mRNA levels of NF-κB p65, toll-like receptor-4 (TLR-4), and IL-6 in the jejunal mucosa. Moreover, dietary OEO supplementation increased the abundances of Ruminococcus, Bifidobacterium and Enterococcus, while the relative abundances of Succiniclasticum, Marvinbryantia and Streptococcus were enriched in LR group. Spearman’s correlation analysis revealed that the abundances of Bifidobacterium, Ruminococcus and Enterococcus were positively correlated with the mRNA expression of mucins. Moreover, the relative abundance of Enterococcus was positively correlated with amylase activity. Metabolomics analysis indicated that OEO and LR increased the levels of indole acetaldehyde and indole-3-acetic acid through the tryptophan metabolism pathway. It was observed that LR also decreased the inflammatory metabolites including tryptamine and 5-hydroxyindole-3-acetic acid. Collectively, these results suggested that OEO exerted a beneficial effect on growth performance and the mucosal barrier, affected tryptophan metabolism and improved the intestinal microbiota of sheep.https://www.frontiersin.org/articles/10.3389/fimmu.2022.908015/fulloregano essential oilileal microbiotametabolic profilesmucosal immunityLactobacillus reuteri |
| spellingShingle | Li Jia Jianping Wu Yu Lei Fanyun Kong Rui Zhang Jianxiang Sun Liao Wang Zemin Li Jinping Shi Ying Wang Yubing Wei Ke Zhang Zhaomin Lei Oregano Essential Oils Mediated Intestinal Microbiota and Metabolites and Improved Growth Performance and Intestinal Barrier Function in Sheep Frontiers in Immunology oregano essential oil ileal microbiota metabolic profiles mucosal immunity Lactobacillus reuteri |
| title | Oregano Essential Oils Mediated Intestinal Microbiota and Metabolites and Improved Growth Performance and Intestinal Barrier Function in Sheep |
| title_full | Oregano Essential Oils Mediated Intestinal Microbiota and Metabolites and Improved Growth Performance and Intestinal Barrier Function in Sheep |
| title_fullStr | Oregano Essential Oils Mediated Intestinal Microbiota and Metabolites and Improved Growth Performance and Intestinal Barrier Function in Sheep |
| title_full_unstemmed | Oregano Essential Oils Mediated Intestinal Microbiota and Metabolites and Improved Growth Performance and Intestinal Barrier Function in Sheep |
| title_short | Oregano Essential Oils Mediated Intestinal Microbiota and Metabolites and Improved Growth Performance and Intestinal Barrier Function in Sheep |
| title_sort | oregano essential oils mediated intestinal microbiota and metabolites and improved growth performance and intestinal barrier function in sheep |
| topic | oregano essential oil ileal microbiota metabolic profiles mucosal immunity Lactobacillus reuteri |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2022.908015/full |
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