Clostridium butyricum and carbohydrate active enzymes contribute to the reduced fat deposition in pigs
Abstract Pig gastrointestinal tracts harbor a heterogeneous and dynamic ecosystem populated with trillions of microbes, enhancing the ability of the host to harvest energy from dietary carbohydrates and contributing to host adipogenesis and fatness. However, the microbial community structure and rel...
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Wiley
2024-02-01
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Online Access: | https://doi.org/10.1002/imt2.160 |
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author | Lingyan Ma Shiyu Tao Tongxing Song Wentao Lyu Ying Li Wen Wang Qicheng Shen Yan Ni Jiang Zhu Jiangchao Zhao Hua Yang Yingping Xiao |
author_facet | Lingyan Ma Shiyu Tao Tongxing Song Wentao Lyu Ying Li Wen Wang Qicheng Shen Yan Ni Jiang Zhu Jiangchao Zhao Hua Yang Yingping Xiao |
author_sort | Lingyan Ma |
collection | DOAJ |
description | Abstract Pig gastrointestinal tracts harbor a heterogeneous and dynamic ecosystem populated with trillions of microbes, enhancing the ability of the host to harvest energy from dietary carbohydrates and contributing to host adipogenesis and fatness. However, the microbial community structure and related mechanisms responsible for the differences between the fatty phenotypes and the lean phenotypes of the pigs remained to be comprehensively elucidated. Herein, we first found significant differences in microbial composition and potential functional capacity among different gut locations in Jinhua pigs with distinct fatness phenotypes. Second, we identified that Jinhua pigs with lower fatness exhibited higher levels of short‐chain fatty acids in the colon, highlighting their enhanced carbohydrate fermentation capacity. Third, we explored the differences in expressed carbohydrate‐active enzyme (CAZyme) in pigs, indicating their involvement in modulating fat storage. Notably, Clostridium butyricum might be a representative bacterial species from Jinhua pigs with lower fatness, and a significantly higher percentage of its genome was dedicated to CAZyme glycoside hydrolase family 13 (GH13). Finally, a subsequent mouse intervention study substantiated the beneficial effects of C. butyricum isolated from experimental pigs, suggesting that it may possess characteristics that promote the utilization of carbohydrates and hinder fat accumulation. Remarkably, when Jinhua pigs were administered C. butyricum, similar alterations in the gut microbiome and host fatness traits were observed, further supporting the potential role of C. butyricum in modulating fatness. Taken together, our findings reveal previously overlooked links between C. butyricum and CAZyme function, providing insight into the basic mechanisms that connect gut microbiome functions to host fatness. |
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language | English |
last_indexed | 2024-03-07T23:28:41Z |
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spelling | doaj.art-6f5a04030fca4cedacb76607f1f95b982024-02-21T00:51:23ZengWileyiMeta2770-596X2024-02-0131n/an/a10.1002/imt2.160Clostridium butyricum and carbohydrate active enzymes contribute to the reduced fat deposition in pigsLingyan Ma0Shiyu Tao1Tongxing Song2Wentao Lyu3Ying Li4Wen Wang5Qicheng Shen6Yan Ni7Jiang Zhu8Jiangchao Zhao9Hua Yang10Yingping Xiao11State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro‐Products, Institute of Agro‐product Safety and Nutrition Zhejiang Academy of Agricultural Sciences Hangzhou ChinaDepartment of Animal Nutrition and Feed Science, College of Animal Sciences and Technology Huazhong Agricultural University Wuhan ChinaDepartment of Animal Nutrition and Feed Science, College of Animal Sciences and Technology Huazhong Agricultural University Wuhan ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro‐Products, Institute of Agro‐product Safety and Nutrition Zhejiang Academy of Agricultural Sciences Hangzhou ChinaGuangdong Provincial Key Laboratory of Animal Molecular Design and Precise Breeding, College of Life Science and Engineering Foshan University Foshan ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro‐Products, Institute of Agro‐product Safety and Nutrition Zhejiang Academy of Agricultural Sciences Hangzhou ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro‐Products, Institute of Agro‐product Safety and Nutrition Zhejiang Academy of Agricultural Sciences Hangzhou ChinaThe Children's Hospital, Zhejiang University School of Medicine National Clinical Research Center for Child Health Hangzhou ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro‐Products, Institute of Agro‐product Safety and Nutrition Zhejiang Academy of Agricultural Sciences Hangzhou ChinaDepartment of Animal Science, Division of Agriculture University of Arkansas Fayetteville Arkansas USAState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro‐Products, Institute of Agro‐product Safety and Nutrition Zhejiang Academy of Agricultural Sciences Hangzhou ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro‐Products, Institute of Agro‐product Safety and Nutrition Zhejiang Academy of Agricultural Sciences Hangzhou ChinaAbstract Pig gastrointestinal tracts harbor a heterogeneous and dynamic ecosystem populated with trillions of microbes, enhancing the ability of the host to harvest energy from dietary carbohydrates and contributing to host adipogenesis and fatness. However, the microbial community structure and related mechanisms responsible for the differences between the fatty phenotypes and the lean phenotypes of the pigs remained to be comprehensively elucidated. Herein, we first found significant differences in microbial composition and potential functional capacity among different gut locations in Jinhua pigs with distinct fatness phenotypes. Second, we identified that Jinhua pigs with lower fatness exhibited higher levels of short‐chain fatty acids in the colon, highlighting their enhanced carbohydrate fermentation capacity. Third, we explored the differences in expressed carbohydrate‐active enzyme (CAZyme) in pigs, indicating their involvement in modulating fat storage. Notably, Clostridium butyricum might be a representative bacterial species from Jinhua pigs with lower fatness, and a significantly higher percentage of its genome was dedicated to CAZyme glycoside hydrolase family 13 (GH13). Finally, a subsequent mouse intervention study substantiated the beneficial effects of C. butyricum isolated from experimental pigs, suggesting that it may possess characteristics that promote the utilization of carbohydrates and hinder fat accumulation. Remarkably, when Jinhua pigs were administered C. butyricum, similar alterations in the gut microbiome and host fatness traits were observed, further supporting the potential role of C. butyricum in modulating fatness. Taken together, our findings reveal previously overlooked links between C. butyricum and CAZyme function, providing insight into the basic mechanisms that connect gut microbiome functions to host fatness.https://doi.org/10.1002/imt2.160CAZymesClostridium butyricumfatnessgut microbiotaJinhua pigsmetagenomics |
spellingShingle | Lingyan Ma Shiyu Tao Tongxing Song Wentao Lyu Ying Li Wen Wang Qicheng Shen Yan Ni Jiang Zhu Jiangchao Zhao Hua Yang Yingping Xiao Clostridium butyricum and carbohydrate active enzymes contribute to the reduced fat deposition in pigs iMeta CAZymes Clostridium butyricum fatness gut microbiota Jinhua pigs metagenomics |
title | Clostridium butyricum and carbohydrate active enzymes contribute to the reduced fat deposition in pigs |
title_full | Clostridium butyricum and carbohydrate active enzymes contribute to the reduced fat deposition in pigs |
title_fullStr | Clostridium butyricum and carbohydrate active enzymes contribute to the reduced fat deposition in pigs |
title_full_unstemmed | Clostridium butyricum and carbohydrate active enzymes contribute to the reduced fat deposition in pigs |
title_short | Clostridium butyricum and carbohydrate active enzymes contribute to the reduced fat deposition in pigs |
title_sort | clostridium butyricum and carbohydrate active enzymes contribute to the reduced fat deposition in pigs |
topic | CAZymes Clostridium butyricum fatness gut microbiota Jinhua pigs metagenomics |
url | https://doi.org/10.1002/imt2.160 |
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