Xylan alleviates dietary fiber deprivation-induced dysbiosis by selectively promoting Bifidobacterium pseudocatenulatum in pigs
Abstract Background Low dietary fiber intake has been shown to disturb the gut microbiome community, damage the mucus barrier, and promote pathogen susceptibility. However, little is known about the temporal response of the gut microbiome to dietary fiber deprivation and the recovery induced by diet...
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| Format: | Article |
| Language: | English |
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BMC
2021-11-01
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| Series: | Microbiome |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s40168-021-01175-x |
| _version_ | 1819000926878302208 |
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| author | Zhenyu Wang Yu Bai Yu Pi Walter J. J. Gerrits Sonja de Vries Lijun Shang Shiyu Tao Shiyi Zhang Dandan Han Zhengpeng Zhu Junjun Wang |
| author_facet | Zhenyu Wang Yu Bai Yu Pi Walter J. J. Gerrits Sonja de Vries Lijun Shang Shiyu Tao Shiyi Zhang Dandan Han Zhengpeng Zhu Junjun Wang |
| author_sort | Zhenyu Wang |
| collection | DOAJ |
| description | Abstract Background Low dietary fiber intake has been shown to disturb the gut microbiome community, damage the mucus barrier, and promote pathogen susceptibility. However, little is known about the temporal response of the gut microbiome to dietary fiber deprivation and the recovery induced by dietary fiber inclusion in pigs. Objective In the present study, temporal responses of ileal and fecal microbiota to dietary fiber deprivation were profiled using an ileum cannulated growing pig model. In addition, the potential of dietary-resistant starch, β-glucan, and xylan to alleviate gut dysbiosis throughout the gastrointestinal tract, as well as its possible mechanisms were investigated. Methods Six cannulated growing pigs were fed a fiber deprivation diet for 35 days. Ileal digesta and feces were collected at days 0, 7, 21, and 35 for 16S rRNA sequencing and short-chain fatty acid (SCFA) determination. Another twenty-four healthy growing pigs were assigned to one of four dietary treatments including (1) fiber-free diet, (2) resistant starch diet, (3) β-glucan diet, and (4) xylan diet. These twenty-four pigs were fed a corresponding diet for 35 days and slaughtered. Gut microbiome and SCFA concentration were profiled along the gastrointestinal tract. Results Dietary fiber deprivation-induced consistent microbiota extinction, mainly Bifidobacterium and Lactobacillus, and decreased SCFA concentrations in both ileum and feces. The community structure partially recovered at day 35 compared with baseline while SCFA concentrations remained low. Xylan supplementation alleviated gut dysbiosis by selectively promoting Bifidobacterium pseudocatenulatum within the large intestine. SCFA concentration increased significantly after xylan supplementation and exhibited a positive association with B. pseudocatenulatum abundance. An elevated abundance of xylan degradation-related enzyme genes was also observed in the gut microbiome after xylan supplementation. In vitro growth assay further verified the xylan utilization capacity of B. pseudocatenulatum. Conclusions Dietary fiber deprivation could induce probiotic extinction and loss of the SCFA production while potential pathogen was promoted. Xylan intervention could partially restore dietary fiber deprivation-induced gut dysbiosis through selectively promoting B. pseudocatenulatum and therefore normalizing the gut environment. These findings collectively provide evidence that dietary fiber-driven microbiota metabolism bridges the interplay between microbiome and gut health. Video abstract |
| first_indexed | 2024-12-20T22:41:05Z |
| format | Article |
| id | doaj.art-06a1f60fee6848f8a225f201570511ca |
| institution | Directory Open Access Journal |
| issn | 2049-2618 |
| language | English |
| last_indexed | 2024-12-20T22:41:05Z |
| publishDate | 2021-11-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj.art-06a1f60fee6848f8a225f201570511ca2022-12-21T19:24:27ZengBMCMicrobiome2049-26182021-11-019111410.1186/s40168-021-01175-xXylan alleviates dietary fiber deprivation-induced dysbiosis by selectively promoting Bifidobacterium pseudocatenulatum in pigsZhenyu Wang0Yu Bai1Yu Pi2Walter J. J. Gerrits3Sonja de Vries4Lijun Shang5Shiyu Tao6Shiyi Zhang7Dandan Han8Zhengpeng Zhu9Junjun Wang10State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural UniversityState Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural UniversityState Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural UniversityAnimal Nutrition Group, Wageningen University & ResearchAnimal Nutrition Group, Wageningen University & ResearchState Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural UniversityState Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural UniversityAnimal Nutrition Group, Wageningen University & ResearchState Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural UniversityTequ Group Co., Ltd.State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural UniversityAbstract Background Low dietary fiber intake has been shown to disturb the gut microbiome community, damage the mucus barrier, and promote pathogen susceptibility. However, little is known about the temporal response of the gut microbiome to dietary fiber deprivation and the recovery induced by dietary fiber inclusion in pigs. Objective In the present study, temporal responses of ileal and fecal microbiota to dietary fiber deprivation were profiled using an ileum cannulated growing pig model. In addition, the potential of dietary-resistant starch, β-glucan, and xylan to alleviate gut dysbiosis throughout the gastrointestinal tract, as well as its possible mechanisms were investigated. Methods Six cannulated growing pigs were fed a fiber deprivation diet for 35 days. Ileal digesta and feces were collected at days 0, 7, 21, and 35 for 16S rRNA sequencing and short-chain fatty acid (SCFA) determination. Another twenty-four healthy growing pigs were assigned to one of four dietary treatments including (1) fiber-free diet, (2) resistant starch diet, (3) β-glucan diet, and (4) xylan diet. These twenty-four pigs were fed a corresponding diet for 35 days and slaughtered. Gut microbiome and SCFA concentration were profiled along the gastrointestinal tract. Results Dietary fiber deprivation-induced consistent microbiota extinction, mainly Bifidobacterium and Lactobacillus, and decreased SCFA concentrations in both ileum and feces. The community structure partially recovered at day 35 compared with baseline while SCFA concentrations remained low. Xylan supplementation alleviated gut dysbiosis by selectively promoting Bifidobacterium pseudocatenulatum within the large intestine. SCFA concentration increased significantly after xylan supplementation and exhibited a positive association with B. pseudocatenulatum abundance. An elevated abundance of xylan degradation-related enzyme genes was also observed in the gut microbiome after xylan supplementation. In vitro growth assay further verified the xylan utilization capacity of B. pseudocatenulatum. Conclusions Dietary fiber deprivation could induce probiotic extinction and loss of the SCFA production while potential pathogen was promoted. Xylan intervention could partially restore dietary fiber deprivation-induced gut dysbiosis through selectively promoting B. pseudocatenulatum and therefore normalizing the gut environment. These findings collectively provide evidence that dietary fiber-driven microbiota metabolism bridges the interplay between microbiome and gut health. Video abstracthttps://doi.org/10.1186/s40168-021-01175-xBifidobacteriumGut healthMicrobiotaXylan |
| spellingShingle | Zhenyu Wang Yu Bai Yu Pi Walter J. J. Gerrits Sonja de Vries Lijun Shang Shiyu Tao Shiyi Zhang Dandan Han Zhengpeng Zhu Junjun Wang Xylan alleviates dietary fiber deprivation-induced dysbiosis by selectively promoting Bifidobacterium pseudocatenulatum in pigs Microbiome Bifidobacterium Gut health Microbiota Xylan |
| title | Xylan alleviates dietary fiber deprivation-induced dysbiosis by selectively promoting Bifidobacterium pseudocatenulatum in pigs |
| title_full | Xylan alleviates dietary fiber deprivation-induced dysbiosis by selectively promoting Bifidobacterium pseudocatenulatum in pigs |
| title_fullStr | Xylan alleviates dietary fiber deprivation-induced dysbiosis by selectively promoting Bifidobacterium pseudocatenulatum in pigs |
| title_full_unstemmed | Xylan alleviates dietary fiber deprivation-induced dysbiosis by selectively promoting Bifidobacterium pseudocatenulatum in pigs |
| title_short | Xylan alleviates dietary fiber deprivation-induced dysbiosis by selectively promoting Bifidobacterium pseudocatenulatum in pigs |
| title_sort | xylan alleviates dietary fiber deprivation induced dysbiosis by selectively promoting bifidobacterium pseudocatenulatum in pigs |
| topic | Bifidobacterium Gut health Microbiota Xylan |
| url | https://doi.org/10.1186/s40168-021-01175-x |
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