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Isomaltooligosaccharides Sustain the Growth of Prevotella Both In Vitro and in Animal Models
The human digestive tract is colonized by trillions of bacterial cells that play important roles in human health and diseases. It is well known that dietary habits are associated with human microbiota enterotypes. However, the factors that determine the enterotype still remain elusive. In this study...
Autores principales: | , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
American Society for Microbiology
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9769830/ https://www.ncbi.nlm.nih.gov/pubmed/36377936 http://dx.doi.org/10.1128/spectrum.02621-21 |
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author | Chen, Junkui Li, Zhengpeng Wang, Xiaofan Fan, Bin Deng, Feilong D.Yu, Hongwei Ze, Xiaolei Zhu, Liying Yin, Yeshi Chen, Yanhong Zhao, Jiangchao Yang, Yunsheng Wang, Xin |
author_facet | Chen, Junkui Li, Zhengpeng Wang, Xiaofan Fan, Bin Deng, Feilong D.Yu, Hongwei Ze, Xiaolei Zhu, Liying Yin, Yeshi Chen, Yanhong Zhao, Jiangchao Yang, Yunsheng Wang, Xin |
author_sort | Chen, Junkui |
collection | PubMed |
description | The human digestive tract is colonized by trillions of bacterial cells that play important roles in human health and diseases. It is well known that dietary habits are associated with human microbiota enterotypes. However, the factors that determine the enterotype still remain elusive. In this study, it was first examined, via in vitro batch fermentation, how different carbohydrates affect the Bacteroides and Prevotella enterotypes. Among the 11 substrates (fructo-, galacto-, xylo-, manno-, and isomalto-oligosaccharides [IMO] and lactulose, raffinose, starch, inulin [INU], mannitol, and xylitol) tested, IMO, INU, and starch were found to sustain the growth of Prevotella through batch fermentation. The development of the Prevotella and Bacteroides enterotypes was further simulated in chemostats using fecal samples. IMO coupled with faster dilution rates and lower pH were required to sustain the growth of Prevotella copri in the chemostat based on 16S rRNA gene and metagenomic sequencing. Meanwhile, starch with relatively lower dilution rates and higher pH was required to support the development of the Bacteroides enterotype. Amylo-α-1,6-glucosidase, pectin, and xylan lyases were the carbohydrate-active enzymes associated with the Prevotella enterotype. The Bacteroides enterotype was associated with more diversified carbohydrate-active enzymes. Consistently, since honey contains high isomaltose content, mice fed IMO and honey displayed an increased relative abundance of Prevotella in the colon. In conclusion, both in vitro systems and a mouse model were used to demonstrate that IMO maintains the Prevotella enterotype. This result provides insight into the nutritional requirements underlying gut enterotype formation. IMPORTANCE The Prevotella enterotype type is a human traditional enterotype with high dietary fiber intake, which is related to healthy ageing and Parkinson’s disease development. Manipulations of the dwelled gut microbes by dietary isomalto-oligosaccharides efficiently sustained Prevotella type enterotypes, indicating that it can be used in the improvement of elderly health by increasing the gut transit time. |
format | Online Article Text |
id | pubmed-9769830 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-97698302022-12-22 Isomaltooligosaccharides Sustain the Growth of Prevotella Both In Vitro and in Animal Models Chen, Junkui Li, Zhengpeng Wang, Xiaofan Fan, Bin Deng, Feilong D.Yu, Hongwei Ze, Xiaolei Zhu, Liying Yin, Yeshi Chen, Yanhong Zhao, Jiangchao Yang, Yunsheng Wang, Xin Microbiol Spectr Research Article The human digestive tract is colonized by trillions of bacterial cells that play important roles in human health and diseases. It is well known that dietary habits are associated with human microbiota enterotypes. However, the factors that determine the enterotype still remain elusive. In this study, it was first examined, via in vitro batch fermentation, how different carbohydrates affect the Bacteroides and Prevotella enterotypes. Among the 11 substrates (fructo-, galacto-, xylo-, manno-, and isomalto-oligosaccharides [IMO] and lactulose, raffinose, starch, inulin [INU], mannitol, and xylitol) tested, IMO, INU, and starch were found to sustain the growth of Prevotella through batch fermentation. The development of the Prevotella and Bacteroides enterotypes was further simulated in chemostats using fecal samples. IMO coupled with faster dilution rates and lower pH were required to sustain the growth of Prevotella copri in the chemostat based on 16S rRNA gene and metagenomic sequencing. Meanwhile, starch with relatively lower dilution rates and higher pH was required to support the development of the Bacteroides enterotype. Amylo-α-1,6-glucosidase, pectin, and xylan lyases were the carbohydrate-active enzymes associated with the Prevotella enterotype. The Bacteroides enterotype was associated with more diversified carbohydrate-active enzymes. Consistently, since honey contains high isomaltose content, mice fed IMO and honey displayed an increased relative abundance of Prevotella in the colon. In conclusion, both in vitro systems and a mouse model were used to demonstrate that IMO maintains the Prevotella enterotype. This result provides insight into the nutritional requirements underlying gut enterotype formation. IMPORTANCE The Prevotella enterotype type is a human traditional enterotype with high dietary fiber intake, which is related to healthy ageing and Parkinson’s disease development. Manipulations of the dwelled gut microbes by dietary isomalto-oligosaccharides efficiently sustained Prevotella type enterotypes, indicating that it can be used in the improvement of elderly health by increasing the gut transit time. American Society for Microbiology 2022-11-15 /pmc/articles/PMC9769830/ /pubmed/36377936 http://dx.doi.org/10.1128/spectrum.02621-21 Text en Copyright © 2022 Chen et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Research Article Chen, Junkui Li, Zhengpeng Wang, Xiaofan Fan, Bin Deng, Feilong D.Yu, Hongwei Ze, Xiaolei Zhu, Liying Yin, Yeshi Chen, Yanhong Zhao, Jiangchao Yang, Yunsheng Wang, Xin Isomaltooligosaccharides Sustain the Growth of Prevotella Both In Vitro and in Animal Models |
title | Isomaltooligosaccharides Sustain the Growth of Prevotella Both In Vitro and in Animal Models |
title_full | Isomaltooligosaccharides Sustain the Growth of Prevotella Both In Vitro and in Animal Models |
title_fullStr | Isomaltooligosaccharides Sustain the Growth of Prevotella Both In Vitro and in Animal Models |
title_full_unstemmed | Isomaltooligosaccharides Sustain the Growth of Prevotella Both In Vitro and in Animal Models |
title_short | Isomaltooligosaccharides Sustain the Growth of Prevotella Both In Vitro and in Animal Models |
title_sort | isomaltooligosaccharides sustain the growth of prevotella both in vitro and in animal models |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9769830/ https://www.ncbi.nlm.nih.gov/pubmed/36377936 http://dx.doi.org/10.1128/spectrum.02621-21 |
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