Impact of early events and lifestyle on the gut microbiota and metabolic phenotypes in young school-age children

Abstract Background The gut microbiota evolves from birth and is in early life influenced by events such as birth mode, type of infant feeding, and maternal and infant antibiotics use. However, we still have a gap in our understanding of gut microbiota development in older children, and to what exte...

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出版年:Microbiome
主要な著者: Huanzi Zhong, John Penders, Zhun Shi, Huahui Ren, Kaiye Cai, Chao Fang, Qiuxia Ding, Carel Thijs, Ellen E. Blaak, Coen D. A. Stehouwer, Xun Xu, Huanming Yang, Jian Wang, Jun Wang, Daisy M. A. E. Jonkers, Ad A. M. Masclee, Susanne Brix, Junhua Li, Ilja C. W. Arts, Karsten Kristiansen
フォーマット: 論文
言語:英語
出版事項: BMC 2019-01-01
主題:
オンライン・アクセス:http://link.springer.com/article/10.1186/s40168-018-0608-z
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author Huanzi Zhong
John Penders
Zhun Shi
Huahui Ren
Kaiye Cai
Chao Fang
Qiuxia Ding
Carel Thijs
Ellen E. Blaak
Coen D. A. Stehouwer
Xun Xu
Huanming Yang
Jian Wang
Jun Wang
Daisy M. A. E. Jonkers
Ad A. M. Masclee
Susanne Brix
Junhua Li
Ilja C. W. Arts
Karsten Kristiansen
author_facet Huanzi Zhong
John Penders
Zhun Shi
Huahui Ren
Kaiye Cai
Chao Fang
Qiuxia Ding
Carel Thijs
Ellen E. Blaak
Coen D. A. Stehouwer
Xun Xu
Huanming Yang
Jian Wang
Jun Wang
Daisy M. A. E. Jonkers
Ad A. M. Masclee
Susanne Brix
Junhua Li
Ilja C. W. Arts
Karsten Kristiansen
author_sort Huanzi Zhong
collection DOAJ
container_title Microbiome
description Abstract Background The gut microbiota evolves from birth and is in early life influenced by events such as birth mode, type of infant feeding, and maternal and infant antibiotics use. However, we still have a gap in our understanding of gut microbiota development in older children, and to what extent early events and pre-school lifestyle modulate the composition of the gut microbiota, and how this impinges on whole body metabolic regulation in school-age children. Results Taking advantage of the KOALA Birth Cohort Study, a long-term prospective birth cohort in the Netherlands with extensive collection of high-quality host metadata, we applied shotgun metagenomics sequencing and systematically investigated the gut microbiota of children at 6–9 years of age. We demonstrated an overall adult-like gut microbiota in the 281 Dutch school-age children and identified 3 enterotypes dominated by the genera Bacteroides, Prevotella, and Bifidobacterium, respectively. Importantly, we found that breastfeeding duration in early life and pre-school dietary lifestyle correlated with the composition and functional competences of the gut microbiota in the children at school age. The correlations between pre-school dietary lifestyle and metabolic phenotypes exhibited a striking enterotype dependency. Thus, an inverse correlation between high dietary fiber consumption and low plasma insulin levels was only observed in individuals with the Bacteroides and Prevotella enterotypes, but not in Bifidobacterium enterotype individuals in whom the gut microbiota displayed overall lower microbial gene richness, alpha-diversity, functional potential for complex carbohydrate fermentation, and butyrate and succinate production. High total fat consumption and elevated plasma free fatty acid levels in the Bifidobacterium enterotype are associated with the co-occurrence of Streptococcus. Conclusions Our work highlights the persistent effects of breastfeeding duration and pre-school dietary lifestyle in affecting the gut microbiota in school-age children and reveals distinct compositional and functional potential in children according to enterotypes. The findings underscore enterotype-specific links between the host metabolic phenotypes and dietary patterns, emphasizing the importance of microbiome-based stratification when investigating metabolic responses to diets. Future diet intervention studies are clearly warranted to examine gut microbe-diet-host relationships to promote knowledge-based recommendations in relation to improving metabolic health in children.
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spelling doaj-art-f492f94de1154965a9d6058c5e273a2b2025-08-19T21:14:43ZengBMCMicrobiome2049-26182019-01-017111410.1186/s40168-018-0608-zImpact of early events and lifestyle on the gut microbiota and metabolic phenotypes in young school-age childrenHuanzi Zhong0John Penders1Zhun Shi2Huahui Ren3Kaiye Cai4Chao Fang5Qiuxia Ding6Carel Thijs7Ellen E. Blaak8Coen D. A. Stehouwer9Xun Xu10Huanming Yang11Jian Wang12Jun Wang13Daisy M. A. E. Jonkers14Ad A. M. Masclee15Susanne Brix16Junhua Li17Ilja C. W. Arts18Karsten Kristiansen19BGI-ShenzhenDepartment of Medical Microbiology, NUTRIM School of Nutrition and Translational Research in Metabolism & Care and Public Health Research Institute CAPHRI, Maastricht University Medical CentreBGI-ShenzhenBGI-ShenzhenBGI-ShenzhenBGI-ShenzhenBGI-ShenzhenDepartment of Epidemiology, Care and Public Health Research Institute CAPHRI, Maastricht UniversityDepartment of Human Biology, NUTRIM School of Nutrition and Translational Research in Metabolism, Maastricht University Medical CentreDepartment of Internal Medicine, CARIM School for Cardiovascular Diseases, Maastricht University Medical CentreBGI-ShenzhenBGI-ShenzhenBGI-ShenzhenBGI-ShenzhenDivision of Gastroenterology-Hepatology, Department of Internal Medicine, NUTRIM School of Nutrition, Toxicology and Metabolism, Maastricht University Medical CentreDivision of Gastroenterology-Hepatology, Department of Internal Medicine, NUTRIM School of Nutrition, Toxicology and Metabolism, Maastricht University Medical CentreDepartment of Biotechnology and Biomedicine, Technical University of DenmarkBGI-ShenzhenMaastricht Centre for Systems Biology (MaCSBio) & Department of Epidemiology, CARIM School for Cardiovascular Diseases, Maastricht UniversityBGI-ShenzhenAbstract Background The gut microbiota evolves from birth and is in early life influenced by events such as birth mode, type of infant feeding, and maternal and infant antibiotics use. However, we still have a gap in our understanding of gut microbiota development in older children, and to what extent early events and pre-school lifestyle modulate the composition of the gut microbiota, and how this impinges on whole body metabolic regulation in school-age children. Results Taking advantage of the KOALA Birth Cohort Study, a long-term prospective birth cohort in the Netherlands with extensive collection of high-quality host metadata, we applied shotgun metagenomics sequencing and systematically investigated the gut microbiota of children at 6–9 years of age. We demonstrated an overall adult-like gut microbiota in the 281 Dutch school-age children and identified 3 enterotypes dominated by the genera Bacteroides, Prevotella, and Bifidobacterium, respectively. Importantly, we found that breastfeeding duration in early life and pre-school dietary lifestyle correlated with the composition and functional competences of the gut microbiota in the children at school age. The correlations between pre-school dietary lifestyle and metabolic phenotypes exhibited a striking enterotype dependency. Thus, an inverse correlation between high dietary fiber consumption and low plasma insulin levels was only observed in individuals with the Bacteroides and Prevotella enterotypes, but not in Bifidobacterium enterotype individuals in whom the gut microbiota displayed overall lower microbial gene richness, alpha-diversity, functional potential for complex carbohydrate fermentation, and butyrate and succinate production. High total fat consumption and elevated plasma free fatty acid levels in the Bifidobacterium enterotype are associated with the co-occurrence of Streptococcus. Conclusions Our work highlights the persistent effects of breastfeeding duration and pre-school dietary lifestyle in affecting the gut microbiota in school-age children and reveals distinct compositional and functional potential in children according to enterotypes. The findings underscore enterotype-specific links between the host metabolic phenotypes and dietary patterns, emphasizing the importance of microbiome-based stratification when investigating metabolic responses to diets. Future diet intervention studies are clearly warranted to examine gut microbe-diet-host relationships to promote knowledge-based recommendations in relation to improving metabolic health in children.http://link.springer.com/article/10.1186/s40168-018-0608-zSchool-age childrenGut microbiotaEnterotypeMetabolic phenotypes
spellingShingle Huanzi Zhong
John Penders
Zhun Shi
Huahui Ren
Kaiye Cai
Chao Fang
Qiuxia Ding
Carel Thijs
Ellen E. Blaak
Coen D. A. Stehouwer
Xun Xu
Huanming Yang
Jian Wang
Jun Wang
Daisy M. A. E. Jonkers
Ad A. M. Masclee
Susanne Brix
Junhua Li
Ilja C. W. Arts
Karsten Kristiansen
Impact of early events and lifestyle on the gut microbiota and metabolic phenotypes in young school-age children
School-age children
Gut microbiota
Enterotype
Metabolic phenotypes
title Impact of early events and lifestyle on the gut microbiota and metabolic phenotypes in young school-age children
title_full Impact of early events and lifestyle on the gut microbiota and metabolic phenotypes in young school-age children
title_fullStr Impact of early events and lifestyle on the gut microbiota and metabolic phenotypes in young school-age children
title_full_unstemmed Impact of early events and lifestyle on the gut microbiota and metabolic phenotypes in young school-age children
title_short Impact of early events and lifestyle on the gut microbiota and metabolic phenotypes in young school-age children
title_sort impact of early events and lifestyle on the gut microbiota and metabolic phenotypes in young school age children
topic School-age children
Gut microbiota
Enterotype
Metabolic phenotypes
url http://link.springer.com/article/10.1186/s40168-018-0608-z
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