Fucosylated Human Milk Oligosaccharides and N-Glycans in the Milk of Chinese Mothers Regulate the Gut Microbiome of Their Breast-Fed Infants during Different Lactation Stages

ABSTRACT The milk glycobiome has a significant impact on the gut microbiota of infants, which plays a pivotal role in health and development. Fucosylated human milk oligosaccharides (HMOs) and N-glycans on milk proteins are beneficial for the development of healthy gut microbiota, and the fucosylati...

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Autores principales: Yaqiang Bai, Jia Tao, Jiaorui Zhou, Qingjie Fan, Man Liu, Yuqi Hu, Yao Xu, Lilong Zhang, Jieli Yuan, Wenzhe Li, Xiaolei Ze, Patrice Malard, Zhimou Guo, Jingyu Yan, Ming Li
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:71945bbf4bd34500aba6cd7b408b8bef2021-12-02T19:46:17ZFucosylated Human Milk Oligosaccharides and N-Glycans in the Milk of Chinese Mothers Regulate the Gut Microbiome of Their Breast-Fed Infants during Different Lactation Stages10.1128/mSystems.00206-182379-5077https://doaj.org/article/71945bbf4bd34500aba6cd7b408b8bef2018-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00206-18https://doaj.org/toc/2379-5077ABSTRACT The milk glycobiome has a significant impact on the gut microbiota of infants, which plays a pivotal role in health and development. Fucosylated human milk oligosaccharides (HMOs) and N-glycans on milk proteins are beneficial for the development of healthy gut microbiota, and the fucosylation levels of these glycans can be affected by the maternal fucosyltransferase 2 gene (FUT2). Here, we present results of longitudinal research on paired milk and stool samples from 56 Chinese mothers (CMs) and their breast-fed children. Changes of HMOs and fucosylated N-glycans in milk of CMs at different lactation stages were detected, which allowed characterization of the major differences in milk glycans and consequential effects on the gut microbiome of infants according to maternal FUT2 status. Significant differences in the abundance of total and fucosylated HMOs between secretor and nonsecretor CMs were noted, especially during early lactation. Despite a tendency toward decreasing milk protein concentrations, the fucosylation levels of milk N-glycans increased during late lactation. The changes in the levels of fucosylated HMOs and milk N-glycans were highly correlated with the growth of Bifidobacterium spp. and Lactobacillus spp. in the gut of infants during early and later lactation, respectively. Enriched expression of genes encoding glycoside hydrolases, glycosyl transferases, ATP-binding cassette (ABC) transporters, and permeases in infants fed by secretor CMs contributed to the promotion of these bacteria in infants. Our data highlight the important role of fucosylated milk glycans in shaping the gut microbiome of infants and provide a solid foundation for development of “personalized” nutrition for Chinese infants. IMPORTANCE Human milk glycans provide a broad range of carbon sources for gut microbes in infants. Levels of protein glycosylation in human milk vary during lactation and may also be affected by the stages of gestation and lactation and by the secretor status of the mother. This was the first study to evaluate systematically dynamic changes in human milk oligosaccharides and fucosylated N-glycans in the milk of Chinese mothers with different secretor statuses during 6 months of lactation. Given the unique single nucleotide polymorphism site (rs1047781, A385T) on the fucosyltransferase 2 gene among Chinese populations, our report provides a specific insight into the milk glycobiome of Chinese mothers, which may exert effects on the gut microbiota of infants that differ from findings from other study cohorts.Yaqiang BaiJia TaoJiaorui ZhouQingjie FanMan LiuYuqi HuYao XuLilong ZhangJieli YuanWenzhe LiXiaolei ZePatrice MalardZhimou GuoJingyu YanMing LiAmerican Society for MicrobiologyarticleFUT2HMOsfucosylationgut microbiomemilk N-glycansMicrobiologyQR1-502ENmSystems, Vol 3, Iss 6 (2018)
institution DOAJ
collection DOAJ
language EN
topic FUT2
HMOs
fucosylation
gut microbiome
milk N-glycans
Microbiology
QR1-502
spellingShingle FUT2
HMOs
fucosylation
gut microbiome
milk N-glycans
Microbiology
QR1-502
Yaqiang Bai
Jia Tao
Jiaorui Zhou
Qingjie Fan
Man Liu
Yuqi Hu
Yao Xu
Lilong Zhang
Jieli Yuan
Wenzhe Li
Xiaolei Ze
Patrice Malard
Zhimou Guo
Jingyu Yan
Ming Li
Fucosylated Human Milk Oligosaccharides and N-Glycans in the Milk of Chinese Mothers Regulate the Gut Microbiome of Their Breast-Fed Infants during Different Lactation Stages
description ABSTRACT The milk glycobiome has a significant impact on the gut microbiota of infants, which plays a pivotal role in health and development. Fucosylated human milk oligosaccharides (HMOs) and N-glycans on milk proteins are beneficial for the development of healthy gut microbiota, and the fucosylation levels of these glycans can be affected by the maternal fucosyltransferase 2 gene (FUT2). Here, we present results of longitudinal research on paired milk and stool samples from 56 Chinese mothers (CMs) and their breast-fed children. Changes of HMOs and fucosylated N-glycans in milk of CMs at different lactation stages were detected, which allowed characterization of the major differences in milk glycans and consequential effects on the gut microbiome of infants according to maternal FUT2 status. Significant differences in the abundance of total and fucosylated HMOs between secretor and nonsecretor CMs were noted, especially during early lactation. Despite a tendency toward decreasing milk protein concentrations, the fucosylation levels of milk N-glycans increased during late lactation. The changes in the levels of fucosylated HMOs and milk N-glycans were highly correlated with the growth of Bifidobacterium spp. and Lactobacillus spp. in the gut of infants during early and later lactation, respectively. Enriched expression of genes encoding glycoside hydrolases, glycosyl transferases, ATP-binding cassette (ABC) transporters, and permeases in infants fed by secretor CMs contributed to the promotion of these bacteria in infants. Our data highlight the important role of fucosylated milk glycans in shaping the gut microbiome of infants and provide a solid foundation for development of “personalized” nutrition for Chinese infants. IMPORTANCE Human milk glycans provide a broad range of carbon sources for gut microbes in infants. Levels of protein glycosylation in human milk vary during lactation and may also be affected by the stages of gestation and lactation and by the secretor status of the mother. This was the first study to evaluate systematically dynamic changes in human milk oligosaccharides and fucosylated N-glycans in the milk of Chinese mothers with different secretor statuses during 6 months of lactation. Given the unique single nucleotide polymorphism site (rs1047781, A385T) on the fucosyltransferase 2 gene among Chinese populations, our report provides a specific insight into the milk glycobiome of Chinese mothers, which may exert effects on the gut microbiota of infants that differ from findings from other study cohorts.
format article
author Yaqiang Bai
Jia Tao
Jiaorui Zhou
Qingjie Fan
Man Liu
Yuqi Hu
Yao Xu
Lilong Zhang
Jieli Yuan
Wenzhe Li
Xiaolei Ze
Patrice Malard
Zhimou Guo
Jingyu Yan
Ming Li
author_facet Yaqiang Bai
Jia Tao
Jiaorui Zhou
Qingjie Fan
Man Liu
Yuqi Hu
Yao Xu
Lilong Zhang
Jieli Yuan
Wenzhe Li
Xiaolei Ze
Patrice Malard
Zhimou Guo
Jingyu Yan
Ming Li
author_sort Yaqiang Bai
title Fucosylated Human Milk Oligosaccharides and N-Glycans in the Milk of Chinese Mothers Regulate the Gut Microbiome of Their Breast-Fed Infants during Different Lactation Stages
title_short Fucosylated Human Milk Oligosaccharides and N-Glycans in the Milk of Chinese Mothers Regulate the Gut Microbiome of Their Breast-Fed Infants during Different Lactation Stages
title_full Fucosylated Human Milk Oligosaccharides and N-Glycans in the Milk of Chinese Mothers Regulate the Gut Microbiome of Their Breast-Fed Infants during Different Lactation Stages
title_fullStr Fucosylated Human Milk Oligosaccharides and N-Glycans in the Milk of Chinese Mothers Regulate the Gut Microbiome of Their Breast-Fed Infants during Different Lactation Stages
title_full_unstemmed Fucosylated Human Milk Oligosaccharides and N-Glycans in the Milk of Chinese Mothers Regulate the Gut Microbiome of Their Breast-Fed Infants during Different Lactation Stages
title_sort fucosylated human milk oligosaccharides and n-glycans in the milk of chinese mothers regulate the gut microbiome of their breast-fed infants during different lactation stages
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/71945bbf4bd34500aba6cd7b408b8bef
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