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Research Article | Host-Microbe Biology

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

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
Janet K. Jansson, Editor
Yaqiang Bai
aCollege of Basic Medical Science, Dalian Medical University, Dalian, China
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Jia Tao
bDepartment of Gynaecology and Obstetrics, the First Affiliated Hospital of Jinzhou Medical University, Jinzhou, China
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Jiaorui Zhou
aCollege of Basic Medical Science, Dalian Medical University, Dalian, China
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Qingjie Fan
aCollege of Basic Medical Science, Dalian Medical University, Dalian, China
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Man Liu
aCollege of Basic Medical Science, Dalian Medical University, Dalian, China
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Yuqi Hu
aCollege of Basic Medical Science, Dalian Medical University, Dalian, China
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Yao Xu
aCollege of Basic Medical Science, Dalian Medical University, Dalian, China
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Lilong Zhang
aCollege of Basic Medical Science, Dalian Medical University, Dalian, China
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Jieli Yuan
aCollege of Basic Medical Science, Dalian Medical University, Dalian, China
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Wenzhe Li
aCollege of Basic Medical Science, Dalian Medical University, Dalian, China
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Xiaolei Ze
cBiostime (Guangzhou) Health Products Ltd., Guangzhou, China
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Patrice Malard
cBiostime (Guangzhou) Health Products Ltd., Guangzhou, China
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Zhimou Guo
dDalian Institute of Chemical Physics, Chinese Academy of Sciences, Key Laboratory of Separation Science for Analytical Chemistry, Dalian, China
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Jingyu Yan
dDalian Institute of Chemical Physics, Chinese Academy of Sciences, Key Laboratory of Separation Science for Analytical Chemistry, Dalian, China
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Ming Li
aCollege of Basic Medical Science, Dalian Medical University, Dalian, China
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Janet K. Jansson
Pacific Northwest National Laboratory
Roles: Editor
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DOI: 10.1128/mSystems.00206-18
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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.

  • Copyright © 2018 Bai et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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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
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
mSystems Dec 2018, 3 (6) e00206-18; DOI: 10.1128/mSystems.00206-18

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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
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
mSystems Dec 2018, 3 (6) e00206-18; DOI: 10.1128/mSystems.00206-18
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KEYWORDS

FUT2
HMOs
fucosylation
gut microbiome
milk N-glycans

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