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...
| Main Authors: | , , , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2018-10-01
|
| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mSystems.00206-18 |
| _version_ | 1818405130500833280 |
|---|---|
| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-14T08:51:09Z |
| format | Article |
| id | doaj.art-71945bbf4bd34500aba6cd7b408b8bef |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-12-14T08:51:09Z |
| publishDate | 2018-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-71945bbf4bd34500aba6cd7b408b8bef2022-12-21T23:09:02ZengAmerican Society for MicrobiologymSystems2379-50772018-10-013610.1128/mSystems.00206-18Fucosylated Human Milk Oligosaccharides and N-Glycans in the Milk of Chinese Mothers Regulate the Gut Microbiome of Their Breast-Fed Infants during Different Lactation StagesYaqiang Bai0Jia Tao1Jiaorui Zhou2Qingjie Fan3Man Liu4Yuqi Hu5Yao Xu6Lilong Zhang7Jieli Yuan8Wenzhe Li9Xiaolei Ze10Patrice Malard11Zhimou Guo12Jingyu Yan13Ming Li14College of Basic Medical Science, Dalian Medical University, Dalian, ChinaDepartment of Gynaecology and Obstetrics, the First Affiliated Hospital of Jinzhou Medical University, Jinzhou, ChinaCollege of Basic Medical Science, Dalian Medical University, Dalian, ChinaCollege of Basic Medical Science, Dalian Medical University, Dalian, ChinaCollege of Basic Medical Science, Dalian Medical University, Dalian, ChinaCollege of Basic Medical Science, Dalian Medical University, Dalian, ChinaCollege of Basic Medical Science, Dalian Medical University, Dalian, ChinaCollege of Basic Medical Science, Dalian Medical University, Dalian, ChinaCollege of Basic Medical Science, Dalian Medical University, Dalian, ChinaCollege of Basic Medical Science, Dalian Medical University, Dalian, ChinaBiostime (Guangzhou) Health Products Ltd., Guangzhou, ChinaBiostime (Guangzhou) Health Products Ltd., Guangzhou, ChinaDalian Institute of Chemical Physics, Chinese Academy of Sciences, Key Laboratory of Separation Science for Analytical Chemistry, Dalian, ChinaDalian Institute of Chemical Physics, Chinese Academy of Sciences, Key Laboratory of Separation Science for Analytical Chemistry, Dalian, ChinaCollege of Basic Medical Science, Dalian Medical University, Dalian, ChinaABSTRACT 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.https://journals.asm.org/doi/10.1128/mSystems.00206-18FUT2HMOsfucosylationgut microbiomemilk N-glycans |
| spellingShingle | 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 mSystems FUT2 HMOs fucosylation gut microbiome milk N-glycans |
| 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_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_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_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 |
| topic | FUT2 HMOs fucosylation gut microbiome milk N-glycans |
| url | https://journals.asm.org/doi/10.1128/mSystems.00206-18 |
| work_keys_str_mv | AT yaqiangbai fucosylatedhumanmilkoligosaccharidesandnglycansinthemilkofchinesemothersregulatethegutmicrobiomeoftheirbreastfedinfantsduringdifferentlactationstages AT jiatao fucosylatedhumanmilkoligosaccharidesandnglycansinthemilkofchinesemothersregulatethegutmicrobiomeoftheirbreastfedinfantsduringdifferentlactationstages AT jiaoruizhou fucosylatedhumanmilkoligosaccharidesandnglycansinthemilkofchinesemothersregulatethegutmicrobiomeoftheirbreastfedinfantsduringdifferentlactationstages AT qingjiefan fucosylatedhumanmilkoligosaccharidesandnglycansinthemilkofchinesemothersregulatethegutmicrobiomeoftheirbreastfedinfantsduringdifferentlactationstages AT manliu fucosylatedhumanmilkoligosaccharidesandnglycansinthemilkofchinesemothersregulatethegutmicrobiomeoftheirbreastfedinfantsduringdifferentlactationstages AT yuqihu fucosylatedhumanmilkoligosaccharidesandnglycansinthemilkofchinesemothersregulatethegutmicrobiomeoftheirbreastfedinfantsduringdifferentlactationstages AT yaoxu fucosylatedhumanmilkoligosaccharidesandnglycansinthemilkofchinesemothersregulatethegutmicrobiomeoftheirbreastfedinfantsduringdifferentlactationstages AT lilongzhang fucosylatedhumanmilkoligosaccharidesandnglycansinthemilkofchinesemothersregulatethegutmicrobiomeoftheirbreastfedinfantsduringdifferentlactationstages AT jieliyuan fucosylatedhumanmilkoligosaccharidesandnglycansinthemilkofchinesemothersregulatethegutmicrobiomeoftheirbreastfedinfantsduringdifferentlactationstages AT wenzheli fucosylatedhumanmilkoligosaccharidesandnglycansinthemilkofchinesemothersregulatethegutmicrobiomeoftheirbreastfedinfantsduringdifferentlactationstages AT xiaoleize fucosylatedhumanmilkoligosaccharidesandnglycansinthemilkofchinesemothersregulatethegutmicrobiomeoftheirbreastfedinfantsduringdifferentlactationstages AT patricemalard fucosylatedhumanmilkoligosaccharidesandnglycansinthemilkofchinesemothersregulatethegutmicrobiomeoftheirbreastfedinfantsduringdifferentlactationstages AT zhimouguo fucosylatedhumanmilkoligosaccharidesandnglycansinthemilkofchinesemothersregulatethegutmicrobiomeoftheirbreastfedinfantsduringdifferentlactationstages AT jingyuyan fucosylatedhumanmilkoligosaccharidesandnglycansinthemilkofchinesemothersregulatethegutmicrobiomeoftheirbreastfedinfantsduringdifferentlactationstages AT mingli fucosylatedhumanmilkoligosaccharidesandnglycansinthemilkofchinesemothersregulatethegutmicrobiomeoftheirbreastfedinfantsduringdifferentlactationstages |