Infant gut microbiota modulation by human milk disaccharides in humanized microbiome mice
Human milk glycans present a unique diversity of structures that suggest different mechanisms by which they may affect the infant microbiome development. A humanized mouse model generated by infant fecal transplantation was utilized here to evaluate the impact of fucosyl-α1,3-GlcNAc (3FN), fucosyl-α1,6-GlcNAc, lacto-N-biose (LNB) and galacto-N-biose on the fecal microbiota and host–microbiota interactions. 16S rRNA amplicon sequencing showed that certain bacterial genera significantly increased (Ruminococcus and Oscillospira) or decreased (Eubacterium and Clostridium) in all disaccharide-supplemented groups. Interestingly, cluster analysis differentiates the consumption of fucosyl-oligosaccharides from galactosyl-oligosaccharides, highlighting the disappearance of Akkermansia genus in both fucosyl-oligosaccharides. An increment of the relative abundance of Coprococcus genus was only observed with 3FN. As well, LNB significantly increased the relative abundance of Bifidobacterium, whereas the absolute levels of this genus, as measured by quantitative real-time PCR, did not significantly increase. OTUs corresponding to the species Bifidobacterium longum, Bifidobacterium adolescentis and Ruminococcus gnavus were not present in the control after the 3-week intervention, but were shared among the donor and specific disaccharide groups, indicating that their survival is dependent on disaccharide supplementation. The 3FN-feeding group showed increased levels of butyrate and acetate in the colon, and decreased levels of serum HDL-cholesterol. 3FN also down-regulated the pro-inflammatory cytokine TNF-α and up-regulated the anti-inflammatory cytokines IL-10 and IL-13, and the Toll-like receptor 2 in the large intestine tissue. The present study revealed that the four disaccharides show efficacy in producing beneficial compositional shifts of the gut microbiota and in addition, the 3FN demonstrated physiological and immunomodulatory roles.
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Taylor & Francis
2021-05-03
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Subjects: | fucosyl-α-13-N-acetylglucosamine, fucosyl-α-16-N-acetylglucosamine, lacto-N-biosegalacto-N–biose, human milk oligosaccharides, infant fecal microbiota, humanized mouse model, short-chain fatty acidscytokines, |
Online Access: | http://hdl.handle.net/10261/244406 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100003359 http://dx.doi.org/10.13039/501100003329 |
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dig-iata-es-10261-2444062022-06-24T09:40:11Z Infant gut microbiota modulation by human milk disaccharides in humanized microbiome mice Rubio-Del-Campo, Antonio Gozalbo-Rovira, Roberto Moya Gonzálvez, Eva M. Alberola, Juan Rodríguez-Díaz, Jesús Yebra, María Jesús Ministerio de Economía y Competitividad (España) Generalitat Valenciana European Commission fucosyl-α-13-N-acetylglucosamine fucosyl-α-16-N-acetylglucosamine lacto-N-biosegalacto-N–biose human milk oligosaccharides infant fecal microbiota humanized mouse model short-chain fatty acidscytokines Human milk glycans present a unique diversity of structures that suggest different mechanisms by which they may affect the infant microbiome development. A humanized mouse model generated by infant fecal transplantation was utilized here to evaluate the impact of fucosyl-α1,3-GlcNAc (3FN), fucosyl-α1,6-GlcNAc, lacto-N-biose (LNB) and galacto-N-biose on the fecal microbiota and host–microbiota interactions. 16S rRNA amplicon sequencing showed that certain bacterial genera significantly increased (Ruminococcus and Oscillospira) or decreased (Eubacterium and Clostridium) in all disaccharide-supplemented groups. Interestingly, cluster analysis differentiates the consumption of fucosyl-oligosaccharides from galactosyl-oligosaccharides, highlighting the disappearance of Akkermansia genus in both fucosyl-oligosaccharides. An increment of the relative abundance of Coprococcus genus was only observed with 3FN. As well, LNB significantly increased the relative abundance of Bifidobacterium, whereas the absolute levels of this genus, as measured by quantitative real-time PCR, did not significantly increase. OTUs corresponding to the species Bifidobacterium longum, Bifidobacterium adolescentis and Ruminococcus gnavus were not present in the control after the 3-week intervention, but were shared among the donor and specific disaccharide groups, indicating that their survival is dependent on disaccharide supplementation. The 3FN-feeding group showed increased levels of butyrate and acetate in the colon, and decreased levels of serum HDL-cholesterol. 3FN also down-regulated the pro-inflammatory cytokine TNF-α and up-regulated the anti-inflammatory cytokines IL-10 and IL-13, and the Toll-like receptor 2 in the large intestine tissue. The present study revealed that the four disaccharides show efficacy in producing beneficial compositional shifts of the gut microbiota and in addition, the 3FN demonstrated physiological and immunomodulatory roles. This work was supported by the Spanish Ministry for Economy and Competitiveness (MINECO)/FEDER under Grant AGL2017-84165-C2 (1-R and 2-R). JRD was supported by a Ramon y Cajal Contract RYC-2013-12442 by the Spanish Ministry for Economy and Competitiveness and by Valencian Government/FEDER grant IDIFEDER/2018/056. EMMG was supported by a pre-doctoral Contract PRE2018-085768 by the Spanish Ministry of Science, Innovation and Universities. Peer reviewed 2021-06-23T05:59:48Z 2021-06-23T05:59:48Z 2021-05-03 artículo http://purl.org/coar/resource_type/c_6501 Gut microbes 13 (1): 1914377 (2021) 1949-0976 http://hdl.handle.net/10261/244406 10.1080/19490976.2021.1914377 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100003359 http://dx.doi.org/10.13039/501100003329 33938391 en #PLACEHOLDER_PARENT_METADATA_VALUE# info:eu-repo/grantAgreement/MINECO/Plan Estatal de Investigación Científica y Técnica y de Innovación 2013-2016/AGL2017-84165-C2 Publisher's version https://doi.org/10.1080/19490976.2021.1914377 Sí open Taylor & Francis |
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fucosyl-α-13-N-acetylglucosamine fucosyl-α-16-N-acetylglucosamine lacto-N-biosegalacto-N–biose human milk oligosaccharides infant fecal microbiota humanized mouse model short-chain fatty acidscytokines fucosyl-α-13-N-acetylglucosamine fucosyl-α-16-N-acetylglucosamine lacto-N-biosegalacto-N–biose human milk oligosaccharides infant fecal microbiota humanized mouse model short-chain fatty acidscytokines |
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fucosyl-α-13-N-acetylglucosamine fucosyl-α-16-N-acetylglucosamine lacto-N-biosegalacto-N–biose human milk oligosaccharides infant fecal microbiota humanized mouse model short-chain fatty acidscytokines fucosyl-α-13-N-acetylglucosamine fucosyl-α-16-N-acetylglucosamine lacto-N-biosegalacto-N–biose human milk oligosaccharides infant fecal microbiota humanized mouse model short-chain fatty acidscytokines Rubio-Del-Campo, Antonio Gozalbo-Rovira, Roberto Moya Gonzálvez, Eva M. Alberola, Juan Rodríguez-Díaz, Jesús Yebra, María Jesús Infant gut microbiota modulation by human milk disaccharides in humanized microbiome mice |
description |
Human milk glycans present a unique diversity of structures that suggest different mechanisms by which they may affect the infant microbiome development. A humanized mouse model generated by infant fecal transplantation was utilized here to evaluate the impact of fucosyl-α1,3-GlcNAc (3FN), fucosyl-α1,6-GlcNAc, lacto-N-biose (LNB) and galacto-N-biose on the fecal microbiota and host–microbiota interactions. 16S rRNA amplicon sequencing showed that certain bacterial genera significantly increased (Ruminococcus and Oscillospira) or decreased (Eubacterium and Clostridium) in all disaccharide-supplemented groups. Interestingly, cluster analysis differentiates the consumption of fucosyl-oligosaccharides from galactosyl-oligosaccharides, highlighting the disappearance of Akkermansia genus in both fucosyl-oligosaccharides. An increment of the relative abundance of Coprococcus genus was only observed with 3FN. As well, LNB significantly increased the relative abundance of Bifidobacterium, whereas the absolute levels of this genus, as measured by quantitative real-time PCR, did not significantly increase. OTUs corresponding to the species Bifidobacterium longum, Bifidobacterium adolescentis and Ruminococcus gnavus were not present in the control after the 3-week intervention, but were shared among the donor and specific disaccharide groups, indicating that their survival is dependent on disaccharide supplementation. The 3FN-feeding group showed increased levels of butyrate and acetate in the colon, and decreased levels of serum HDL-cholesterol. 3FN also down-regulated the pro-inflammatory cytokine TNF-α and up-regulated the anti-inflammatory cytokines IL-10 and IL-13, and the Toll-like receptor 2 in the large intestine tissue. The present study revealed that the four disaccharides show efficacy in producing beneficial compositional shifts of the gut microbiota and in addition, the 3FN demonstrated physiological and immunomodulatory roles. |
author2 |
Ministerio de Economía y Competitividad (España) |
author_facet |
Ministerio de Economía y Competitividad (España) Rubio-Del-Campo, Antonio Gozalbo-Rovira, Roberto Moya Gonzálvez, Eva M. Alberola, Juan Rodríguez-Díaz, Jesús Yebra, María Jesús |
format |
artículo |
topic_facet |
fucosyl-α-13-N-acetylglucosamine fucosyl-α-16-N-acetylglucosamine lacto-N-biosegalacto-N–biose human milk oligosaccharides infant fecal microbiota humanized mouse model short-chain fatty acidscytokines |
author |
Rubio-Del-Campo, Antonio Gozalbo-Rovira, Roberto Moya Gonzálvez, Eva M. Alberola, Juan Rodríguez-Díaz, Jesús Yebra, María Jesús |
author_sort |
Rubio-Del-Campo, Antonio |
title |
Infant gut microbiota modulation by human milk disaccharides in humanized microbiome mice |
title_short |
Infant gut microbiota modulation by human milk disaccharides in humanized microbiome mice |
title_full |
Infant gut microbiota modulation by human milk disaccharides in humanized microbiome mice |
title_fullStr |
Infant gut microbiota modulation by human milk disaccharides in humanized microbiome mice |
title_full_unstemmed |
Infant gut microbiota modulation by human milk disaccharides in humanized microbiome mice |
title_sort |
infant gut microbiota modulation by human milk disaccharides in humanized microbiome mice |
publisher |
Taylor & Francis |
publishDate |
2021-05-03 |
url |
http://hdl.handle.net/10261/244406 http://dx.doi.org/10.13039/501100000780 http://dx.doi.org/10.13039/501100003359 http://dx.doi.org/10.13039/501100003329 |
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