Maternal fucosyltransferase 2 status affects the gut bifidobacterial communities of breastfed infants

Zachery T. Lewis, Sarah M. Totten, Jennifer T. Smilowitz, Mina Popovic, Evan Parker, Danielle G. Lemay, Maxwell L. Van Tassell, Michael J. Miller, Yong Su Jin, J. Bruce German, Carlito B Lebrilla, David A. Mills

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124 Citations (Scopus)

Abstract

Background Individuals with inactive alleles of the fucosyltransferase 2 gene (FUT2; termed the 'secretor' gene) are common in many populations. Some members of the genus Bifidobacterium, common infant gut commensals, are known to consume 2'-fucosylated glycans found in the breast milk of secretor mothers. We investigated the effects of maternal secretor status on the developing infant microbiota with a special emphasis on bifidobacterial species abundance. Results On average, bifidobacteria were established earlier and more often in infants fed by secretor mothers than in infants fed by non-secretor mothers. In secretor-fed infants, the relative abundance of the Bifidobacterium longum group was most strongly correlated with high percentages of the order Bifidobacteriales. Conversely, in non-secretor-fed infants, Bifidobacterium breve was positively correlated with Bifidobacteriales, while the B. longum group was negatively correlated. A higher percentage of bifidobacteria isolated from secretorfed infants consumed 2'-fucosyllactose. Infant feces with high levels of bifidobacteria had lower milk oligosaccharide levels in the feces and higher amounts of lactate. Furthermore, feces containing different bifidobacterial species possessed differing amounts of oligosaccharides, suggesting differential consumption in situ. Conclusions Infants fed by non-secretor mothers are delayed in the establishment of a bifidobacteria-laden microbiota. This delay may be due to difficulties in the infant acquiring a species of bifidobacteria able to consume the specific milk oligosaccharides delivered by the mother. This work provides mechanistic insight into how milk glycans enrich specific beneficial bacterial populations in infants and reveals clues for enhancing enrichment of bifidobacterial populations in at risk populations - such as premature infants.

Original languageEnglish (US)
Article number13
JournalMicrobiome
Volume3
Issue number1
DOIs
StatePublished - Apr 10 2015

Fingerprint

Mothers
Bifidobacterium
Oligosaccharides
Feces
Milk
Microbiota
Polysaccharides
galactoside 2-alpha-L-fucosyltransferase
Population
Human Milk
Premature Infants
Genes
Lactic Acid
Alleles

Keywords

  • Bifidobacteria
  • Breastfeeding
  • FUT2
  • Human milk oligosaccharides
  • Infant
  • Marker gene sequencing
  • Secretor
  • Short-chain fatty acids

ASJC Scopus subject areas

  • Microbiology
  • Microbiology (medical)

Cite this

Lewis, Z. T., Totten, S. M., Smilowitz, J. T., Popovic, M., Parker, E., Lemay, D. G., ... Mills, D. A. (2015). Maternal fucosyltransferase 2 status affects the gut bifidobacterial communities of breastfed infants. Microbiome, 3(1), [13]. https://doi.org/10.1186/s40168-015-0071-z

Maternal fucosyltransferase 2 status affects the gut bifidobacterial communities of breastfed infants. / Lewis, Zachery T.; Totten, Sarah M.; Smilowitz, Jennifer T.; Popovic, Mina; Parker, Evan; Lemay, Danielle G.; Van Tassell, Maxwell L.; Miller, Michael J.; Jin, Yong Su; German, J. Bruce; Lebrilla, Carlito B; Mills, David A.

In: Microbiome, Vol. 3, No. 1, 13, 10.04.2015.

Research output: Contribution to journalArticle

Lewis, ZT, Totten, SM, Smilowitz, JT, Popovic, M, Parker, E, Lemay, DG, Van Tassell, ML, Miller, MJ, Jin, YS, German, JB, Lebrilla, CB & Mills, DA 2015, 'Maternal fucosyltransferase 2 status affects the gut bifidobacterial communities of breastfed infants', Microbiome, vol. 3, no. 1, 13. https://doi.org/10.1186/s40168-015-0071-z
Lewis, Zachery T. ; Totten, Sarah M. ; Smilowitz, Jennifer T. ; Popovic, Mina ; Parker, Evan ; Lemay, Danielle G. ; Van Tassell, Maxwell L. ; Miller, Michael J. ; Jin, Yong Su ; German, J. Bruce ; Lebrilla, Carlito B ; Mills, David A. / Maternal fucosyltransferase 2 status affects the gut bifidobacterial communities of breastfed infants. In: Microbiome. 2015 ; Vol. 3, No. 1.
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abstract = "Background Individuals with inactive alleles of the fucosyltransferase 2 gene (FUT2; termed the 'secretor' gene) are common in many populations. Some members of the genus Bifidobacterium, common infant gut commensals, are known to consume 2'-fucosylated glycans found in the breast milk of secretor mothers. We investigated the effects of maternal secretor status on the developing infant microbiota with a special emphasis on bifidobacterial species abundance. Results On average, bifidobacteria were established earlier and more often in infants fed by secretor mothers than in infants fed by non-secretor mothers. In secretor-fed infants, the relative abundance of the Bifidobacterium longum group was most strongly correlated with high percentages of the order Bifidobacteriales. Conversely, in non-secretor-fed infants, Bifidobacterium breve was positively correlated with Bifidobacteriales, while the B. longum group was negatively correlated. A higher percentage of bifidobacteria isolated from secretorfed infants consumed 2'-fucosyllactose. Infant feces with high levels of bifidobacteria had lower milk oligosaccharide levels in the feces and higher amounts of lactate. Furthermore, feces containing different bifidobacterial species possessed differing amounts of oligosaccharides, suggesting differential consumption in situ. Conclusions Infants fed by non-secretor mothers are delayed in the establishment of a bifidobacteria-laden microbiota. This delay may be due to difficulties in the infant acquiring a species of bifidobacteria able to consume the specific milk oligosaccharides delivered by the mother. This work provides mechanistic insight into how milk glycans enrich specific beneficial bacterial populations in infants and reveals clues for enhancing enrichment of bifidobacterial populations in at risk populations - such as premature infants.",
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AU - Totten, Sarah M.

AU - Smilowitz, Jennifer T.

AU - Popovic, Mina

AU - Parker, Evan

AU - Lemay, Danielle G.

AU - Van Tassell, Maxwell L.

AU - Miller, Michael J.

AU - Jin, Yong Su

AU - German, J. Bruce

AU - Lebrilla, Carlito B

AU - Mills, David A.

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N2 - Background Individuals with inactive alleles of the fucosyltransferase 2 gene (FUT2; termed the 'secretor' gene) are common in many populations. Some members of the genus Bifidobacterium, common infant gut commensals, are known to consume 2'-fucosylated glycans found in the breast milk of secretor mothers. We investigated the effects of maternal secretor status on the developing infant microbiota with a special emphasis on bifidobacterial species abundance. Results On average, bifidobacteria were established earlier and more often in infants fed by secretor mothers than in infants fed by non-secretor mothers. In secretor-fed infants, the relative abundance of the Bifidobacterium longum group was most strongly correlated with high percentages of the order Bifidobacteriales. Conversely, in non-secretor-fed infants, Bifidobacterium breve was positively correlated with Bifidobacteriales, while the B. longum group was negatively correlated. A higher percentage of bifidobacteria isolated from secretorfed infants consumed 2'-fucosyllactose. Infant feces with high levels of bifidobacteria had lower milk oligosaccharide levels in the feces and higher amounts of lactate. Furthermore, feces containing different bifidobacterial species possessed differing amounts of oligosaccharides, suggesting differential consumption in situ. Conclusions Infants fed by non-secretor mothers are delayed in the establishment of a bifidobacteria-laden microbiota. This delay may be due to difficulties in the infant acquiring a species of bifidobacteria able to consume the specific milk oligosaccharides delivered by the mother. This work provides mechanistic insight into how milk glycans enrich specific beneficial bacterial populations in infants and reveals clues for enhancing enrichment of bifidobacterial populations in at risk populations - such as premature infants.

AB - Background Individuals with inactive alleles of the fucosyltransferase 2 gene (FUT2; termed the 'secretor' gene) are common in many populations. Some members of the genus Bifidobacterium, common infant gut commensals, are known to consume 2'-fucosylated glycans found in the breast milk of secretor mothers. We investigated the effects of maternal secretor status on the developing infant microbiota with a special emphasis on bifidobacterial species abundance. Results On average, bifidobacteria were established earlier and more often in infants fed by secretor mothers than in infants fed by non-secretor mothers. In secretor-fed infants, the relative abundance of the Bifidobacterium longum group was most strongly correlated with high percentages of the order Bifidobacteriales. Conversely, in non-secretor-fed infants, Bifidobacterium breve was positively correlated with Bifidobacteriales, while the B. longum group was negatively correlated. A higher percentage of bifidobacteria isolated from secretorfed infants consumed 2'-fucosyllactose. Infant feces with high levels of bifidobacteria had lower milk oligosaccharide levels in the feces and higher amounts of lactate. Furthermore, feces containing different bifidobacterial species possessed differing amounts of oligosaccharides, suggesting differential consumption in situ. Conclusions Infants fed by non-secretor mothers are delayed in the establishment of a bifidobacteria-laden microbiota. This delay may be due to difficulties in the infant acquiring a species of bifidobacteria able to consume the specific milk oligosaccharides delivered by the mother. This work provides mechanistic insight into how milk glycans enrich specific beneficial bacterial populations in infants and reveals clues for enhancing enrichment of bifidobacterial populations in at risk populations - such as premature infants.

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KW - Breastfeeding

KW - FUT2

KW - Human milk oligosaccharides

KW - Infant

KW - Marker gene sequencing

KW - Secretor

KW - Short-chain fatty acids

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