Consumption of human milk glycoconjugates by infant-associated bifidobacteria: mechanisms and implications

Garrido, Daniel; Dallas, David C.; Mills, David A.

doi:10.1099/mic.0.064113-0

Cited by 228Infant Nutrition and HealthGut microbiota and healthProbiotics and Fermented Foods

Consumption of human milk glycoconjugates by infant-associated bifidobacteria: mechanisms and implications

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Garrido, Daniel, Dallas, David C., Mills, David A.·2013·Microbiology

DOI 10.1099/mic.0.064113-0PMC PMC4083661

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Abstract

Human milk is a rich source of nutrients and energy, shaped by mammalian evolution to provide all the nutritive requirements of the newborn. In addition, several molecules in breast milk act as bioactive agents, playing an important role in infant protection and guiding a proper development. While major breast milk nutrients such as lactose, lipids and proteins are readily digested and consumed by the infant, other molecules, such as human milk oligosaccharides and glycosylated proteins and lipids, can escape intestinal digestion and transit through the gastrointestinal tract. In this environment, these molecules guide the composition of the developing infant intestinal microbiota by preventing the colonization of enteric pathogens and providing carbon and nitrogen sources for other colonic commensals. Only a few bacteria, in particular Bifidobacterium species, can gain access to the energetic content of milk as it is displayed in the colon, probably contributing to their predominance in the intestinal microbiota in the first year of life. Bifidobacteria deploy exquisite molecular mechanisms to utilize human milk oligosaccharides, and recent evidence indicates that their activities also target other human milk glycoconjugates. Here, we review advances in our understanding of how these microbes have been shaped by breast milk components and the strategies associated with their consumption of milk glycoconjugates.

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Infants fed formula supplemented with B-GOS had increased abundance of Bifidobacterium and Lactobacillus compared to unsupplemented infants, similar to breastfed infants.
“Infants fed formula supplemented with Bimuno-galactooligosaccharide (B-GOS®; Bimuno™, Clasado Biosciences Ltd, Buckinghamshire, UK), a proprietary product containing at least 65% GOS, had increased abundance of Bifidobacterium and Lactobacillus compared to unsupplemented infants, similar to levels reported in breastfed infants (Garrido et al., 2013;Vandenplas et al., 2014).”
From The Microbiota-Gut-Brain Axis (2019) · cites this paper as Garrido et al., 2013
B. infantis is able to produce extracellular glycosidases that allow it to cleave and consume these glycan moieties.
“However, B. infantis is able to produce extracellular glycosidases that allow it to cleave and consume these glycan moieties [45, 92].”
From Pilot study of probiotic/colostrum supplementation on gut function in children with autism and gastrointestinal symptoms (2019) · cites this paper as [92]

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The Microbiota-Gut-Brain Axis
Cryan, J. F., O'Riordan, K. J., Cowan, C. S. M., Sandhu, K. V., Bastiaanssen, T. F. S., Boehme, M., Codagnone, M. G., Cussotto, S., Fulling, C., Golubeva, A. V., et al. (2019) · Physiological Reviews · doi:10.1152/physrev.00018.2018 · Cited by 5,286 · see citing works
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Variation in Consumption of Human Milk Oligosaccharides by Infant Gut-Associated Strains of Bifidobacterium breve
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Both Lewis and Secretor Status Mediate Susceptibility to Rotavirus Infections in a Rotavirus Genotype–Dependent Manner
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Oral supplementation of healthy adults with 2′- O -fucosyllactose and lacto- N -neotetraose is well tolerated and shifts the intestinal microbiota
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Salmonella versus the Microbiome
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Human Milk Glycomics and Gut Microbial Genomics in Infant Feces Show a Correlation between Human Milk Oligosaccharides and Gut Microbiota: A Proof-of-Concept Study
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Microbiota and Lifestyle: A Special Focus on Diet
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A novel gene cluster allows preferential utilization of fucosylated milk oligosaccharides in Bifidobacterium longum subsp. longum SC596
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The Impact of the Milk Glycobiome on the Neonate Gut Microbiota
Pacheco, A. R., Barile, D., Underwood, M. A., & Mills, D. A. (2014) · Annual Review of Animal Biosciences · doi:10.1146/annurev-animal-022114-111112 · Cited by 182 · see citing works
The Preterm Gut Microbiota: An Inconspicuous Challenge in Nutritional Neonatal Care
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Oligosaccharides Released from Milk Glycoproteins Are Selective Growth Substrates for Infant-Associated Bifidobacteria
Karav, S., Parc, A. L., Bell, J. M. L. N. D. M., Frese, S. A., Kirmiz, N., Block, D. E., Barile, D., & Mills, D. A. (2016) · Applied and Environmental Microbiology · doi:10.1128/aem.00547-16 · Cited by 169 · see citing works
Associations between Gut Microbial Colonization in Early Life and Respiratory Outcomes in Cystic Fibrosis
Hoen, A. G., Li, J., Moulton, L. A., O’Toole, G. A., Housman, M. L., Koestler, D. C., Guill, M. F., Moore, J. H., Hibberd, P. L., Morrison, H. G., et al. (2015) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2015.02.049 · Cited by 165 · see citing works
Cultivating Healthy Growth and Nutrition through the Gut Microbiota
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Akkermansia muciniphila uses human milk oligosaccharides to thrive in the early life conditions in vitro
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Fecal Short-Chain Fatty Acid Variations by Breastfeeding Status in Infants at 4 Months: Differences in Relative versus Absolute Concentrations
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Article Commentary: The Influence of Early Infant-Feeding Practices on the Intestinal Microbiome and Body Composition in Infants
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Enzymatic and cell factory approaches to the production of human milk oligosaccharides
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Human milk oligosaccharides and infant gut microbiota: Molecular structures, utilization strategies and immune function
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Bifidobacterium bifidum Enhances the Intestinal Epithelial Tight Junction Barrier and Protects against Intestinal Inflammation by Targeting the Toll-like Receptor-2 Pathway in an NF-κB-Independent Manner
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Comparative genomics of the Bifidobacterium brevetaxon
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Exploring the role of the microbiota member Bifidobacterium in modulating immune-linked diseases
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Utilization of Host-Derived Glycans by Intestinal Lactobacillus and Bifidobacterium Species
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Gold standard for nutrition: a review of human milk oligosaccharide and its effects on infant gut microbiota
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Linking human milk oligosaccharide metabolism and early life gut microbiota: bifidobacteria and beyond
Lordan, C., Roche, A. K., Delsing, D. J. M., Nauta, A., Groeneveld, A., MacSharry, J. A., Cotter, P. D., & van Sinderen, D. (2024) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00094-23 · Cited by 113 · see citing works
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
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Identification of Oligosaccharides in Feces of Breast-fed Infants and Their Correlation with the Gut Microbial Community
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Characterization of goat milk lactoferrin N‐glycans and comparison with the N‐glycomes of human and bovine milk
Parc, A. L., Dallas, D. C., Duaut, S., Léonil, J., Martin, P., & Barile, D. (2014) · Electrophoresis · doi:10.1002/elps.201300619 · Cited by 88 · see citing works
Dosing a synbiotic of human milk oligosaccharides and B. infantis leads to reversible engraftment in healthy adult microbiomes without antibiotics
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A Milk‐Oriented Microbiota (MOM) in Infants: Lessons from Your Other MOM
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Authors: Garrido, D., Dallas, D. C., & Mills, D. A.
Affiliations: University of California, Davis (US)
ORCID: Garrido, Daniel
Dallas, David C.
Mills, David A.
Venue: Microbiology
Publisher: Microbiology Society
Published: 2013-04-01
Volume: 159
Issue: Pt_4
Pages: 649-664
ISSN: 1350-0872 (ISSN-L)
1465-2080
DOI: 10.1099/mic.0.064113-0
PMC: PMC4083661
OpenAlex: W2147201779
Cited by: 228
References: 194
Citations by year: 2026: 3 · 2025: 10 · 2024: 13 · 2023: 10 · 2022: 22 · 2021: 20 · 2020: 28 · 2019: 20 · 2018: 18 · 2017: 24 · 2016: 15 · 2015: 25 · 2014: 16 · 2013: 4
FWCI: 2.25
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Microbiology (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Bill and Melinda Gates Foundation
California Dairy Research Foundation
National Institutes of Health
University of California, Davis
National Center for Complementary and Integrative Health (R01AT007079, R21AT006180)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD065122, R01HD061923, R01HD059127)
Topics: Health Sciences › Nursing › Nutrition and Dietetics › Infant Nutrition and Health
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
Keywords: human milk oligosaccharides, Bifidobacterium, glycosylated proteins, colonic fermentation, infant gut colonization, bioactive milk components
MeSH terms: Bifidobacterium, Female, Glycoconjugates, Humans, Infant, Infant, Newborn, Milk, Human, Gastrointestinal Tract

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Consumption of human milk glycoconjugates by infant-associated bifidobacteria: mechanisms and implications

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