Consumption of human milk oligosaccharides by gut-related microbes - PubMed (original) (raw)
Consumption of human milk oligosaccharides by gut-related microbes
Angela Marcobal et al. J Agric Food Chem. 2010.
Abstract
Human milk contains large amounts of complex oligosaccharides that putatively modulate the intestinal microbiota of breast-fed infants by acting as decoy binding sites for pathogens and as prebiotics for enrichment of beneficial bacteria. Several bifidobacterial species have been shown to grow well on human milk oligosaccharides. However, few data exist on other bacterial species. This work examined 16 bacterial strains belonging to 10 different genera for growth on human milk oligosaccharides. For this propose, a chemically defined medium, ZMB1, was used, which allows vigorous growth of a number of gut-related microorganisms in a fashion similar to complex media. Interestingly, Bifidobacterium longum subsp. infantis, Bacteroides fragilis , and Bacteroides vulgatus strains were able to metabolize milk oligosaccharides with high efficiency, whereas Enterococcus , Streptococcus , Veillonella , Eubacterium , Clostridium , and Escherichia coli strains grew less well or not at all. Mass spectrometry-based glycoprofiling of the oligosaccharide consumption behavior revealed a specific preference for fucosylated oligosaccharides by Bi. longum subsp. infantis and Ba. vulgatus. This work expands the current knowledge of human milk oligosaccharide consumption by gut microbes, revealing bacteroides as avid consumers of this substrate. These results provide insight on how human milk oligosaccharides shape the infant intestinal microbiota.
Figures
Figure 1
Human milk oligosaccharide consumption profiles of Bifidobacterium infantis, Bacteroides fragilis and Bacteroides vulgatus in modified ZMB1 (2% HMO), as determined using MALDI-FTICR MS. Asterisks represents number of fucose residues on the specific oligosaccharide depicted by the mass/charge ratio (m/z).
Figure 2
Annotated genes coding for some carbohydrate active enzymes in the genomes of Bacteroides fragilis ATCC25285, Bacteroides vulgatus ATCC8483, Bifidobacterium infantis ATCC15697 and Bifidobacterium longum DJO10A, as it is described at the CAZy database (
) (27). The glycoside hydrolase families (GHF) shown are potentially related to the degradation of HMOs, and they include the following activities: GH2, α-galactosidase; GH3, β-N-Acetylgalactosaminidase; GH20, β-hexosaminidase; GH27, α-N-acetylgalactosaminidase; GH29, α-L-fucosidase; GH33, sialidase; GH42, β-galactosidase; GH95, α-1,2-L-fucosidase.
Similar articles
- Galacto- and Fructo-oligosaccharides Utilized for Growth by Cocultures of Bifidobacterial Species Characteristic of the Infant Gut.
Sims IM, Tannock GW. Sims IM, et al. Appl Environ Microbiol. 2020 May 19;86(11):e00214-20. doi: 10.1128/AEM.00214-20. Print 2020 May 19. Appl Environ Microbiol. 2020. PMID: 32220841 Free PMC article. - Variation in consumption of human milk oligosaccharides by infant gut-associated strains of Bifidobacterium breve.
Ruiz-Moyano S, Totten SM, Garrido DA, Smilowitz JT, German JB, Lebrilla CB, Mills DA. Ruiz-Moyano S, et al. Appl Environ Microbiol. 2013 Oct;79(19):6040-9. doi: 10.1128/AEM.01843-13. Epub 2013 Jul 26. Appl Environ Microbiol. 2013. PMID: 23892749 Free PMC article. - Selective Utilization of the Human Milk Oligosaccharides 2'-Fucosyllactose, 3-Fucosyllactose, and Difucosyllactose by Various Probiotic and Pathogenic Bacteria.
Salli K, Hirvonen J, Siitonen J, Ahonen I, Anglenius H, Maukonen J. Salli K, et al. J Agric Food Chem. 2021 Jan 13;69(1):170-182. doi: 10.1021/acs.jafc.0c06041. Epub 2020 Dec 31. J Agric Food Chem. 2021. PMID: 33382612 - A molecular basis for bifidobacterial enrichment in the infant gastrointestinal tract.
Garrido D, Barile D, Mills DA. Garrido D, et al. Adv Nutr. 2012 May 1;3(3):415S-21S. doi: 10.3945/an.111.001586. Adv Nutr. 2012. PMID: 22585920 Free PMC article. Review. - Human milk oligosaccharides: the novel modulator of intestinal microbiota.
Jeong K, Nguyen V, Kim J. Jeong K, et al. BMB Rep. 2012 Aug;45(8):433-41. doi: 10.5483/BMBRep.2012.45.8.168. BMB Rep. 2012. PMID: 22917027 Review.
Cited by
- The Role of Milk Oligosaccharides in Enhancing Intestinal Microbiota, Intestinal Integrity, and Immune Function in Pigs: A Comparative Review.
Gormley A, Garavito-Duarte Y, Kim SW. Gormley A, et al. Biology (Basel). 2024 Aug 26;13(9):663. doi: 10.3390/biology13090663. Biology (Basel). 2024. PMID: 39336091 Free PMC article. Review. - Determining the metabolic fate of human milk oligosaccharides: it may just be more complex than you think?
Jackson PPJ, Wijeyesekera A, Rastall RA. Jackson PPJ, et al. Gut Microbiome (Camb). 2022 Sep 7;3:e9. doi: 10.1017/gmb.2022.8. eCollection 2022. Gut Microbiome (Camb). 2022. PMID: 39295778 Free PMC article. Review. - Structural Characterization and Abundance of Sialylated Milk Oligosaccharides in Holstein Cows during Early Lactation.
Isernhagen L, Galuska CE, Vernunft A, Galuska SP. Isernhagen L, et al. Foods. 2024 Aug 7;13(16):2484. doi: 10.3390/foods13162484. Foods. 2024. PMID: 39200411 Free PMC article. - Metatranscriptomic analysis indicates prebiotic effect of isomalto/malto-polysaccharides on human colonic microbiota in-vitro.
Borewicz K, Hornung B, Gu F, van der Zaal PH, Schols HA, Schaap PJ, Smidt H. Borewicz K, et al. Sci Rep. 2024 Aug 14;14(1):18866. doi: 10.1038/s41598-024-69685-w. Sci Rep. 2024. PMID: 39143192 Free PMC article. - Comparison of gnotobiotic communities reveals milk-adapted metabolic functions and unexpected amino acid metabolism by the pre-weaning microbiome.
Lubin JB, Silverman MA, Planet PJ. Lubin JB, et al. Gut Microbes. 2024 Jan-Dec;16(1):2387875. doi: 10.1080/19490976.2024.2387875. Epub 2024 Aug 12. Gut Microbes. 2024. PMID: 39133869 Free PMC article.
References
- Kunz C, Rudloff S, Baier W, Klein N, Strobel S. Oligosaccharides in human milk: Structural, functional, and metabolic aspects. Annu. Rev.Nutr. 2000;20:699–722. - PubMed
- Ninonuevo MR, Park Y, Yin HF, Zhang JH, Ward RE, Clowers BH, German JB, Freeman SL, Killeen K, Grimm R, Lebrilla CB. A strategy for annotating the human milk glycome. J. Agric.Food Chem. 2006;54:7471–7480. - PubMed
- Newburg DS, Ruiz-Palacios GM, Morrow AL. Human milk glycans protect infants against enteric pathogens. Annu. Rev.Nutr. 2005;25:37–58. - PubMed
- Chaturvedi P, Warren CD, Buescher CR, Pickering LK, Newburg DS. Bioactive Components of Human Milk. Vol. 501. New York: Kluwer Academic/Plenum Publ; 2001. Survival of human milk oligosaccharides in the intestine of infants; pp. 315–323. - PubMed
- Engfer MB, Stahl B, Finke B, Sawatzki G, Daniel H. Human milk oligosaccharides are resistant to enzymatic hydrolysis in the upper gastrointestinal tract. Am. J. Clin. Nutr. 2000;71:1589–1596. - PubMed
Publication types
MeSH terms
Substances
Grants and funding
- R01 HD059127/HD/NICHD NIH HHS/United States
- R01 HD061923/HD/NICHD NIH HHS/United States
- R01 HD061923-01/HD/NICHD NIH HHS/United States
- HD059127/HD/NICHD NIH HHS/United States
LinkOut - more resources
Full Text Sources
Other Literature Sources