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Relative fermentation of oligosaccharides from human milk and plants by gut microbes

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Abstract

Gut microbiota is important to human health. Specific dietary glycans promote favorable microbiota growth and inhibit pathobionts. Dietary glycans most relevant to adults and weaned infants are derived from plants or lactose; human milk oligosaccharides (HMOS) are most relevant to breastfed infants. Their efficacy in supporting bacterial growth is compared to determine their potential roles in the initiation and maintenance of colonization. Bioactivities of gluco-manno-oligosaccharides (GMOS), galacto-oligosaccharides (GOS), xylo-oligosaccharides (XOS), cellobiose (CBS), HMOS, and the most prominent individual HMOS, 2′-fucosyllactose (2′-FL) were contrasted. Two representative gut microbiota mutualists, Bifidobacteria longum ATCC15697 and Lactobacillus acidophilus NRRL B-4495, and two non-mutualists, Campylobacter jejuni S107 and Escherichia coli K12, were used to assess the in vitro prebiotic potential of these oligosaccharides. All oligosaccharides afforded growth of B. longum and L. acidophilus, with HMOS supporting the most robust growth, while none of these oligosaccharides afforded meaningful growth of non-mutualists. B. longum efficiently converted HMOS, GMOS, GOS, and XOS into organic acid fermentation products, and, to a lesser degree, L. acidophilus metabolized HMOS, GMOS, and GOS. Fermentation of these glycans by C. jejuni and E. coli was sparse. B. longum fermentation products inhibited C. jejuni and E. coli. Thus, HMOS most strongly promoted growth of the two mutualists, and both HMOS and GMOS were efficiently fermented by these mutualists into organic acids. This is consistent with a primary role of HMOS in guiding early colonization of the infant microbiota by mutualist symbionts, and of plant oligosaccharides, especially GMOS, in maintaining a favorable microbiota through adulthood.

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Abbreviations

HMOS:

Human milk oligosaccharides

GMOS:

Gluco-manno-oligosaccharides

GOS:

Galacto-oligosaccharides

XOS:

Xylo-oligosaccharides

2′-FL:

2′-fucosyllactose

CBS:

Cellobiose

B. longum ATCC15697:

Bifidobacteria longum ATCC15697

L. acidophilus NRRL B-4495:

Lactobacillus acidophilus NRRL B-4495

C. jejuni S107:

Campylobacter jejuni S107

E. coli K12:

Escherichia coli K12

3-FL:

3-fucosyllactose

LNT/LNnT:

Lacto-N-tetraose/lacto-N-neotetraose

LNFP:

Lacto-N-fucopentaose

LDFT:

Lactodifucotetraose

LNDFH:

Lacto-N-difucohexaose

M2:

Mannobiose

M3:

Mannotriose

M4:

Mannotetraose

M5:

Mannopentaose

M6:

Mannohexaose

X2:

Xylobiose

X3:

Xylotriose

X4:

Xylotetraose

X5:

Mannopentaose

X6:

Xylohexaose

LC–MS:

Liquid chromatography–mass spectrometry

AA:

Acetic acid

PA:

Propionic acid

BA:

Butyric acid

LA:

Lactic acid

VA:

Valoric acid

HA:

Hexanic acid

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Acknowledgments

This work was supported in part by the National Institutes of Health grant number R01HD059140 (DSN), U01AI075563 (DSN) and P01HD013021 (DSN). Wang’s study was also supported by the Governmental Public Industry Research Special Funds for Projects (Grant No. 201404615), Graduate Research Innovation Projects of Jiangsu Province Ordinary University (CXZZ13_0545), and the Priority Academic Program Development of Jiangsu Higher Education Institution (PAPD).

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Authors and Affiliations

  1. College of Chemical Engineering, Nanjing Forestry University, Nanjing, 210037, People’s Republic of China

    Jing Wang & Qiang Yong

  2. Department of Biology, Boston College, Chestnut Hill, MA, 02367, USA

    Jing Wang, Ceng Chen, Zhuoteng Yu, Yingying He & David S. Newburg

  3. Program in Glycobiology, Boston College, Chestnut Hill, MA, 02467, USA

    David S. Newburg

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  1. Jing Wang
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  2. Ceng Chen
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  3. Zhuoteng Yu
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Correspondence to David S. Newburg.

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Conflict of interest

D.S.N. owns stock in Glycosyn, LLC, which makes human milk oligosaccharides. This potential competing financial interest is managed by Boston College. J.W., C.C., Z.Y., Y.H., and Q.Y. declare no potential conflicts of interest.

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Wang, J., Chen, C., Yu, Z. et al. Relative fermentation of oligosaccharides from human milk and plants by gut microbes. Eur Food Res Technol 243, 133–146 (2017). https://doi.org/10.1007/s00217-016-2730-0

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