Fucosyllactose and L-fucose utilization of infant Bifidobacterium longum and Bifidobacterium kashiwanohense.

Vera Bunesova,Christophe Lacroix,Clarissa Schwab

doi:10.1186/s12866-016-0867-4

Abstract

BackgroundHuman milk oligosaccharides (HMOs) are one of the major glycan source of the infant gut microbiota. The two species that predominate the infant bifidobacteria community, Bifidobacterium longum subsp. infantis and Bifidobacterium bifidum, possess an arsenal of enzymes including α-fucosidases, sialidases, and β-galactosidases to metabolise HMOs. Recently bifidobacteria were obtained from the stool of six month old Kenyan infants including species such as Bifidobacterium kashiwanohense, and Bifidobacterium pseudolongum that are not frequently isolated from infant stool.The aim of this study was to characterize HMOs utilization by these isolates. Strains were grown in presence of 2′-fucosyllactose (2′-FL), 3′-fucosyllactose (3′-FL), 3′-sialyl-lactose (3′-SL), 6′-sialyl-lactose (6′-SL), and Lacto-N-neotetraose (LNnT). We further investigated metabolites formed during L-fucose and fucosyllactose utilization, and aimed to identify genes and pathways involved through genome comparison.Results Bifidobacterium longum subsp. infantis isolates, Bifidobacterium longum subsp. suis BSM11-5 and B. kashiwanohense strains grew in the presence of 2′-FL and 3′- FL. All B. longum isolates utilized the L-fucose moiety, while B. kashiwanohense accumulated L-fucose in the supernatant. 1,2-propanediol (1,2-PD) was the major metabolite from L-fucose fermentation, and was formed in equimolar amounts by B. longum isolates.Alpha-fucosidases were detected in all strains that degraded fucosyllactose. B. longum subsp. infantis TPY11-2 harboured four α-fucosidases with 95–99 % similarity to the type strain. B. kashiwanohense DSM 21854 and PV20-2 possessed three and one α-fucosidase, respectively. The two α-fucosidases of B. longum subsp. suis were 78–80 % similar to B. longum subsp. infantis and were highly similar to B. kashiwanohense α-fucosidases (95–99 %). The genomes of B. longum strains that were capable of utilizing L-fucose harboured two gene regions that encoded enzymes predicted to metabolize L-fucose to L-lactaldehyde, the precursor of 1,2-PD, via non-phosphorylated intermediates.ConclusionHere we observed that the ability to utilize fucosyllactose is a trait of various bifidobacteria species. For the first time, strains of B. longum subsp. infantis and an isolate of B. longum subsp. suis were shown to use L-fucose to form 1,2-PD. As 1,2-PD is a precursor for intestinal propionate formation, bifidobacterial L-fucose utilization may impact intestinal short chain fatty acid balance. A L-fucose utilization pathway for bifidobacteria is suggested.Electronic supplementary materialThe online version of this article (doi:10.1186/s12866-016-0867-4) contains supplementary material, which is available to authorized users.

Highlights

Human milk oligosaccharides (HMOs) are one of the major glycan source of the infant gut microbiota
B. longum subsp. infantis utilized of 2′-FL, 3′-FL, 3′SL and LNnT and degraded all HMOs when supplied together
Strains of B. bifidum liberated L-fucose and a second degradation product (Fig. 1, peak y) in the supernatant when grown in the presence of fucosyllactose while L-fucose accumulation or the release of any other degradation intermediate was not observed for B. longum subsp. infantis strains [28] (Fig. 1)

Summary

Introduction

Human milk oligosaccharides (HMOs) are one of the major glycan source of the infant gut microbiota. The two species that predominate the infant bifidobacteria community, Bifidobacterium longum subsp. Bifidobacteria are highly specialized organisms in using non-digestible oligosaccharides and a major part of their genomes is devoted to the utilization of carbon sources [1,2,3,4,5]. Host-specific adaption in regard to carbohydrate degradation has been suggested [7, 8] Adult species, such as Bifidobacterium adolescentis and Bifidobacterium longum subsp. Longum, are well equipped to degrade plant derived polysaccharides [4, 9] Infant species, such as Bifidobacterium longum subsp. Infantis and Bifidobacterium bifidum, are adapted to utilize human milk oligosaccharides (HMOs), one of the major glycan sources of breast milk [3, 10,11,12]. Lactose can be elongated with units of N-acetyllactosamine (Gal-β1-4GlcNAc) with its simplest form being Lacto-N-neotetraose (LNnT) [13]

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