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

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.

Metabolic Fate and Distribution of 2´‐Fucosyllactose: Direct Influence on Gut Microbial Activity but not on Brain

“…Interestingly, 2´FL application to mice increases the levels of Barnesiella indicating that in mice 2´FL metabolization is a possible route to generate metabolites which could cross the intestinal barrier and accumulate in the circulation. In this context, the consumption of 2´FL by microbial species from the genera Barnesiella, Bifidobacterium , and Bacteroides may lead to the production of smaller molecules such as lactose, fucose or organic acids such as butyrate, acetate, or lactate . With regard to our experiments, we speculate that 13 C‐enrichment may reflect the presence of fucose itself or a fucose‐derived metabolite since the fucose moiety of 2´FL carried the 13 C‐labeling at the C 1 ‐atom and 2´FL itself could not pass the blood–brain barrier as has been shown by i.v.…”

Bifidobacterium longum subsp. infantis ATCC 15697 and Goat Milk Oligosaccharides Show Synergism In Vitro as Anti-Infectives against Campylobacter jejuni

“…infantis BRS8-2 and TPY1201 are known to degrade 2 FL, 3FL, 3 SL and LNnT, while B. longum subsp. infantis DSM 20088 has been shown to utilise 2 FL, 3FL, and LNnT [68]. Therefore, it is likely that the prebiotic effect associated with GMOs may extend to other strains.…”

Milk Glycans and Their Interaction with the Infant-Gut Microbiota

“…The genome of B. infantis ATCC 15697 possesses two gene clusters containing genes that are similar to a fucose pathway involving nonphosphorylated intermediates that have been previously described in C. jejuni and Xanthomonas campestris (Sela et al 2012, Yew et al 2006). Bunesova et al (2016) showed that fermentation end products lactate, acetate, and 1,2-propanediol were formed during growth of B. infantis and Bifidobacterium longum subsp. suis on L-fucose.…”

“…suis on L-fucose. This work proposed an L-fucose pathway similar to X. campestris and C. jejuni involving the formation of nonphosphorylated intermediates (Bunesova et al 2016). …”