Trophic Interactions of Infant Bifidobacteria and Eubacterium hallii during L-Fucose and Fucosyllactose Degradation

Abstract

Fucosyllactoses (2′- or 3′-FL) account for up to 20% of human milk oligosaccharides (HMOs). Infant bifidobacteria, such as Bifidobacterium longum subsp. infantis, utilize the lactose moiety to form lactate and acetate, and metabolize L-fucose to 1,2-propanediol (1,2-PD). Eubacterium hallii is a common member of the adult gut microbiota that can produce butyrate from lactate and acetate, and convert 1,2-PD to propionate. Recently, a Swiss cohort study identified E. hallii as one of the first butyrate producers in the infant gut. However, the global prevalence of E. hallii and its role in utilization of HMO degradation intermediates remains unexplored. Fecal 16S rRNA gene libraries (n = 857) of humans of all age groups from Venezuela, Malawi, Switzerland, and the USA were screened for the occurrence of E. hallii. Single and co-culture experiments of B. longum subsp. infantis and E. hallii were conducted in modified YCFA containing acetate and glucose, L-fucose, or FL. Bifidobacterium spp. (n = 56) of different origin were screened for the ability to metabolize L-fucose. Relative abundance of E. hallii was low (10−5–10−3%) during the first months but increased and reached adult levels (0.01–10%) at 5–10 years of age in all four populations. In single culture, B. longum subsp. infantis grew in the presence of all three carbohydrates while E. hallii was metabolically active only with glucose. In co-culture E. hallii also grew with L-fucose or FL. In co-cultures grown with glucose, acetate, and glucose were consumed and nearly equimolar proportions of formate and butyrate were formed. B. longum subsp. infantis used L-fucose and produced 1,2-PD, acetate and formate in a ratio of 1:1:1, while 1,2-PD was used by E. hallii to form propionate. E. hallii consumed acetate, lactate and 1,2-PD released by B. longum subsp. infantis from FL, and produced butyrate, propionate, and formate. Beside B. longum subsp. infantis, Bifidobacterium breve, and a strain of B. longum subsp. suis were able to utilize L-fucose. This study identified a trophic interaction of infant bifidobacteria and E. hallii during L-fucose degradation, and pointed at E. hallii as a metabolically versatile species that occurs in infants and utilizes intermediates of bifidobacterial HMO fermentation.

Bifidobacterium bifidum ATCC 15696 and Bifidobacterium breve 24b Metabolic Interaction Based on 2′- O -Fucosyl-Lactose Studied in Steady-State Cultures in a Freter-Style Chemostat

“…B. breve 24b grown as monoculture in fucose-containing medium produced 1,2-propanediol as a fermentation product (Fig. 5C), confirming previous observations of this species (17). However, 1,2-propanediol was not detected in steady-state 2FL cocultures.…”

“…Fucose is fermented to 1,2-propanediol by Bifidobacterium longum subspecies infantis and B. breve (17). The production of 1,2-propanediol by B. breve from fucose in batch culture but its absence in chemostat coculture with B. bifidum indicated that it might be used as a growth substrate by the latter species (a quid pro quo for fucose/lactose).…”

Breast milk-derived human milk oligosaccharides promote Bifidobacterium interactions within a single ecosystem

“…Quantified metabolic products indicates that fucose, acetate, pyruvate, and 1,2-propanediol are liberated from HMO degradation and could potentially function as candidates for cross-feeding. However, we did not see evidence of metabolism of these compounds by the B. longum strain as has been reported with other members of the infant microbiota; such as the 2′FL metabolic end product 1,2-propanediol which drives cross-feeding interactions between B. infantis and Eubacterium halli [52]. Recent work suggests that extracellular sialidases are the main source of crossfeeding interactions between bifidobacterial strains, as has been described for B. longum, which by producing sialylated carbohydrates and free sialic acid promotes B. breve growth [38,39].…”

Non-digestible carbohydrates in infant formula as substitution for human milk oligosaccharide functions: Effects on microbiota and gut maturation

“…Both butyric acid and propionate are important for gut health as they can interact with host epithelium to stimulate mucin release, increase mucosal blood flow and modulate the immune system (Pl€ oger et al 2012;Reichardt et al 2014). Schwab and colleagues (Schwab et al 2017) found a trophic interaction between Bifidobacteria and Eubacterium hallii (E. hallii), a common member of the adult gut microbiota, during L-fucose degradation. In a single culture E. hallii was not able to grow on L-fucose.…”