Abstract
Gut microbiota of breast-fed infants are generally rich in bifidobacteria. Recent studies show that infant gut-associated bifidobacteria can assimilate human milk oligosaccharides (HMOs) specifically among the gut microbes. Nonetheless, little is known about how bifidobacterial-rich communities are shaped in the gut. Interestingly, HMOs assimilation ability is not related to the dominance of each species. Bifidobacterium longum susbp. longum and Bifidobacterium breve are commonly found as the dominant species in infant stools; however, they show limited HMOs assimilation ability in vitro. In contrast, avid in vitro HMOs consumers, Bifidobacterium bifidum and Bifidobacterium longum subsp. infantis, are less abundant in infant stools. In this study, we observed altruistic behaviour by B. bifidum when incubated in HMOs-containing faecal cultures. Four B. bifidum strains, all of which contained complete sets of HMO-degrading genes, commonly left HMOs degradants unconsumed during in vitro growth. These strains stimulated the growth of other Bifidobacterium species when added to faecal cultures supplemented with HMOs, thereby increasing the prevalence of bifidobacteria in faecal communities. Enhanced HMOs consumption by B. bifidum-supplemented cultures was also observed. We also determined the complete genome sequences of B. bifidum strains JCM7004 and TMC3115. Our results suggest B. bifidum-mediated cross-feeding of HMOs degradants within bifidobacterial communities.
Highlights
Gut microbiota of breast-fed infants are generally rich in bifidobacteria
Our understanding of the human milk oligosaccharides (HMOs) degradation pathway in bifidobacteria is incomplete, it appears that B. bifidum and LnbX-positive B. longum use extracellular hydrolases, while B. breve, B. infants, and LnbX-negative B. longum rely on oligosaccharide transporters[21]
We found that the culture supernatant of early exponential phase of B. bifidum JCM1254 grown in the presence of HMOs contained significant amounts of lacto-N-biose I (LNB: Galβ1-3GlcNAc) and lactose (Lac: Galβ1-4Glc), which are produced from lacto-N-tetraose (LNT: Galβ1-3GlcNAcβ1-3Galβ1-4Glc, the most abundant HMO core structure) by lacto-N-biosidase (LnbB)[22]
Summary
Gut microbiota of breast-fed infants are generally rich in bifidobacteria. Recent studies show that infant gut-associated bifidobacteria can assimilate human milk oligosaccharides (HMOs) among the gut microbes. It should be noted that the occurrence of lnbX in B. longum is strain-dependent, and less than half of the genome-sequenced B. longum strains contain the gene These results strongly suggest that HMOs serve as a selective pressure for the formation of the gut microbiota, which could be driven by HMO-mediated symbiosis between certain bifidobacteria and humans. LnbX-positive B. longum JCM1217 transiently released Lac into the culture Given these results, we hypothesised that the HMOs degradants may be symbiotically shared among different species of Bifidobacterium in the gut community, as LNB, Lac, and Gal serve as good carbon sources[16,22]. The relationship was absent in the stools of formula-fed babies These results imply cross-feeding of HMOs degradants produced by B. bifidum within the bifidobacterial community of the gut. The results suggest that extracellular glycosidase-dependent bifidobacterial species may act in an altruistic manner, while oligosaccharide transporter-dependent bifidobacterial species appear more selfish
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