Two extracellular sialidases from Bifidobacterium bifidum promote the degradation of sialyl-oligosaccharides and support the growth of Bifidobacterium breve

Nishiyama, Keita; Nagai, Aki; Uribayashi, Kazuya; Yamamoto, Yuji; Mukai, T.; Okada, Nobuhiko

doi:10.1016/j.anaerobe.2018.05.007

Cited by 52 publications

(49 citation statements)

References 37 publications

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“…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]. Currently there is little evidence suggesting cooperation between non-extracellular HMO degraders.…”

Section: Discussionmentioning

confidence: 76%

“…The use of key metabolites produced from HMO degradation from one species of Bifidobacterium to another, highlights a potential way to permit growth of multiple different bifidobacterial species and strains within the breast-fed infant gut [13,27,38]. Moreover, a cooperative balance between bifidobacterial strains in the early-life microbiota [51] may further enhance their dominance in breast-fed infants by enabling a genus-specific exploitative competition i.e., depleting the GI tract of breast milk-derived nutrients, thereby preventing colonisation of other microbes, including pathobionts.…”

Section: Discussionmentioning

confidence: 99%

“…HMOs that are sialylated require sialidase enzymes for degradation such as the extracellular sialidase (SiaBb1) found in B. bifidum ATCC 15696 that permits sialylated HMOs digestion on the bacterial cell surface [38,39] GH1 GH2 GH3 GH4 GH5 GH8 GH10 GH13 GH18 GH20 GH23 GH25 GH27 GH29 GH30 GH31 GH32 GH33 GH35 GH36 GH38 GH42 GH43 GH51 GH53 GH77 GH78 GH85 GH95 GH101 GH109 GH112 GH120 GH121 GH123 GH125 GH127 GH129 GH136 0 5 Supplementary Fig. 4B)…”

Section: Functional Annotation Of Genomes Of Bifidobacterium From Infmentioning

confidence: 99%

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

et al. 2019

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Diet-microbe interactions play an important role in modulating the early-life microbiota, with Bifidobacterium strains and species dominating the gut of breast-fed infants. Here, we sought to explore how infant diet drives distinct bifidobacterial community composition and dynamics within individual infant ecosystems. Genomic characterisation of 19 strains isolated from breast-fed infants revealed a diverse genomic architecture enriched in carbohydrate metabolism genes, which was distinct to each strain, but collectively formed a pangenome across infants. Presence of gene clusters implicated in digestion of human milk oligosaccharides (HMOs) varied between species, with growth studies indicating that within single infants there were differences in the ability to utilise 2′FL and LNnT HMOs between strains. Cross-feeding experiments were performed with HMO degraders and non-HMO users (using spent or 'conditioned' media and direct co-culture). Further 1 H-NMR analysis identified fucose, galactose, acetate, and N-acetylglucosamine as key by-products of HMO metabolism; as demonstrated by modest growth of non-HMO users on spend media from HMO metabolism. These experiments indicate how HMO metabolism permits the sharing of resources to maximise nutrient consumption from the diet and highlights the cooperative nature of bifidobacterial strains and their role as 'foundation' species in the infant ecosystem. The intra-and inter-infant bifidobacterial community behaviour may contribute to the diversity and dominance of Bifidobacterium in early life and suggests avenues for future development of new diet and microbiota-based therapies to promote infant health.

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Section: Discussionmentioning

confidence: 76%

Section: Discussionmentioning

confidence: 99%

Section: Functional Annotation Of Genomes Of Bifidobacterium From Infmentioning

confidence: 99%

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

et al. 2019

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“…These efforts have illustrated how B. bifidum extracellularly degrades HMOs and mucin O-glycans into smaller sugars by the concerted action of the many cell surface-anchored GHs summarized in Figure 1. Terminal modifications such as fucosylation and sialylation can be removed by either a GH95 1,2-α-l-fucosidase (AfcA) [56,67], a GH29 1,3-1,4-α-l-fucosidase (AfcB) [62], or a GH33 sialidases (SiaBb1 [65,68] and SiaBb2 [42,60]) to expose the internal core structures. The internal type-1/2 LacNAc units are removed by GH20 lacto-N-biosidase (LnbB) to liberate LNB [66] and by a sequential digestion with GH2 β-galactosidase, BbgIII [63], and GH20 β-N-acetylhexosaminidase, BbhI, to liberate Gal and GlcNAc [63], respectively.…”

Section: Glycoside Hydrolases Involved In the Degradation Of Hmos/mucmentioning

confidence: 99%

Enzymatic Adaptation of Bifidobacterium bifidum to Host Glycans, Viewed from Glycoside Hydrolyases and Carbohydrate-Binding Modules

et al. 2020

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Certain species of the genus Bifidobacterium represent human symbionts. Many studies have shown that the establishment of symbiosis with such bifidobacterial species confers various beneficial effects on human health. Among the more than ten (sub)species of human gut-associated Bifidobacterium that have significantly varied genetic characteristics at the species level, Bifidobacterium bifidum is unique in that it is found in the intestines of a wide age group, ranging from infants to adults. This species is likely to have adapted to efficiently degrade host-derived carbohydrate chains, such as human milk oligosaccharides (HMOs) and mucin O-glycans, which enabled the longitudinal colonization of intestines. The ability of this species to assimilate various host glycans can be attributed to the possession of an adequate set of extracellular glycoside hydrolases (GHs). Importantly, the polypeptides of those glycosidases frequently contain carbohydrate-binding modules (CBMs) with deduced affinities to the target glycans, which is also a distinct characteristic of this species among members of human gut-associated bifidobacteria. This review firstly describes the prevalence and distribution of B. bifidum in the human gut and then explains the enzymatic machinery that B. bifidum has developed for host glycan degradation by referring to the functions of GHs and CBMs. Finally, we show the data of co-culture experiments using host-derived glycans as carbon sources, which underpin the interesting altruistic behavior of this species as a cross-feeder.

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“…Nevertheless, cross-feeding of human-derived glycans has been shown only for the species B. bifidum and B. breve through batch cultivation on a limited number of substrates, i.e. mucin and 6 0 sialyllactose (Egan et al, 2014a,b;Nishiyama et al, 2018). For this reason, in order to obtain a comprehensive and accurate overview of cross-feeding interactions between B. bifidum PRL2010 and other co-occurring key members of the infant bifidobacterial population, we developed a bioreactor model using human milk as growth substrate.…”

Section: Cross-feeding Activities Between B Bifidum Prl2010 and Othementioning

confidence: 99%

Bifidobacterium bifidum and the infant gut microbiota: an intriguing case of microbe‐host co‐evolution

Duranti

Lugli

Milani

et al. 2019

Environmental Microbiology

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Summary Bifidobacterium bifidum is reported to be among the first colonizers of the newborn's gastrointestinal tract due to its ability to metabolize human milk oligosaccharides (HMOs). In order to investigate biological features that allow this bifidobacterial species to colonize a newborn, bifidobacterial internally transcribed spacer profiling of stool samples of 50 mother‐infant dyads, as well as corresponding breastmilk samples, was performed. Hierarchical clustering based on bifidobacterial population profiles found in infant faecal samples revealed the presence of four bifidobacterial clusters or the so‐called bifidotypes. Bifidobacterium bifidum was shown to be a key member among bifidotypes, in which its presence correlate with several different bifidobacterial species retrieved in infant faecal samples. For this reason, we investigated cross‐feeding behaviour facilitated by B. bifidum on a bioreactor model using human milk as growth substrate. Transcriptional profiles of this strain were evaluated when grown on nine specific glycans typically constituting HMOs. Remarkably, these analyses suggest extensive co‐evolution with the host and other bifidobacterial species in terms of resource provision and sharing, respectively, activities that appear to support a bifidobacteria‐dominant microbiome.

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Two extracellular sialidases from Bifidobacterium bifidum promote the degradation of sialyl-oligosaccharides and support the growth of Bifidobacterium breve

Cited by 52 publications

References 37 publications

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

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

Enzymatic Adaptation of Bifidobacterium bifidum to Host Glycans, Viewed from Glycoside Hydrolyases and Carbohydrate-Binding Modules

Bifidobacterium bifidum and the infant gut microbiota: an intriguing case of microbe‐host co‐evolution

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