Investigating bifidobacteria and human milk oligosaccharide composition of lactating mothers
Gabriele Andrea LugliSabrina DurantiChristian MilaniLeonardo MancabelliFrancesca TurroniGiulia AlessandriGiulia LonghiRosaria AnzaloneAlice ViappinaiChiara TarracchiniSergio BernasconiChloe YonemitsuLars BodeMichael I. GoranMaria Cristina OssiprandiDouwe van SinderenMarco Ventura
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ABSTRACT Human milk is known to carry its own microbiota, of which the precise origin remains obscure. Breastfeeding allows mother-to-baby transmission of microorganisms as well as the transfer of many other milk components, such as human milk oligosaccharides (HMOs), which act as metabolizable substrates for particular bacteria, such as bifidobacteria, residing in infant intestinal tract. In the current study, we report the HMO composition of 249 human milk samples, in 163 of which we quantified the abundance of members of the Bifidobacterium genus using a combination of metagenomic and flow cytometric approaches. Metagenomic data allowed us to identify four clusters dominated by Bifidobacterium adolescentis and Bifidobacterium pseudolongum, Bifidobacterium crudilactis or Bifidobacterium dentium, as well as a cluster represented by a heterogeneous mix of bifidobacterial species such as Bifidobacterium breve and Bifidobacterium longum. Furthermore, in vitro growth assays on HMOs coupled with in silico glycobiome analyses allowed us to elucidate that members of the Bifidobacterium bifidum and B. breve species exhibit the greatest ability to degrade and grow on HMOs. Altogether, these findings indicate that the bifidobacterial component of the human milk microbiota is not strictly correlated with their ability to metabolize HMOs.Keywords:
Bifidobacterium longum
Bifidobacterium breve
Bifidobacterium bifidum
Actinomycetaceae
Human gastrointestinal tract
Bifidobacterium longum
Actinomycetaceae
Bifidobacterium bifidum
Bifidobacterium breve
Fermented Milk Products
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Bifidobacterium breve
Bifidobacterium longum
Actinomycetaceae
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Following an application from Topfer GmbH submitted pursuant to Article 14 of Regulation (EC) No 1924/2006 via the Competent Authority of Germany, the Panel on Dietetic Products, Nutrition and Allergies was asked to deliver an opinion on the scientific substantiation of a health claim related to a combination of bifidobacteria (Bifidobacterium bifidum, Bifidobacterium breve, Bifidobacterium infantis, Bifidobacterium longum) and decreasing potentially pathogenic intestinal microorganisms. The scope of the application was proposed to fall under a health claim referring to children's development and health. The food constituent that is the subject of the proposed claim, a combination of Bifidobacterium bifidum, Bifidobacterium breve, Bifidobacterium infantis, Bifidobacterium longum, has not been sufficiently characterised. The claimed effect is “establishment of a natural, beneficial bifidobacterial dominance in the large intestine, which can lead to a suppression of harmful bacteria and thereby to a better health status”. The target population is infants and children aged between 0 to 36 months. The Panel considers that decreasing potentially pathogenic intestinal microorganisms might be beneficial to human health. The applicant identified a total of 34 publications considered as being pertinent to the health claim. In weighing the evidence, the Panel notes that the strains that are the subject of the health claim have not been sufficiently characterised and that from the evidence provided it cannot be established that the strains used in the studies are the same strains that are the subject of the claim.
Bifidobacterium longum
Bifidobacterium bifidum
Bifidobacterium breve
Actinomycetaceae
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Bifidobacterium bifidum
Bifidobacterium longum
Bifidobacterium breve
Actinomycetaceae
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Bifidobacterium longum
Bifidobacterium bifidum
Bifidobacterium animalis
Bifidobacterium breve
Actinomycetaceae
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Bifidobacterium bifidum
Bifidobacterium breve
Bifidobacterium longum
Lactobacillus rhamnosus
Actinomycetaceae
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Importance of bifidobacteria as part of the infant intestinal microbiota has been highlighted. Their acquisition is influenced by the mode of birth and the feed regime afterwards, with a special role of the maternal microbiota. The presence of the same shared bifidobacterial strains between breast milk and infant faeces in 14 mother-infant pairs was assessed by means of pulsed-field gel electrophoresis (PFGE) genotyping. Four shared strains of Bifidobacterium breve (2), Bifidobacterium longum subsp. infantis and B. longum subsp. longum were found in breast milk-infant faeces pairs. Two years later, a second survey yielded four shared strains of the species Bifidobacterium adolescentis , Bifidobacterium bifidum , B. longum subsp. longum and Bifidobacterium pseudocatenulatum . Moreover, a B. bifidum strain was found to be shared by the infant faeces of the first study and the mother faeces tested two years later, pointing out a long term persistence. Some of the selected bifidobacterial strains showed probiotic potential due to their survival to gastrointestinal conditions and their ability to form biofilms.
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Extracellular proteins are important factors in host-microbe interactions; however, the specific factors that enable bifidobacterial adhesion and survival in the gastrointestinal (GI) tract are not fully characterized. Here, we discovered that Bifidobacterium longum NCC2705 cultured in bacterium-free supernatants of human fecal fermentation broth released a myriad of particles into the extracellular environment. The aim of this study was to characterize the physiological properties of these extracellular particles. The particles, approximately 50 to 80 nm in diameter, had high protein and double-stranded DNA contents, suggesting that they were extracellular vesicles (EVs). A proteomic analysis showed that the EVs primarily consisted of cytoplasmic proteins with crucial functions in essential cellular processes. We identified several mucin-binding proteins by performing a biomolecular interaction analysis of phosphoketolase, GroEL, elongation factor Tu (EF-Tu), phosphoglycerate kinase, transaldolase (Tal), and heat shock protein 20 (Hsp20). The recombinant GroEL and Tal proteins showed high binding affinities to mucin. Furthermore, the immobilization of these proteins on microbeads affected the permanence of the microbeads in the murine GI tract. These results suggest that bifidobacterial exposure conditions that mimic the intestine stimulate B. longum EV production. The resulting EVs exported several cytoplasmic proteins that may have promoted B. longum adhesion. This study improved our understanding of the Bifidobacterium colonization strategy in the intestinal microbiome.IMPORTANCEBifidobacterium is a natural inhabitant of the human gastrointestinal (GI) tract. Morphological observations revealed that extracellular appendages of bifidobacteria in complex microbial communities are important for understanding its adaptations to the GI tract environment. We identified dynamic extracellular vesicle (EV) production by Bifidobacterium longum in bacterium-free fecal fermentation broth that was strongly suggestive of differing bifidobacterial extracellular appendages in the GI tract. In addition, export of the adhesive moonlighting proteins mediated by EVs may promote bifidobacterial colonization. This study provides new insight into the roles of EVs in bifidobacterial colonization processes as these bacteria adapt to the GI environment.
Bifidobacterium longum
Extracellular Vesicles
Actinomycetaceae
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The bifidogenic effect of human milk oligosaccharides (HMOs) has long been known, yet the precise mechanism underlying it remains unresolved. Recent studies show that some species/subspecies of Bifidobacterium are equipped with genetic and enzymatic sets dedicated to the utilization of HMOs, and consequently they can grow on HMOs; however, the ability to metabolize HMOs has not been directly linked to the actual metabolic behavior of the bacteria. In this report, we clarify the fate of each HMO during cultivation of infant gut-associated bifidobacteria. Bifidobacterium bifidum JCM1254, Bifidobacterium longum subsp. infantis JCM1222, Bifidobacterium longum subsp. longum JCM1217, and Bifidobacterium breve JCM1192 were selected for this purpose and were grown on HMO media containing a main neutral oligosaccharide fraction. The mono- and oligosaccharides in the spent media were labeled with 2-anthranilic acid, and their concentrations were determined at various incubation times using normal phase high performance liquid chromatography. The results reflect the metabolic abilities of the respective bifidobacteria. B. bifidum used secretory glycosidases to degrade HMOs, whereas B. longum subsp. infantis assimilated all HMOs by incorporating them in their intact forms. B. longum subsp. longum and B. breve consumed lacto-N-tetraose only. Interestingly, B. bifidum left degraded HMO metabolites outside of the cell even when the cells initiate vegetative growth, which indicates that the different species/subspecies can share the produced sugars. The predominance of type 1 chains in HMOs and the preferential use of type 1 HMO by infant gut-associated bifidobacteria suggest the coevolution of the bacteria with humans.
Bifidobacterium longum
Bifidobacterium bifidum
Bifidobacterium breve
Subspecies
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Bifidobacteria are considered beneficial for infant health, however, they are less prevalent in gut microbiota of formula-fed than in breast-fed infants. This study investigated the bifidogenic effects of cow's glycomacropeptide (GMP) and metabolic enzymes that Bifidobacterium bifidum JCM1254 uses when grown in the GMP-containing medium. Bifidobacterium bifidum JCM1254 was able to be grown in the GMP-containing medium, and the growth was abolished when glycans were chemically cleaved. Abundance of carbohydrate metabolism-related proteins, including sialidase, were higher when Bifidobacterium bifidum JCM1254 was cultured in the GMP-containing medium than in the glucose-supplemented medium. Bifidobacterium breve ATCC15700 and Bifidobacterium longum subsp. infantis ATCC15697 were grown in the GMP-containing medium spent by Bifidobacterium bifidum JCM1254, and N-acetylneuraminic acid liberated by Bifidobacterium bifidum JCM1254 decreased when Bifidobacterium breve ATCC15700 was cultured in the spent medium. Collectively, GMP glycans are "cross-fed" among bifidobacteria, and carbohydrate metabolism-related proteins, expressed by Bifidobacterium bifidum, is involved in the cross-feeding.
Bifidobacterium bifidum
Bifidobacterium breve
Bifidobacterium longum
Actinomycetaceae
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