Dataset Information

Priority effects shape the structure of infant-type Bifidobacterium communities on human milk oligosaccharides.

ABSTRACT: Bifidobacteria are among the first colonizers of the infant gut, and human milk oligosaccharides (HMOs) in breastmilk are instrumental for the formation of a bifidobacteria-rich microbiota. However, little is known about the assembly of bifidobacterial communities. Here, by applying assembly theory to a community of four representative infant-gut associated Bifidobacterium species that employ varied strategies for HMO consumption, we show that arrival order and sugar consumption phenotypes significantly affected community formation. Bifidobacterium bifidum and Bifidobacterium longum subsp. infantis, two avid HMO consumers, dominate through inhibitory priority effects. On the other hand, Bifidobacterium breve, a species with limited HMO-utilization ability, can benefit from facilitative priority effects and dominates by utilizing fucose, an HMO degradant not utilized by the other bifidobacterial species. Analysis of publicly available breastfed infant faecal metagenome data showed that the observed trends for B. breve were consistent with our in vitro data, suggesting that priority effects may have contributed to its dominance. Our study highlights the importance and history dependency of initial community assembly and its implications for the maturation trajectory of the infant gut microbiota.

SUBMITTER: Ojima MN

PROVIDER: S-EPMC9381805 | biostudies-literature | 2022 Sep

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Priority effects shape the structure of infant-type Bifidobacterium communities on human milk oligosaccharides.

Ojima Miriam N MN Jiang Lin L Arzamasov Aleksandr A AA Yoshida Keisuke K Odamaki Toshitaka T Xiao Jinzhong J Nakajima Aruto A Kitaoka Motomitsu M Hirose Junko J Urashima Tadasu T Katoh Toshihiko T Gotoh Aina A van Sinderen Douwe D Rodionov Dmitry A DA Osterman Andrei L AL Sakanaka Mikiyasu M Katayama Takane T

The ISME journal 20220629 9

Bifidobacteria are among the first colonizers of the infant gut, and human milk oligosaccharides (HMOs) in breastmilk are instrumental for the formation of a bifidobacteria-rich microbiota. However, little is known about the assembly of bifidobacterial communities. Here, by applying assembly theory to a community of four representative infant-gut associated Bifidobacterium species that employ varied strategies for HMO consumption, we show that arrival order and sugar consumption phenotypes signi ...[more]

PMID: 35768643

Similar Datasets

Project description:Human milk contains a high concentration of complex oligosaccharides that influence the composition of the intestinal microbiota in breast-fed infants. Previous studies have indicated that select species such as Bifidobacterium longum subsp. infantis and Bifidobacterium bifidum can utilize human milk oligosaccharides (HMO) in vitro as the sole carbon source, while the relatively few B. longum subsp. longum and Bifidobacterium breve isolates tested appear less adapted to these substrates. Considering the high frequency at which B. breve is isolated from breast-fed infant feces, we postulated that some B. breve strains can more vigorously consume HMO and thus are enriched in the breast-fed infant gastrointestinal tract. To examine this, a number of B. breve isolates from breast-fed infant feces were characterized for the presence of different glycosyl hydrolases that participate in HMO utilization, as well as by their ability to grow on HMO or specific HMO species such as lacto-N-tetraose (LNT) and fucosyllactose. All B. breve strains showed high levels of growth on LNT and lacto-N-neotetraose (LNnT), and, in general, growth on total HMO was moderate for most of the strains, with several strain differences. Growth and consumption of fucosylated HMO were strain dependent, mostly in isolates possessing a glycosyl hydrolase family 29 ?-fucosidase. Glycoprofiling of the spent supernatant after HMO fermentation by select strains revealed that all B. breve strains can utilize sialylated HMO to a certain extent, especially sialyl-lacto-N-tetraose. Interestingly, this specific oligosaccharide was depleted before neutral LNT by strain SC95. In aggregate, this work indicates that the HMO consumption phenotype in B. breve is variable; however, some strains display specific adaptations to these substrates, enabling more vigorous consumption of fucosylated and sialylated HMO. These results provide a rationale for the predominance of this species in breast-fed infant feces and contribute to a more accurate picture of the ecology of the developing infant intestinal microbiota.

Project description:BackgroundThe initial colonization of the infant gut is a complex process that defines the foundation for a healthy microbiome development. Bifidobacterium longum is one of the first colonizers of newborns' gut, playing a crucial role in the healthy development of both the host and its microbiome. However, B. longum exhibits significant genomic diversity, with subspecies (e.g., Bifidobacterium longum subsp. infantis and subsp. longum) displaying distinct ecological and metabolic strategies including differential capabilities to break down human milk glycans (HMGs). To promote healthy infant microbiome development, a good understanding of the factors governing infant microbiome dynamics is required.MethodologyWe analyzed newly sequenced gut microbiome samples of mother-infant pairs from the Amsterdam Infant Microbiome Study (AIMS) and four publicly available datasets to identify important environmental and bifidobacterial features associated with the colonization success and succession outcomes of B. longum subspecies. Metagenome-assembled genomes (MAGs) were generated and assessed to identify characteristics of B. longum subspecies in relation to early-life gut colonization. We further implemented machine learning tools to identify significant features associated with B. longum subspecies abundance.ResultsB. longum subsp. longum was the most abundant and prevalent gut Bifidobacterium at one month, being replaced by B. longum subsp. infantis at six months of age. By utilizing metagenome-assembled genomes (MAGs), we reveal significant differences between and within B. longum subspecies in their potential to break down HMGs. We further combined strain-tracking, meta-pangenomics and machine learning to understand these abundance dynamics and found an interplay of priority effects, milk-feeding type and HMG-utilization potential to govern them across the first six months of life. We find higher abundances of B. longum subsp. longum in the maternal gut microbiome, vertical transmission, breast milk and a broader range of HMG-utilizing genes to promote its abundance at one month of age. Eventually, we find B. longum subsp. longum to be replaced by B. longum subsp. infantis at six months of age due to a combination of nutritional intake, HMG-utilization potential and a diminishment of priority effects.DiscussionOur results establish a strain-level ecological framework explaining early-life abundance dynamics of B. longum subspecies. We highlight the role of priority effects, nutrition and significant variability in HMG-utilization potential in determining the predictable colonization and succession trajectories of B. longum subspecies, with potential implications for promoting infant health and well-being.

Project description:While ample research on independent associations between infant cognition and gut microbiota composition and human milk (HM) oligosaccharides (HMOs) has been reported, studies on how the interactions between gut microbiota and HMOs may yield associations with cognitive development in infancy are lacking. We aimed to determine how HMOs and species of Bacteroides and Bifidobacterium genera interact with each other and their associations with cognitive development in typically developing infants. A total of 105 mother-infant dyads were included in this study. The enrolled infants [2.9-12 months old (8.09 ± 2.48)] were at least predominantly breastfed at 4 months old. A total of 170 HM samples from the mothers and fecal samples of the children were collected longitudinally. Using the Mullen Scales of Early Learning to assess cognition and the scores as the outcomes, linear mixed effects models including both the levels of eight HMOs and relative abundance of Bacteroides and Bifidobacterium species as main associations and their interactions were employed with adjusting covariates; infant sex, delivery mode, maternal education, site, and batch effects of HMOs. Additionally, regression models stratifying infants based on the A-tetrasaccharide (A-tetra) status of the HM they received were also employed to determine if the associations depend on the A-tetra status. With Bacteroides species, we observed significant associations with motor functions, while Bif. catenulatum showed a negative association with visual reception in the detectable A-tetra group both as main effect (value of p = 0.012) and in interaction with LNFP-I (value of p = 0.007). Additionally, 3-FL showed a positive association with gross motor (p = 0.027) and visual reception (p = 0.041). Furthermore, significant associations were observed with the interaction terms mainly in the undetectable A-tetra group. Specifically, we observed negative associations for Bifidobacterium species and LNT [breve (p = 0.011) and longum (p = 0.022)], and positive associations for expressive language with 3'-SL and Bif. bifidum (p = 0.01), 6'-SL and B. fragilis (p = 0.019), and LNFP-I and Bif. kashiwanohense (p = 0.048), respectively. Our findings suggest that gut microbiota and HMOs are both independently and interactively associated with early cognitive development. In particular, the diverse interactions between HMOs and Bacteroides and Bifidobacterium species reveal different candidate pathways through which HMOs, Bifidobacterium and Bacteroides species potentially interact to impact cognitive development in infancy.

Dataset Information

Priority effects shape the structure of infant-type Bifidobacterium communities on human milk oligosaccharides.

Publications

Priority effects shape the structure of infant-type Bifidobacterium communities on human milk oligosaccharides.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets