Pucci Nicholas, Ujčič-Voortman Joanne, Verhoeff Arnoud P, Mende Daniel R
Department of Medical Microbiology and Infection Prevention, Amsterdam University Medical Centers, Amsterdam, Netherlands.
Sarphati Amsterdam, Department of Public Health Service Amsterdam, Amsterdam, Netherlands.
PeerJ. 2025 Jan 21;13:e18602. doi: 10.7717/peerj.18602. eCollection 2025.
The initial colonization of the infant gut is a complex process that defines the foundation for a healthy microbiome development. 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, exhibits significant genomic diversity, with subspecies ( subsp. and subsp. ) 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.
We 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 subspecies. Metagenome-assembled genomes (MAGs) were generated and assessed to identify characteristics of subspecies in relation to early-life gut colonization. We further implemented machine learning tools to identify significant features associated with subspecies abundance.
subsp. was the most abundant and prevalent gut at one month, being replaced by subsp. at six months of age. By utilizing metagenome-assembled genomes (MAGs), we reveal significant differences between and within 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 subsp. 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 subsp. to be replaced by subsp. at six months of age due to a combination of nutritional intake, HMG-utilization potential and a diminishment of priority effects.
Our results establish a strain-level ecological framework explaining early-life abundance dynamics of 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 subspecies, with potential implications for promoting infant health and well-being.
婴儿肠道的初始定植是一个复杂的过程，它为健康的微生物组发育奠定了基础。 是新生儿肠道最早的定植者之一，在宿主及其微生物组的健康发育中起着至关重要的作用。然而， 表现出显著的基因组多样性，其亚种（亚种 和亚种 ）展现出不同的生态和代谢策略，包括分解人乳聚糖（HMGs）的不同能力。为促进婴儿微生物组的健康发育，需要深入了解影响婴儿微生物组动态变化的因素。
我们分析了来自阿姆斯特丹婴儿微生物组研究（AIMS）的母婴对新测序的肠道微生物组样本以及四个公开可用的数据集，以确定与亚种定植成功和演替结果相关的重要环境和双歧杆菌特征。生成并评估了宏基因组组装基因组（MAGs），以确定亚种与早期生命肠道定植相关的特征。我们进一步应用机器学习工具来识别与亚种丰度相关的显著特征。
亚种 在一个月时是最丰富和普遍的肠道 ，在六个月大时被亚种 取代。通过利用宏基因组组装基因组（MAGs），我们揭示了亚种之间及其内部在分解HMGs潜力方面的显著差异。我们进一步结合菌株追踪、元泛基因组学和机器学习来理解这些丰度动态变化，发现优先效应、哺乳类型和HMG利用潜力之间的相互作用在生命的前六个月中支配着它们。我们发现母亲肠道微生物组中亚种 的丰度更高、垂直传播、母乳以及更广泛的HMG利用基因促进了其在一个月龄时的丰度。最终，由于营养摄入、HMG利用潜力和优先效应的减弱，我们发现亚种 在六个月大时被亚种 取代。
我们的结果建立了一个菌株水平的生态框架，解释了亚种在生命早期的丰度动态变化。我们强调了优先效应、营养和HMG利用潜力的显著变异性在决定亚种可预测的定植和演替轨迹方面的作用，这对促进婴儿健康和福祉具有潜在影响。
