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Background: <i>Bifidobacterium</i> represents an important early life microbiota member. Specific bifidobacterial components, exopolysaccharides (EPS), positively modulate host responses, with purified EPS also suggested to impact microbe–microbe interactions by acting as a nutrient substrate. Thus, we determined the longitudinal effects of bifidobacterial EPS on microbial communities and metabolite profiles using an infant model colon system. Methods: Differential gene expression and growth characteristics were determined for each strain; <i>Bifidobacterium breve</i> UCC2003 and corresponding isogenic EPS-deletion mutant (<i>B. breve</i> UCC2003del). Model colon vessels were inoculated with <i>B. breve</i> and microbiome dynamics monitored using 16S rRNA sequencing and metabolomics (NMR). Results: Transcriptomics of EPS mutant vs. <i>B. breve</i> UCC2003 highlighted discrete differential gene expression (e.g., <i>eps</i> biosynthetic cluster), though overall growth dynamics between strains were unaffected. The EPS-positive vessel had significant shifts in microbiome and metabolite profiles until study end (405 h); with increases of <i>Tyzzerella</i> and <i>Faecalibacterium</i>, and short-chain fatty acids, with further correlations between taxa and metabolites which were not observed within the EPS-negative vessel. Conclusions: These data indicate that <i>B. breve</i> UCC2003 EPS is potentially metabolized by infant microbiota members, leading to differential microbial metabolism and altered metabolite by-products. Overall, these findings may allow development of EPS-specific strategies to promote infant health.