Bifidobacteria are bacterial gut commensals of mammals, birds and social insects that are perceived to influence the metabolism/physiology of their host. In this context, members of the Bifidobacterium bifidum species are believed to significantly contribute to the overall microbiota of the human gut at infant stage. However, the molecular reasons for their adaptation to this environment are poorly understood. In this study, we analysed the pan-genome of B.bifidum species by decoding genomes of 15 B.bifidum strains, which highlighted the existence of a conserved gene uniquely present in this bifidobacterial taxon, underscoring a nutrient acquisition strategy that targets host-derived glycans, such as those present in mucin. Growth experiments and corresponding transcriptomic analyses confirmed the in silico data and supported these intriguing and unique host glycan-specific saccharolytic features. The ubiquity of the genetic features of B.bifidum for the breakdown of host glycans was confirmed by interrogating metagenomic datasets, thereby supporting the notion that metabolic access to host-derived glycans is a potent evolutionary force that has shaped B.bifidum genomes and consequently the ecology of the infant intestinal microbiota. © 2014 Society for Applied Microbiology and John Wiley & Sons Ltd. ; We thank GenProbio srl for financial support of the Laboratory of Probiogenomics. This work was financially supported by a FEMS Jensen Award to FT, and by a Ph.D. fellowship (Spinner 2013, Regione Emilia Romagna) to S.D. DvS and FT are members of The Alimentary Pharmabiotic Centre; DvS is also a member of the Alimentary Glycoscience Research Cluster, both funded by Science Foundation Ireland (SFI), through the Irish Government's National Development Plan (Grant Nos. 07/CE/B1368, SFI/12/RC/2273 and 08/SRC/B1393). The authors declare that no competing interests exist. ; Peer Reviewed