Assessment of genome evolution in Bifidobacterium adolescentis indicates genetic adaptation to the human gut

Bifidobacterium adolescentis is one of the most frequently encountered bifidobacterial species present in the adult human gut microbiota, with a prevalence of approximately 60%. Despite its high prevalence, B. adolescentis has not been extensively studied and characterized, and our understanding of its physiological traits, genetic diversity, and potential interactions with other members of the human gut microbiota or with its host is therefore fragmentary. In the current study, a data set comprising 1,682 B. adolescentis genomes was compiled by combining publicly available data and metagenome assemblies from 131 projects to uncover the unique genetic characteristics of this species. A pangenome analysis of B. adolescentis identified 203 clusters of orthologous genes absent from the other five human-associated Bifidobacterium species, six of which were in silico predicted to encode functions unique to this taxon. Furthermore, 2,597 genes were predicted to have been acquired by horizontal gene transfer, including genes encoding extracellular structures involved in interaction with the host and other microorganisms, and phage defense mechanisms against bacteriophages. Detailed phylogenetic analysis revealed seven clusters within the B. adolescentis species, each partially associated with the origin of strain isolation, suggesting phylogenetic differentiation shaped by geographical strain origin. Moreover, a large-scale metagenomic analysis of over 10,000 human gut metagenomes from healthy adults revealed that B. adolescentis co-occurs with 36 putative beneficial commensals and butyrate-producing taxa, highlighting its role as a key bifidobacterial species involved in microbial networking within the adult human gut microbiota.

To comprehensively explore the biodiversity within a microbial species, the reconstruction of a substantial number of genomes is essential. In this study, we successfully uncovered the genetic diversity of Bifidobacterium adolescentis by retrieving a large number of genomes from human gut metagenomic samples. The complete overview of the B. adolescentis pangenome enabled us to investigate the genetic features that distinguish this gut commensal from other bifidobacterial species residing in the human intestinal microbiota.