Strain-level translocation and enrichment dynamics of oral bacteria in the lower gastrointestinal tract of stunted children

Abstract

Emerging evidence suggests that ectopic colonization of oral bacteria in the lower digestive tract may exacerbate gastrointestinal disorders. Nevertheless, it remains unclear whether bacteria of oral origin are continuously translocating from the oral cavity to the lower gastrointestinal tract or are locally adapted and persist in their respective niches. We investigated strain translocation dynamics in 44 healthy and stunted children from Bangui, Central African Republic. Using cross-sectional shotgun metagenomic sequencing of saliva, gastric, duodenal, and fecal samples, and isolation and whole-genome sequencing of 87 Streptococcus salivarius isolates, we showed the translocation of members of the genera Streptococcus, Veillonella, Rothia, and Haemophilus. Fecal isolates were more closely related to oral isolates from the same individuals than to those from other individuals. Additionally, saliva showed higher S. salivarius nucleotide diversity compared to other compartments, which is consistent with frequent intraindividual translocations from the oral cavity to the lower gastrointestinal tract. Finally, we showed that overrepresentation of oral bacteria in the duodenum of stunted children is related to increased biomass, while in the colon, it is linked to depletion of overall biomass, including in butyrate-producing strains. Our study quantifies dynamics of oral-to-gut translocation and enrichment of oral taxa, providing key insights into microbiota disruption in stunted children.