Mobile genetic elements from the maternal microbiome shape infant gut microbial assembly and metabolism

• Published in: Cell 2022-12, Vol.185 (26), p.4921-4936.e15
• Main Authors: Vatanen, Tommi, Jabbar, Karolina S., Ruohtula, Terhi, Honkanen, Jarno, Avila-Pacheco, Julian, Siljander, Heli, Stražar, Martin, Oikarinen, Sami, Hyöty, Heikki, Ilonen, Jorma, Mitchell, Caroline M., Yassour, Moran, Virtanen, Suvi M., Clish, Clary B., Plichta, Damian R., Vlamakis, Hera, Knip, Mikael, Xavier, Ramnik J.
• Format: Article
• Language: English
• Subjects: Breast Feeding; Feces; Female; Gastrointestinal Microbiome - genetics; gut metabolome; horizontal gene transfer; Humans; Infant; infant gut microbiome; Interspersed Repetitive Sequences; Microbiota - genetics; mother-to-infant microbiome transmission; Mothers; Pregnancy
• ISSN: 0092-8674; 1097-4172
• DOI: 10.1016/j.cell.2022.11.023

The perinatal period represents a critical window for cognitive and immune system development, promoted by maternal and infant gut microbiomes and their metabolites. Here, we tracked the co-development of microbiomes and metabolomes from late pregnancy to 1 year of age using longitudinal multi-omics data from a cohort of 70 mother-infant dyads. We discovered large-scale mother-to-infant interspecies transfer of mobile genetic elements, frequently involving genes associated with diet-related adaptations. Infant gut metabolomes were less diverse than maternal but featured hundreds of unique metabolites and microbe-metabolite associations not detected in mothers. Metabolomes and serum cytokine signatures of infants who received regular—but not extensively hydrolyzed—formula were distinct from those of exclusively breastfed infants. Taken together, our integrative analysis expands the concept of vertical transmission of the gut microbiome and provides original insights into the development of maternal and infant microbiomes and metabolomes during late pregnancy and early life. [Display omitted] •Mobile genetic elements from maternal bacteria shape offspring gut microbiomes•Microbiome and metabolome shifts in pregnancy may impact maternal metabolic health•The infant gut harbors unique metabolites and species-metabolite relationships•Diet modulates metabolomic profiles and immune system maturation in infants Maternal gut bacteria that fail to engraft in infants instead influence the assembly and metabolic potential of the infant gut microbiome through horizontal gene transfer.