Maternal Perinatal Gut Microbiome Is Shaped by Traditional Farming Lifestyle and Associated With Early Childhood Atopic Disease.

Abstract

Maternal exposure to a traditional farming lifestyle during pregnancy is associated with protection against allergic disease in childhood; however, the mechanism remains unclear. Pre-clinical work has demonstrated a role for the maternal gut microbiome in fetal immune programming. Given the diverse microbial exposure on farms, we sought to assess whether the maternal gut microbiome may mediate the relationship between maternal farm exposure and protection against offspring allergic disease. Deep shotgun metagenomic analysis of the perinatal fecal microbiome showed that women from an Old Order Mennonite traditional farming community (OOM, n = 68) harbored a more diverse gut microbiome relative to women from urban/suburban Rochester, NY (ROC, n = 55). We identified several bacterial species differentially abundant between lifestyle groups, including those from Dorea, Anaerobutyricum, Bifidobacterium, and Bacteroides genera, which translated to marked differences in microbiome functional capacity. These differences in the gut microbiome composition were accompanied by targeted metabolite findings indicating higher serum acetate and isobutyrate levels in OOM women that were positively correlated with cord plasma levels and infant systemic IgA concentrations. Among urban women, maternal microbiome composition was associated with early childhood atopic disease outcomes. Specifically, Dorea longicatena and Segatella copri were least abundant in urban mothers whose infants developed atopic disease (atopic dermatitis) or IgE-mediated food allergy alone, respectively, and were most abundant in the OOM mothers. Together, these findings highlight the maternal gut microbiome and metabolites as potential contributors to prenatal farming lifestyle protection against early childhood allergic disease.