Effects of paternal high-fat diet and maternal rearing environment on the gut microbiota and behavior

Abstract

Exposing a male rat to an obesogenic high-fat diet (HFD) influences attractiveness to potential female mates, the subsequent interaction of female mates with infant offspring, and the development of stress-related behavioral and neural responses in offspring. To examine the stomach and fecal microbiome’s potential roles, fecal samples from 44 offspring and stomach samples from offspring and their fathers were collected and bacterial community composition was studied by 16 small subunit ribosomal RNA (16S rRNA) gene sequencing. Paternal diet (control, high-fat), maternal housing conditions (standard or semi-naturalistic housing), and maternal care (quality of nursing and other maternal behaviors) affected the within-subjects alpha-diversity of the offspring stomach and fecal microbiomes. We provide evidence from beta-diversity analyses that paternal diet and maternal behavior induced community-wide shifts to the adult offspring gut microbiome. Additionally, we show that paternal HFD significantly altered the adult offspring Firmicutes to Bacteroidetes ratio, an indicator of obesogenic potential in the gut microbiome. Additional machine-learning analyses indicated that microbial species driving these differences converged on Bifidobacterium pseudolongum. These results suggest that differences in early-life care induced by paternal diet and maternal care significantly influence the microbiota composition of offspring through the microbiota-gut-brain axis, having implications for adult stress reactivity.

A Review of the Impact of Maternal Prenatal Stress on Offspring Microbiota and Metabolites

“…A recent study identified novel interactions between paternal diet, maternal care, and offspring microbiome and stress reactivity [95]. Paternal high-fat diet exposure significantly altered the adult offspring Fermicutes to Bacteroidetes ratio and behavior [95]. These findings are consistent with the emerging concept that stress leads to dramatic changes in the composition of gut bacteria and regulates stress-induced changes in social behavior.…”

“…Thus, microbe-induced paternal care could modulate horizontal microbial transmission to the offspring. A recent study identified novel interactions between paternal diet, maternal care, and offspring microbiome and stress reactivity [95]. Paternal high-fat diet exposure significantly altered the adult offspring Fermicutes to Bacteroidetes ratio and behavior [95].…”

Transgenerational impact of grand‐paternal lifetime exposures to both folic acid deficiency and supplementation on genome‐wide DNA methylation in male germ cells

“…Studies have examined paternal stress and the transmission of stress phenotypes, implicating a role for RNAs in sperm, in particular small non‐coding RNAs 50 . Similarly, paternal high fat diets have been shown to induce increased anxiety and fear reactivity in the next generation 51 . Interestingly, we found in F1 spermatogonia and sperm from F1 and F2 an enrichment of GO terms for nervous system development and social behavior.…”

“…50 Similarly, paternal high fat diets have been shown to induce increased anxiety and fear reactivity in the next generation. 51 Interestingly, we found in F1 spermatogonia and sperm from F1 and F2 an enrichment of GO terms for nervous system development and social behavior. Variants in Camta1, a DMR found to be affected in all diets in F1 spermatogonia, have been associated with neurological phenotypes and intellectual disabilities.…”

Molecular Mechanisms and Pathophysiological Pathways of High-Fat Diets and Caloric Restriction Dietary Patterns on Pain

“…101 Even paternal and maternal HFD altered microbial composition and function through the gut-brain axis in offspring. [102][103][104][105] Moreover, HFDinduced gut microbial changes contributed to the development of enteric neuropathy. 106 A possible causal connection has been reported between HFDdriven gut microbial changes and proinflammatory effects.…”