Intestinal Microbiota and Host Cooperate for Adaptation as a Hologenome

Multiomic analyses reported here involved two lines of chickens, from a common founder population, that had undergone long-term selection for high (HWS) or low (LWS) 56-day body weight. In these lines that differ by around 15-fold in body weight, we observed different compositions of intestinal microbiota in the holobionts and variation in DNA methylation, mRNA expression, and microRNA profiles in the ceca. Insulin-like growth factor 2 mRNA-binding protein 1 (IGF2BP1) was the most upregulated gene in HWS ceca with its expression likely affected by the upregulation of expression of gga-miR-2128 and a methylated region near its transcription start site (388 bp). Correlation analysis showed that IGF2BP1 expression was associated with an abundance of microbes, such as Lactobacillus and Methanocorpusculum. These findings suggest that IGF2BP1 was regulated in the hologenome in adapting to long-term artificial selection for body weight. Our study provides evidence that adaptation of the holobiont can occur in the microbiome as well as in the epigenetic profile of the host. IMPORTANCE The hologenome concept has broadened our perspectives for studying host-microbe coevolution. The multiomic analyses reported here involved two lines of chickens, from a common founder population, that had undergone long-term selection for high (HWS) or low (LWS) 56-day body weight. In these lines that differ by around 15-fold in body weight, we observed different compositions of intestinal microbiota in the holobionts, and variation in DNA methylation, mRNA expression, and microRNA profiles in ceca. The insulin-like growth factor 2 mRNA-binding protein 1 (IGF2BP1) was the most upregulated gene in HWS ceca with its expression likely affected by a methylated region near its transcription start site and the upregulation of expression of gga-miR-2128. Correlation analysis also showed that IGF2BP1 expression was associated with the abundance of microbes, such as Lactobacillus and Methanocorpusculum. These findings suggest that IGF2BP1 was regulated in the hologenome in response to long-term artificial selection for body weight. Our study shows that the holobiont may adapt in both the microbiome and the host's epigenetic profile.