Multi-Omics Association Reveals the Effects of Intestinal Microbiome–Host Interactions on Fat Deposition in Broilers

Abstract

Growing evidence indicates that gut microbiota factors cannot be viewed as independent in the occurrence of obesity. Because the gut microbiome is highly dimensional and complex, studies on interactions between gut microbiome and host in obesity are still rare. To explore the relationship of gut microbiome–host interactions with obesity, we performed multi-omics associations of gut metagenome, intestinal transcriptome, and host obesity phenotypes in divergently selected obese–lean broiler lines. Metagenomic shotgun sequencing generated a total of 450 gigabases of clean data from 80 intestinal segment contents of 20 broilers (10 of each line). The microbiome comparison showed that microbial diversity and composition in the duodenum, jejunum, ileum, and ceca were altered variously between the lean- and fat-line broilers. We identified two jejunal microbes (Escherichia coli and Candidatus Acetothermia bacterium) and four cecal microbes (Alistipes sp. CHKCI003, Ruminococcaceae bacterium CPB6, Clostridiales bacterium, and Anaeromassilibacillus sp. An200), which were significantly different between the two lines (FDR < 0.05). When comparing functional metagenome, the fat-line broilers had an intensive microbial metabolism in the duodenum and jejunum but degenerative microbial activities in the ileum and ceca. mRNA-sequencing identified a total of 1,667 differentially expressed genes (DEG) in the four intestinal compartments between the two lines (| log2FC| > 1.5 and FDR < 0.05). Multi-omics associations showed that the 14 microbial species with abundances that were significantly related with abdominal fat relevant traits (AFRT) also have significant correlations with 155 AFRT-correlated DEG (p < 0.05). These DEG were mainly involved in lipid metabolism, immune system, transport and catabolism, and cell growth-related pathways. The present study constructed a gut microbial gene catalog of the obese–lean broiler lines. Intestinal transcriptome and metagenome comparison between the two lines identified candidate DEG and differential microbes for obesity, respectively. Multi-omics associations suggest that abdominal fat deposition may be influenced by the interactions of specific gut microbiota abundance and the expression of host genes in the intestinal compartments in which the microbes reside. Our study explored the interactions between gut microbiome and host intestinal gene expression in lean and obese broilers, which may expand knowledge on the relationships between obesity and gut microbiome.

A comprehensive comparison of fecal microbiota in three ecological bird groups of raptors, waders, and waterfowl

“…The coevolution of vertebrates and their gut microbiota can maintain homeostasis and improve the host dietary niches ( Ley et al, 2008 ). An increasing amount of data from humans, cows, mice, chickens, insects, and fish has provided insight into the vital influence of gut microbes on host health, nutrition, immunity, and morphology ( Muegge et al, 2011 ; Engel and Moran, 2013 ; Jing et al, 2021 ; Stressmann et al, 2021 ). Previous studies on the gut microbiota of bird species have focused on the effects of specific bacteria or bacterial pathogens, demonstrating the essential role of the gut microbiota ( Benson et al, 2010 ).…”

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“…Through original data filtering, sequencing error rate checking and GC-content distribution checking, clean reads were obtained. Then, clean reads were compared with the reference genome using HISAT2 software (v2.0.5) quickly and accurately( Jing et al, 2021 ). Differentially expressed genes (DEGs) were identified in the intergroup comparison.…”

Research progress and applications of genome‐wide association study in farm animals

“…Notably, Yang et al showed that a quantitative trait locus affecting the abundance of Erysipelotrichaceae species is caused by a 2.3 kb deletion in the gene encoding N-acetyl-galactosaminyltransferase that underpins the ABO blood group in humans [128]. Jing et al indicated that abdominal fat in broilers was closely correlated with 14 microbial species and 155 genes in different intestinal tracts, which suggested that abdominal fat deposition may be influenced by the interactions of specific gut microbes and expression of host genes in the intestinal compartments [138].…”

“…Jing et al. indicated that abdominal fat in broilers was closely correlated with 14 microbial species and 155 genes in different intestinal tracts, which suggested that abdominal fat deposition may be influenced by the interactions of specific gut microbes and expression of host genes in the intestinal compartments [138].…”