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.
Highlights
Obesity is a systemic lipodystrophic syndrome which is a serious health problem worldwide in humans
A commercial soybean-based diet that met all of the National Research Council (NRC) requirements was provided; a starter diet of 3,000 kcal ME/kg and 210 g/kg CP was fed to the birds until 3 weeks of age, while a grower diet of 3,100 kcal metabolizable energy (ME)/kg and 190 g/kg crude protein (CP) was fed from 3 to 7 weeks of age (Guo et al, 2011)
For clinical serum biochemical phenotypes, high-density lipoprotein cholesterol (HDL-C), ratio of HDL-C to low-density lipoprotein cholesterol (LDL-C), total protein (TP), ALB, γ-glutamyl transpeptidase (GGT), and uric acid (UA) in the fat line were significantly higher than in the lean line, while GLU was significant decreased in fat-line broilers (p < 0.05)
Summary
Obesity is a systemic lipodystrophic syndrome which is a serious health problem worldwide in humans. The intestinal tract functional variations directly impact systemic nutrition metabolism, especially lipid metabolism, which contributes to obesity (Kondo et al, 2006; Mao et al, 2013). Altered functions such as an increase in mucus layer permeability and breach of intestinal integrity have been reported in obese mice, though causality was unclear (Teixeira et al, 2012; Araujo et al, 2017). Several intestinal genes and pathways were significantly changed in obese humans and mice, compared to controls (Mao et al, 2013; Pfalzer et al, 2016; Xie et al, 2017).
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