Abstract
BackgroundThe gastrointestinal tract is populated by a complex and vast microbial network, with a composition that reflects the relationships of the symbiosis, co-metabolism, and co-evolution of these microorganisms with their host. The mechanism that underlies such interactions between the genetics of the host and gut microbiota remains elusive.ResultsTo understand how genetic variation of the host shapes the gut microbiota and interacts with it to affect the metabolic phenotype of the host, we compared the abundance of microbial taxa and their functional performance between two lines of chickens (fat and lean) that had undergone long-term divergent selection for abdominal fat pad weight, which resulted in a 4.5-fold increase in the fat line compared to the lean line. Our analysis revealed that the proportions of Fusobacteria and Proteobacteria differed significantly between the two lines (8 vs. 18% and 33 vs. 24%, respectively) at the phylum level. Eight bacterial genera and 11 species were also substantially influenced by the host genotype. Differences between the two lines in the frequency of host alleles at loci that influence accumulation of abdominal fat were associated with differences in the abundance and composition of the gut microbiota. Moreover, microbial genome functional analysis showed that the gut microbiota was involved in pathways that are associated with fat metabolism such as lipid and glycan biosynthesis, as well as amino acid and energy metabolism. Interestingly, citrate cycle and peroxisome proliferator activated receptor (PPAR) signaling pathways that play important roles in lipid storage and metabolism were more prevalent in the fat line than in the lean line.ConclusionsOur study demonstrates that long-term divergent selection not only alters the composition of the gut microbiota, but also influences its functional performance by enriching its relative abundance in microbial taxa. These results support the hypothesis that the host and gut microbiota interact at the genetic level and that these interactions result in their co-evolution.Electronic supplementary materialThe online version of this article (doi:10.1186/s12711-016-0270-5) contains supplementary material, which is available to authorized users.
Highlights
The gastrointestinal tract is populated by a complex and vast microbial network, with a composition that reflects the relationships of the symbiosis, co-metabolism, and co-evolution of these microorganisms with their host
In order to quantify the influence of genetic variation of the host on the structure of the gut microbiota, the abundance of gut microbiota was considered as a quantitative trait of the host, and we calculated the heritability of abundance of specific microorganisms in the gut microbiota
Functional prediction results revealed that signal transduction mechanisms and fatty acid biosynthesis were more abundant in the fat line than in the lean line and this was consistent with the results of the microbial composition of the gut microbiota [see Additional file 5: Table S4 and Additional file 8: Figure S2]
Summary
The gastrointestinal tract is populated by a complex and vast microbial network, with a composition that reflects the relationships of the symbiosis, co-metabolism, and co-evolution of these microorganisms with their host. Suppression of the expression of these genes by direct action of the gut microbiota on the villi epithelia causes increased lipoprotein lipase activity, which leads to increased triglyceride uptake and peripheral fat storage [8]. These findings are in agreement with previous studies in other chicken populations selected for high or low body fat [9, 10] and show that the gut microbiota affects energy uptake from the diet and energy storage in the host [7]. Most studies focused on microbial taxa instead of microbial functional performance to understand the interactions between host genetics and gut microbiota
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