Implication of digestive functions and microbiota in the establishment of muscle glycogen differences between divergent lines for ultimate pH

Abstract

Both the quality of chicken meat and the quality of chicks are influenced by the level of breast muscle glycogen reserves. In order to study the role of digestive metabolism in establishing this muscular phenotype, we compared two divergent chicken lines for the ultimate pH (pHu) of the breast meat, a proxy for glycogen reserves. Males aged 4 weeks had twice the breast muscle glycogen content in the pHu- line (low pHu) than in the pHu + line (high pHu). The increase in glycogen reserves (pHu-) was associated with a higher relative weight of the proventriculus and gizzard, as well as better apparent ileal digestibility of nitrogen and calcium. The diversity of the cecal microbiota was comparable, but three bacterial genera (Lachnospira, Lachnospiraceae UCG-010, Caproiciproducens) varied between the lines. The differences observed could lead to down-regulation of carbon fixation in prokaryotes and of the citrate cycle in the pHu + line. RNA-seq analysis of the jejunum, the major site of nutrient absorption, revealed 149 genes differentially expressed (DE) between the lines, including several genes linked to immunity, hormonal response and circadian rhythms that are less expressed in pHu + animals. Others involved in cell migration and proliferation, and more generally tissue morphogenesis, also differed between the lines. Among the DE genes, several co-localized with Quantitative Trait Loci (QTL) controlling pHu and selection signatures identified in the divergent lines, such as the gene coding for ghrelin, a hormone regulating appetite.

Keywords: Chicken; Glycogen; Gut; Microbiota; Muscle; RNA-seq.

Fig.1

Differences in morphological (A), digestibility (B) and histological (C) parameters between pHu- and pHu + lines (N = 15 per line). In orange the pHu—line and in blue the pHu + line.

Fig.2

Hierarchical clustering of enriched GO terms obtained from the set of DE genes in jejunum. The clustering heatmap plot obtained by VISEAGO combines the dendrogram of enriched GO terms based on semantic similarity, the heatmap of -log10(P-value) from the functional enrichment test and the information content (IC) of the GO terms (with a colour scale from white for 0 to dark purple for 10).

Fig.3

Composition of the caecal microbial community in pHu- and pHu + lines. Stacked bar graphs showing the relative abundances of the different bacterial genera in all samples from the pHu- and pHu + lines (A). Diagram of the three significant bacterial genera between pHu- and pHu + lines. In orange, the pHu- line and in blue, the pHu + line (B). Hierarchical classification of pathways based on subgroup identification and pathway names, starting from the inner ring outwards (C). The two black arrows indicate the two metabolic pathways that were differentially abundant between the pHu + and pHu- lines (surrounded in red).