Dietary Energy Level Impacts the Performance of Donkeys by Manipulating the Gut Microbiome and Metabolome.

Chongyu Zhang,Yunkyoung Lee,Chen Zhang,Guiguo Zhang,Yunpeng Wang,Meiyu Du

doi:10.3389/fvets.2021.694357

Chongyu Zhang, Yunkyoung Lee + Show 4 more

Open Access

https://doi.org/10.3389/fvets.2021.694357

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Abstract

Considerable evidence suggests that dietary energy levels and gut microbiota are pivotal for animal health and productivity. However, little information exists about the correlations among dietary energy level, performance, and the gut microbiota and metabolome of donkeys. The objective of this study was to investigate the mechanisms by which dietary energy content dictates the growth performance by modulating the intestinal microbiome and metabolome of donkeys. Thirty-six nine-month-old male Dezhou donkeys with similar body weights were randomly assigned to two groups fed low- or high-energy diets (LE or HE). The results showed that donkeys fed HE had increased (p < 0.05) the average daily gain (ADG) and feed efficiency (G/F) compared with those that received LE diet. The gut microbiota in both groups was dominated by the phyla Firmicutes and Bacteroidetes regardless of the dietary energy level. However, feeding HE to donkeys significantly decreased (p < 0.05) the ratio of Firmicutes to Bacteroidetes (F/B). Compared to the LE group, feeding HE specifically increased the abundances of unidentified_Prevotellaceae (p = 0.02) while decreasing the richness of unidentified_Ruminococcaceae (p = 0.05). Compared to the LE group, feeding the HE diet significantly (p < 0.05) upregulated certain metabolic pathways involving the aspartate metabolism and the urea cycle. In addition, the increased bacteria and metabolites in the HE-fed group exhibited a positive correlation with improved growth performance of donkeys. Taken together, feeding the HE diet increased the richness of Prevotellaceae and upregulated growth-related metabolic pathways, which may have contributed to the ameliorated growth performance of donkeys. Thus, it is a recommendable dietary strategy to feed HE diets to fattening donkeys for superior product performance and feed efficiency.

Highlights

The Dezhou donkey (Equus asinus) is an excellent indigenous herbivorous domestic animal in China, with superior productivity and high forage efficiency [1]
2,063 operational taxonomic units (OTUs) were obtained in the HE groups, which belonged to 25 phyla, 37 classes, 70 orders, 127 families, and 239 genera
Feeding HE diets improved the concentrations of L-aspartic acid, ornithine, L-glutamine, L-phenylalanine, L-serine, methionine, lysine, L-isoleucine, and N-acetylaspartic acid in the gut content of donkeys and affected some growth-related metabolic pathways mainly involving aspartate metabolism and urea cycle

Summary

Introduction

The Dezhou donkey (Equus asinus) is an excellent indigenous herbivorous domestic animal in China, with superior productivity and high forage efficiency [1]. The gut microbiota is the key mediator through which the diet impacts the host health [4] and productivity [5]. The dietary energy level is considered to be a pivotal factor that impacts the growth performance and health condition of animals [6], and the richness and compositions of the microbial community residing in the digestible tract are tightly correlated with the energy harvest efficiency of the host [7]. It has been documented that the dietary energy level could profoundly affect the gut microbiota and result in the changes in nutrient digestibility, microbial protein synthesis, and milk production parameters by intervening in the ruminal microbial community [6]. How the dietary energy level affects the gut microbiota and growth performance of donkeys remains unclear

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