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Dietary β-hydroxybutyrate sodium alters rumen microbiome and nutrient metabolism in the rumen epithelium of young goats

Yimin Zhuang1, 2, 3*, Guanglei Liu3, 4*, Chuyun Jiang1, Mahmoud M ABDELSATTAR2, 6, Yuze Fu2, Ying Li1, Naifeng Zhang2#, Jianmin Chai1, 5#

Guangdong Provincial Key Laboratory of Animal Molecular Design and Precise Breeding, School of Animal Science and Technology, Foshan University, Foshan 528000, China

Key laboratory of Feed Biotechnology of the Ministry of Agriculture and Rural Affairs, Institute of Feed Research, Chinese Academy of Agricultural Sciences, Beijing 100081, China

State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, China

Jockey Club College of Veterinary Medicine and Life Sciences, City University of Hong Kong, Hong Kong SAR 999077, China.

Department of Animal Science, Division of Agriculture, University of Arkansas, Fayetteville, AR 72701, USA

Department of Animal and Poultry Production, Faculty of Agriculture, South Valley University, Qena 83523, Egypt

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摘要  

β-羟基丁酸(β-Hydroxybutyric acid, BHBA)在宿主中具有提供能量、调节信号通路以及改善肠道微生物群等多种功能。然而,BHBA在促进幼龄反刍动物瘤胃上皮发育方面的营养机制尚不明确。本研究旨在通过饲粮中添加β-羟基丁酸钠(BHBA-Na)来探讨其对幼龄山羊瘤胃发育的影响。

试验选用12只30日龄的雌性海门山羊,随机分为两组:对照组(CON)饲喂基础日粮,处理组饲喂基础日粮并额外添加6克/天的BHBA-Na。试验周期30天,所有山羊在60日龄时屠宰。通过多组学联合分析,包括瘤胃微生物群、瘤胃上皮转录组和瘤胃上皮代谢组,系统研究了BHBA-Na对瘤胃发育的影响。

研究结果表明,BHBA-Na显著提高了幼龄山羊的生长性能,包括体重、平均日增重(ADG)和干物质采食量(DMI)(P < 0.05)。同时,BHBA-Na促进了瘤胃重量的增加和瘤胃上皮的发育(P < 0.05)。在微生物群方面,处理组瘤胃中多种有益细菌的丰度显著提高,如纤维杆菌属(Fibrobacter)、琥珀弧菌属(Succinivibrio)和梭菌目(Clostridiales)。瘤胃上皮转录组学和代谢组学的分析表明,补充BHBA-Na对瘤胃上皮的营养代谢产生了显著影响,激活了“脂肪酸代谢”、“胆固醇稳态”、“活性氧(ROS)通路”和“过氧化物酶体”通路(P < 0.05)。此外,与这些通路相关的基因(如HMGCS2ECSH1ACAA2ECH1ACADS)和代谢物(如琥珀酸、α-酮异戊酸等)也呈现出显著上调(P < 0.05),表明瘤胃上皮通过挥发性脂肪酸(VFA)分解获得能量,以促进其发育。此外,研究发现生长表型、瘤胃微生物群、宿主基因表达和上皮代谢物之间存在紧密的相关性。

综上所述,BHBA-Na可能通过增强DMI、调节瘤胃微生物群及瘤胃上皮的VFA和氨基酸代谢,促进幼龄山羊的生长及瘤胃发育。这项研究揭示了BHBA-Na在反刍动物营养代谢中的新作用,为幼龄反刍动物的瘤胃发育提供了新的调控策略。

关键词:



Abstract  

The role of β-hydroxybutyric acid (BHBA) includes providing energy, regulating signaling pathways, and ameliorating the gut microbiota in the host, while its nutrient mechanism to improve rumen epithelium development in young ruminants is still unclear. In this study, a total of 12 female Haimen goats with 30 days of age were chosen and divided into two groups. One group was fed with basic diet (CON), and the other group was fed a basal diet supplemented with 6 g d-1 dietary β-hydroxybutyrate sodium (BHBA-Na). The experimental period was 30 days, and all goats were slaughtered at 60 days of age. The joint analysis of multi-omics, including rumen microbiota, rumen epithelial transcriptome and rumen epithelial metabolomics in young goat model, was performed to systematically investigate the effect of dietary BHBA-Na on rumen development in young goats. As the results, we found that dietary BHBA-Na improved the growth performance of young goat including body weight, average daily gain (ADG) and dry matter intake (DMI) (P<0.05). Dietary BHBA-Na also increased the weight of rumen, and promoted the growth of rumen epithelium development (P < 0.05). The abundance of several beneficial bacteria was increased (Fibrobacter, Succinivibrio, Clostridiales, etc.,). The rumen epithelium transcriptome and metabolomics indicated that BHBA-Na supplementation showed a remarkable effect on the nutrient metabolism of the rumen epithelium. Specifically, the pathways of “fatty acid metabolism”, “cholesterol homeostasis”, “reactive oxygen species (ROS) pathway” and “peroxisome” were activated in response to BHBA-Na addition (P < 0.05). Moreover, the genes (HMGCS2, ECSH1, ACAA2, ECH1, ACADS etc.) and metabolites (succinic acid, alpha-ketoisovaleric acid, etc.) involved in these pathways were also regulated positively (P < 0.05). The rumen epithelium obtained the energy for its development from the process of volatile fatty acids (VFAs) decomposition. Finally, we observed the close correlations among the phenotypes, ruminal microbiota, host genes and epithelial metabolites. Overall, our results revealed that the BHBA-Na promoted the growth and rumen development of young goats possibly by enhancing DMI and regulating the rumen microbiota and the metabolisms of VFA and amino acid in the rumen epithelium.

Keywords:  goats       β-hydroxybutyrate acid              rumen microbiota              rumen transcriptome              rumen epithelial metabolomic              rumen epithelium development  
Online: 12 November 2024  
Fund: 

The authors thank the goat farm for their cooperation in animal handling. We also appreciate the assistance with sampling collection from Dr. Shiqin Wang, Prof. Shaoxian Cao, Dr. Hongbing Gui, Dr. Yue Wang, Dr. Xiaoxiao Guo and Dr. Han Zhang, Jiangsu Academy of Agricultural Sciences. This study was funded by grants from National Natural Science Foundation of China (31872385), Guangdong Provincial Key Laboratory of Animal Molecular Design and Precise Breeding (2019B030301010), Foshan Postdoctoral Sustentation Fund (BKS209151), the Inner Mongolia Science and Technology Key Project (2021SZD0014), and the National Key R&D Program Projects (2018YFD0501902).

Cite this article: 

Yimin Zhuang, Guanglei Liu, Chuyun Jiang, Mahmoud M ABDELSATTAR, Yuze Fu, Ying Li, Naifeng Zhang, Jianmin Chai. 2024. Dietary β-hydroxybutyrate sodium alters rumen microbiome and nutrient metabolism in the rumen epithelium of young goats. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2024.11.016

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