Ruminal microbial metagenomes and host transcriptomes shed light on individual variability in the growth rate of lambs before weaning: the regulated mechanism and potential long-term effect on the host.

IF 5 2区 生物学 Q1 MICROBIOLOGY mSystems Pub Date : 2024-09-17 Epub Date: 2024-08-20 DOI:10.1128/msystems.00873-24
Fan Hu, Yan Cheng, Bing Fan, Wei Li, Bingsen Ye, Zhiwu Wu, Zhiliang Tan, Zhixiong He
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Abstract

Weaning weight is a reflection of management during the breastfeeding phase and will influence animal performance in subsequent phases, considered important indicators within production systems. The aims of this study were as follows: (i) to investigate variability in the growth rate among individual lambs from ewes rearing single or twin lambs fed with two different diets and (ii) to explore the molecular mechanisms regulating the growth rate and the potential long-term effects on the host. No significant change in lamb average daily gain (ADG) was observed in litter size and diet treatment, and there were large variations among individual lambs (ranging from 0.13 to 0.41 kg/day). Further analysis was conducted on serum amino acids, rumen fermentation characteristics, rumen metagenomics and transcriptome, and hepatic transcriptome of lambs with extremely high (HA; n = 6) and low (LA; n = 6) ADG. We observed significant increases in serum lysine, leucine, alanine, and phenylalanine in the HA group. The metagenome revealed that the HA group presented a higher rumen propionate molar proportion via increasing gene abundance in the succinate pathway for propionate synthesis. For the rumen transcriptome, higher expressed gene sets in the HA group were mainly related to rumen epithelial growth, including cytokine-cytokine receptor interaction, Jak-STAT signaling pathway, and adherens junction. For the liver transcriptome, the upregulated KEGG pathways in the HA group were primarily associated with fatty acid degradation, glyoxylate and dicarboxylate metabolism, cholesterol metabolism, and the immune system. This research suggests that preweaning lambs with high ADG may benefit from rumen development and enhanced liver metabolic and immune function.

Importance: There is accumulating evidence indicating that the early-life rumen microbiome plays vital roles in rumen development and microbial fermentation, which subsequently affects the growth of young ruminants. The liver is also vital to regulate the metabolism and distribution of nutrients. Our results demonstrate that lambs with high average daily gain (ADG) enhanced microbial volatile fatty acid (VFA) metabolism toward rumen propionate and serum amino acid (AA) production to support host growth. The study highlights that high ADG in the preweaning period is beneficial for the rumen development and liver energy metabolism, leading to better growth later in life. Overall, this study explores the molecular mechanisms regulating the growth rate and the potential long-term effects of increased growth rate on the host metabolism, providing fundamental knowledge about nutrient manipulation in pre-weaning.

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反刍微生物元基因组和宿主转录组揭示了羔羊断奶前生长速度的个体差异:调节机制和对宿主的潜在长期影响。
断奶体重反映了哺乳阶段的管理情况,并将影响动物在随后阶段的表现,被视为生产系统中的重要指标。本研究的目的如下(i) 研究用两种不同日粮饲喂单羔或双羔的母羊所产羔羊个体生长率的变化;(ii) 探索调节生长率的分子机制以及对宿主的潜在长期影响。在窝产仔数和日粮处理中,未观察到羔羊平均日增重(ADG)有明显变化,而且羔羊个体之间的差异很大(从 0.13 到 0.41 千克/天不等)。我们对ADG极高(HA;n = 6)和极低(LA;n = 6)羔羊的血清氨基酸、瘤胃发酵特征、瘤胃元基因组学和转录组以及肝脏转录组进行了进一步分析。我们观察到,HA 组的血清赖氨酸、亮氨酸、丙氨酸和苯丙氨酸明显增加。元基因组显示,通过增加丙酸合成琥珀酸途径中的基因丰度,HA 组的瘤胃中丙酸的摩尔比例较高。在瘤胃转录组中,HA组表达较高的基因集主要与瘤胃上皮生长有关,包括细胞因子-细胞因子受体相互作用、Jak-STAT信号通路和粘连接头。在肝脏转录组中,HA 组中上调的 KEGG 通路主要与脂肪酸降解、乙醛酸和二羧酸代谢、胆固醇代谢以及免疫系统有关。这项研究表明,ADG 高的断奶前羔羊可能受益于瘤胃发育和肝脏代谢及免疫功能的增强:越来越多的证据表明,生命早期的瘤胃微生物群在瘤胃发育和微生物发酵中发挥着重要作用,进而影响幼年反刍动物的生长。肝脏对调节营养物质的代谢和分配也至关重要。我们的研究结果表明,平均日增重(ADG)高的羔羊会增强微生物挥发性脂肪酸(VFA)的代谢,促进瘤胃丙酸和血清氨基酸(AA)的产生,从而支持宿主的生长。该研究强调,断奶前的高日增重有利于瘤胃发育和肝脏能量代谢,从而使犊牛日后的生长更好。总之,本研究探讨了调节生长速度的分子机制以及生长速度提高对宿主代谢的潜在长期影响,为断奶前的营养调控提供了基础知识。
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来源期刊
mSystems
mSystems Biochemistry, Genetics and Molecular Biology-Biochemistry
CiteScore
10.50
自引率
3.10%
发文量
308
审稿时长
13 weeks
期刊介绍: mSystems™ will publish preeminent work that stems from applying technologies for high-throughput analyses to achieve insights into the metabolic and regulatory systems at the scale of both the single cell and microbial communities. The scope of mSystems™ encompasses all important biological and biochemical findings drawn from analyses of large data sets, as well as new computational approaches for deriving these insights. mSystems™ will welcome submissions from researchers who focus on the microbiome, genomics, metagenomics, transcriptomics, metabolomics, proteomics, glycomics, bioinformatics, and computational microbiology. mSystems™ will provide streamlined decisions, while carrying on ASM''s tradition of rigorous peer review.
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