Temperament affects the impact of dietary tryptophan on the gut-liver-brain axis in sheep

doi:10.1016/j.jia.2025.09.015

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Feifan Wu^1,², Luoyang Ding^1,², Shane K Maloney³, Dominique Blache^1,², Mengzhi Wang^{1, 4}^#

¹College of Animal Science and Technology, Yangzhou University, Yangzhou 225300, China;

²School of Agriculture and Environment and UWA Institute of Agriculture, The University of Western Australia, 35 Stirling Highway, Crawley 6009, Western Australia, Australia;

³School of Human Sciences, The University of Western Australia, 35 Stirling Highway, Crawley 6009, Western Australia, Australia;

⁴State Key Laboratory of Sheep Genetic Improvement and Healthy Production, Xinjiang Academy of Agricultural Reclamation Sciences, Shihezi 832000, China.

Highlights

• Dietary tryptophan affects sheep temperament via the gut–liver–brain axis.

•The microbiome activates SCFA and tryptophan metabolites pathways in a temperament-specific manner.

• Nutrition strategies tailored to temperament could improve sheep welfare.

Abstract
References

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摘要

性情是个体在面对外界挑战时表现出的稳定反应模式，与人格特征类似，例如在相同情境下表现为安静或激动的差异。性情不仅受遗传因素影响，还可受到调控大脑相关通路的内在生理与代谢因素的调节。在单胃动物中，已有研究表明肠–脑轴（GBA）参与性情的形成。然而，最新研究发现来自肝脏的信号亦可通过调节大脑功能和肠道微生物群而产生作用，从而构成肠–肝–脑轴（GLBA）的三向互作机制，但肝脏在GLBA调控性情中的具体作用尚不明确。为探究这一问题，本研究首次在反刍动物中系统评估了饮食色氨酸（tryptophan, Trp）补充对GLBA信号通路的影响。Trp是一种已知可调节性情的营养补充剂，本研究以湖羊为模型，选取性情差异明显的个体（安静型C与紧张型N），并设置Trp补充处理（T），形成四个实验组（C、CT、N、NT）。通过对瘤胃微生物群、结肠和肝脏代谢物以及脑内相关信号的综合分析，探索Trp通过GLBA影响性情的潜在机制。结果表明，Trp补充显著改变了瘤胃微生物群结构，其中Chloroflexi和Bdellovibrionota在补充组显著增加，Flexilinea在CT组富集，而Monoglobus和Sediminispirochaeta在NT组富集。其中特定菌群和门水平的丰度变化可能导致循环中短链脂肪酸（SCFAs）、氨基酸和Trp代谢物水平的改变，从而部分解释了此前观察到的Trp对紧张型湖羊性情改善的现象。结肠和肝脏样品的代谢组学分析进一步提示，这些组织中的氨基酸代谢及SCFAs可能参与了性情的表达。综上所述，本研究首次在绵羊中提供了饮食Trp通过GLBA依赖性通路影响行为的证据。研究结果强调SCFAs、Trp代谢物及微生物互作为关键介质，并提示GLBA可能是反刍动物性情调控的重要信号网络。这一发现不仅拓展了对GLBA与性情关系的认识，也表明基于个体性情差异的营养策略有望改善动物福利，并推动精准畜牧业的发展。

Abstract

Temperament, similarly to personality, is defined by a consistency in the response of an individual to a challenge, for example, calm or agitated responses. Temperament is partly determined by genetic factors but can also be modulated by internal factors that act on the brain pathways that control temperament. In monogastric animals, the gut-brain axis (GBA) influences temperament. Recently, it has been shown that signals from the liver can impact both brain function and the gut microbiome in a three-way interaction named the GLBA. The role of the liver in GLBA signalling in the expression of temperament is unknown. Here, we report the first broad investigation on the impact of dietary tryptophan (Trp), a supplement that is known to affect temperament, on the communication pathways of the GLBA in Hu sheep of calm (C) or nervous (N) temperaments. In the rumen, Trp supplementation (T) increased the abundance of Chloroflexi and Bdellovibrionota abundance, with Flexilinea enriched in CT and Monoglobus and Sediminispirochaeta enriched in NT. Changes in the abundance of specific genera and phyla probably caused the observed changes in circulating levels of SCFAs, amino acids, and tryptophan metabolites. Changes in the rumen microbiome could partly explain the impact of dietary Trp on the temperament of nervous Hu sheep that was observed previously. The results of a metabolomics analysis of samples from the colon microbiome and the liver suggests that amino acid metabolism and SCFAs from these two tissues could be involved in the expression of temperament. Our findings highlight the GLBA as a potential signalling network modulating temperament in ruminants, with SCFAs, Trp metabolites, and microbial interactions as key mediators. Our data provide the first evidence that, in sheep, Trp affects behaviour through GLBA-dependent pathways and suggest that nutritional strategies, tailored for individuals’ temperament, would improve welfare in precision livestock farming.

Keywords: Tryptophan microbiome temperament gut-brain axis

Online: 12 September 2025

Fund:

This work was supported by Research on the Dynamic Nutrient Requirements of Meat-Producing Livestock and the Development of Precision Nutrition Supply Models-National Key R&D Program of China (14th Five-Year Plan): “Key Technologies for Efficient Utilization of Feed and Forage and Carbon Emission Reduction in Cattle and Sheep” (2024YFD1300204), Postgraduate Research & Practice Innovation Program of Jiangsu Province (KYCX24_3808), Multi-omics Investigation of the Role of Gut Microbiota in Temperament Regulation in Altay Sheep-Ministry of Science and Technology, High-end Foreign Expert Program (G2023014066L), and the International Academic Exchange Fund for Graduate Students of Yangzhou University.

About author: Feifan Wu, E-mail: wffyzu@126.com; #Corresponding Mengzhi Wang, mengzhiwangyz@126.com.

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Feifan Wu, Luoyang Ding, Shane K Maloney, Dominique Blache, Mengzhi Wang. 2025. Temperament affects the impact of dietary tryptophan on the gut-liver-brain axis in sheep. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.09.015

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