The interaction between rumen microbiota and neurotransmitters plays an important role in the adaptation of phenological changes in Tibetan sheep

Abstract The gut-brain axis is regarded as the “second brain” of the host. Gut microbiota and their metabolites affect intestinal homeostasis, function, and phenotype by regulating bidirectional communication between the gut and brain. This serves as a vital strategy for understanding how gut microb...

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Main Authors: Wei Huang, Yuzhu Sha, Qianling Chen, Xiaowei Chen, Min Gao, Xiu Liu, Yapeng He, Xu Gao, Jiang Hu, Jiqing Wang, Shaobin Li, Zhiyun Hao, Yanyu He
Format: Article
Language:English
Published: BMC 2025-05-01
Series:BMC Veterinary Research
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Online Access:https://doi.org/10.1186/s12917-025-04823-8
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author Wei Huang
Yuzhu Sha
Qianling Chen
Xiaowei Chen
Min Gao
Xiu Liu
Yapeng He
Xu Gao
Jiang Hu
Jiqing Wang
Shaobin Li
Zhiyun Hao
Yanyu He
author_facet Wei Huang
Yuzhu Sha
Qianling Chen
Xiaowei Chen
Min Gao
Xiu Liu
Yapeng He
Xu Gao
Jiang Hu
Jiqing Wang
Shaobin Li
Zhiyun Hao
Yanyu He
author_sort Wei Huang
collection DOAJ
description Abstract The gut-brain axis is regarded as the “second brain” of the host. Gut microbiota and their metabolites affect intestinal homeostasis, function, and phenotype by regulating bidirectional communication between the gut and brain. This serves as a vital strategy for understanding how gut microbiota regulate nutrient metabolism and adaptability in animals. This study explored the metabolic mechanisms through which Tibetan sheep adapt to high-altitude environments via the rumen microbiota-gut-brain axis across different phenological periods (returning-green period, fresh grass period and withered grass period). By analyzing metabolic indicators, neurotransmitters, and gene and protein expression in serum, rumen, adipose, and hypothalamic tissues, we discovered that energy metabolism markers (creatine kinase, lactate dehydrogenase, glucose) and immunoglobulins (IgG, IgM) in the serum were significantly elevated during the fresh grass period (P < 0.05). In contrast, thyroid hormones T3 and T4 were at higher levels during the returning-green period (P < 0.05). The density of rumen fiber-degrading bacteria was higher during the returning-green period (P < 0.05). Meanwhile, the densities of Butyrivibrio fibrisolvens, Selenomonas ruminantium, and Treponema bryantii microbiota significantly during the fresh grass period and were positively correlated with isovaleric acid concentration (P < 0.05). Neurotransmitters (5-HT, DOPAC, 5-HIAA, and NE) were significantly elevated in both the rumen epithelium and hypothalamus during the fresh grass period (P < 0.05). The analysis of the cAMP-PKA-pCREB pathway showed that the genes and proteins of UCP1, PKA, and CREB1 were highly expressed in adipose tissue during the fresh grass and withered grass periods, and there significant negative correlations to specific microbiota (P < 0.05). In summary, Tibetan sheep adapt to high-altitude environments through the rumen microbiota-gut-brain axis, regulating metabolic and neurotransmitter changes to establish a unique metabolic adaptation mechanism.
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spelling doaj-art-584f0faf0e0f46b9a504a1344a344f212025-08-20T03:22:07ZengBMCBMC Veterinary Research1746-61482025-05-0121111510.1186/s12917-025-04823-8The interaction between rumen microbiota and neurotransmitters plays an important role in the adaptation of phenological changes in Tibetan sheepWei Huang0Yuzhu Sha1Qianling Chen2Xiaowei Chen3Min Gao4Xiu Liu5Yapeng He6Xu Gao7Jiang Hu8Jiqing Wang9Shaobin Li10Zhiyun Hao11Yanyu He12College of Animal Science and Technology, Gansu Agricultural UniversityCollege of Animal Science and Technology, Gansu Agricultural UniversityCollege of Animal Science and Technology, Gansu Agricultural UniversityCollege of Animal Science and Technology, Gansu Agricultural UniversityCollege of Animal Science and Technology, Gansu Agricultural UniversityCollege of Animal Science and Technology, Gansu Agricultural UniversityCollege of Animal Science and Technology, Gansu Agricultural UniversityCollege of Animal Science and Technology, Gansu Agricultural UniversityCollege of Animal Science and Technology, Gansu Agricultural UniversityCollege of Animal Science and Technology, Gansu Agricultural UniversityCollege of Animal Science and Technology, Gansu Agricultural UniversityCollege of Animal Science and Technology, Gansu Agricultural UniversitySchool of Fundamental Sciences, Massey UniversityAbstract The gut-brain axis is regarded as the “second brain” of the host. Gut microbiota and their metabolites affect intestinal homeostasis, function, and phenotype by regulating bidirectional communication between the gut and brain. This serves as a vital strategy for understanding how gut microbiota regulate nutrient metabolism and adaptability in animals. This study explored the metabolic mechanisms through which Tibetan sheep adapt to high-altitude environments via the rumen microbiota-gut-brain axis across different phenological periods (returning-green period, fresh grass period and withered grass period). By analyzing metabolic indicators, neurotransmitters, and gene and protein expression in serum, rumen, adipose, and hypothalamic tissues, we discovered that energy metabolism markers (creatine kinase, lactate dehydrogenase, glucose) and immunoglobulins (IgG, IgM) in the serum were significantly elevated during the fresh grass period (P < 0.05). In contrast, thyroid hormones T3 and T4 were at higher levels during the returning-green period (P < 0.05). The density of rumen fiber-degrading bacteria was higher during the returning-green period (P < 0.05). Meanwhile, the densities of Butyrivibrio fibrisolvens, Selenomonas ruminantium, and Treponema bryantii microbiota significantly during the fresh grass period and were positively correlated with isovaleric acid concentration (P < 0.05). Neurotransmitters (5-HT, DOPAC, 5-HIAA, and NE) were significantly elevated in both the rumen epithelium and hypothalamus during the fresh grass period (P < 0.05). The analysis of the cAMP-PKA-pCREB pathway showed that the genes and proteins of UCP1, PKA, and CREB1 were highly expressed in adipose tissue during the fresh grass and withered grass periods, and there significant negative correlations to specific microbiota (P < 0.05). In summary, Tibetan sheep adapt to high-altitude environments through the rumen microbiota-gut-brain axis, regulating metabolic and neurotransmitter changes to establish a unique metabolic adaptation mechanism.https://doi.org/10.1186/s12917-025-04823-8PhylogenyTibetan sheepRumen microbiotaNeurotransmitters
spellingShingle Wei Huang
Yuzhu Sha
Qianling Chen
Xiaowei Chen
Min Gao
Xiu Liu
Yapeng He
Xu Gao
Jiang Hu
Jiqing Wang
Shaobin Li
Zhiyun Hao
Yanyu He
The interaction between rumen microbiota and neurotransmitters plays an important role in the adaptation of phenological changes in Tibetan sheep
BMC Veterinary Research
Phylogeny
Tibetan sheep
Rumen microbiota
Neurotransmitters
title The interaction between rumen microbiota and neurotransmitters plays an important role in the adaptation of phenological changes in Tibetan sheep
title_full The interaction between rumen microbiota and neurotransmitters plays an important role in the adaptation of phenological changes in Tibetan sheep
title_fullStr The interaction between rumen microbiota and neurotransmitters plays an important role in the adaptation of phenological changes in Tibetan sheep
title_full_unstemmed The interaction between rumen microbiota and neurotransmitters plays an important role in the adaptation of phenological changes in Tibetan sheep
title_short The interaction between rumen microbiota and neurotransmitters plays an important role in the adaptation of phenological changes in Tibetan sheep
title_sort interaction between rumen microbiota and neurotransmitters plays an important role in the adaptation of phenological changes in tibetan sheep
topic Phylogeny
Tibetan sheep
Rumen microbiota
Neurotransmitters
url https://doi.org/10.1186/s12917-025-04823-8
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