Interaction Between Rumen Microbiota and Epithelial Mitochondrial Dynamics in Tibetan Sheep: Elucidating the Mechanism of Rumen Epithelial Energy Metabolism

Investigating the functional interactions between rumen microbial fermentation and epithelial mitochondrial dynamics/energy metabolism in Tibetan sheep at different altitudes, this study examined ultrastructural changes in rumen epithelial tissues, expression levels of mitochondrial dynamics-related...

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Main Authors: Ying Xu, Yuzhu Sha, Xiaowei Chen, Qianling Chen, Xiu Liu, Yanyu He, Wei Huang, Yapeng He, Xu Gao
Format: Article
Language:English
Published: MDPI AG 2025-06-01
Series:BioTech
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Online Access:https://www.mdpi.com/2673-6284/14/2/43
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Summary:Investigating the functional interactions between rumen microbial fermentation and epithelial mitochondrial dynamics/energy metabolism in Tibetan sheep at different altitudes, this study examined ultrastructural changes in rumen epithelial tissues, expression levels of mitochondrial dynamics-related genes (fusion: <i>Mfn1</i>, <i>Mfn2</i>, <i>OPA1</i>, <i>Mic60</i>; fission: <i>Drp1</i>, <i>Fis1</i>, <i>MFF</i>), and ketogenesis pathway genes (<i>HMGS2</i>, <i>HMGCL</i>) in Tibetan sheep raised at three altitudes (TS 2500m, TS 3500m, TS 4500m). Correlation analysis was performed between rumen microbiota/metabolites and mitochondrial energy metabolism. Results: Ultrastructural variations were observed across altitudes. With increasing altitude, keratinized layer became more compact; desmosome connections between granular layer cells increased; mitochondrial quantity and distribution in spinous and basal layers increased. Mitochondrial dynamics regulation: Fission genes (<i>FIS1</i>, <i>DRP1</i>, <i>MFF</i>) showed significantly higher expression at TS 4500m (<i>p</i> < 0.01); fusion genes (<i>Mfn1</i>, <i>OPA1</i>) exhibited altitude-dependent upregulation. Energy metabolism markers: Pyruvate (PA) decreased significantly at TS 3500m/TS 4500m (<i>p</i> < 0.01); citrate (CA) increased with altitude; NAD<sup>+</sup> peaked at TS 3500m but decreased significantly at TS 4500m (<i>p</i> < 0.01); Complex II (SDH) and Complex IV (CO) activities decreased at TS 4500m (<i>p</i> < 0.01). Ketogenesis pathway: β-hydroxybutyrate increased significantly with altitude (<i>p</i> < 0.01); acetoacetate peaked at TS 2500 m/TS 4500 m; <i>HMGCS2</i> expression exceeded <i>HMGCL</i>, showing altitude-dependent upregulation at TS 4500m (<i>p</i> < 0.01). Microbiome–metabolism correlations: Butyrivibrio_2 and Fibrobacter negatively correlated with <i>Mic60</i> (<i>p</i> < 0.01); Ruminococcaceae_NK4A214_Group positively correlated with <i>Mfn1/OPA1</i> (<i>p</i> < 0.05); WGCNA identified 17 metabolite modules, with MEturquoise module positively correlated with <i>DRP1/Mfn2/MFF</i> (<i>p</i> < 0.05). Conclusion: Altitude-induced ultrastructural adaptations in rumen epithelium correlate with mitochondrial dynamics stability and ketogenesis upregulation. Mitochondrial fission predominates at extreme altitudes, while microbiota–metabolite interactions suggest compensatory energy regulation mechanisms.
ISSN:2673-6284