Commensal Lactobacillus stimulates the intestinal methionine metabolism of weaning piglets by reshaping gut microbiota and metabolites

IF 5.2 2区 农林科学 Q1 AGRICULTURE, MULTIDISCIPLINARY
Woong Ji Lee, Anna Kang, Min-Jin Kwak, Sangdon Ryu, Hyeon-Jin Kim, Minho Song, Younghoon Kim
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引用次数: 0

Abstract

Background

The mammalian gastrointestinal tract hosts a complex microbiome essential for sustaining host health, particularly during pivotal stages such as weaning in piglets. Weaning represents a significant stressor, leading to substantial shifts in the gut microbiota composition and functionality. This study investigated the impact of weaning stress on the gut microbiome and metabolite profiles of piglets, focusing on how methionine supplementation influences gut health and physiological development.

Results

A multiomics approach that integrates metagenomics, metabolomics, culturomics, and transcriptomics was employed to characterize the gut microbiota before and after weaning. During the weaning period, weaning stress was characterized by a reduction in the abundance of beneficial bacteria in the gut, particularly a significant decrease in commensal Lactobacillus species, such as L. mucosae, L. reuteri, and L. amylovorus. Metabolomic analysis further revealed reductions in methionine and other metabolites associated with methionine metabolism and reductions in branched-chain amino acids (BCAAs) and lipid-related metabolites. Analysis of culture supernatants from Lactobacillus isolates demonstrated that these commensal Lactobacillus produced methionine, methionine-related metabolites, and BCAAs, highlighting a close relationship between methionine and commensal Lactobacillus abundance under weaning stress. Moreover, methionine supplementation in intestinal epithelial cells under methionine-deficient conditions led to the upregulation of genes related to methionine and pyruvate metabolism.

Conclusions

Weaning stress results in the simultaneous reduction of both commensal Lactobacillus abundance and methionine levels in the piglet gut, with a significant inter-relationship between these factors. Methionine supplementation shows potential in mitigating gut dysbiosis and metabolic disruptions induced by weaning stress.

Graphical abstract

共生乳杆菌通过重塑肠道菌群和代谢物来促进断奶仔猪肠道蛋氨酸代谢
哺乳动物胃肠道拥有复杂的微生物群,对维持宿主健康至关重要,特别是在关键阶段,如仔猪断奶。断奶是一个重要的应激源,导致肠道菌群组成和功能发生重大变化。本研究探讨了断奶应激对仔猪肠道微生物群和代谢物谱的影响,重点研究了蛋氨酸对仔猪肠道健康和生理发育的影响。结果采用综合宏基因组学、代谢组学、培养组学和转录组学的多组学方法对断奶前后的肠道微生物群进行了表征。在断奶期间,断奶应激的特点是肠道中有益菌的丰度减少,尤其是共生乳杆菌种类的显著减少,如粘膜乳杆菌、罗伊氏乳杆菌和淀粉状乳杆菌。代谢组学分析进一步显示蛋氨酸和其他与蛋氨酸代谢相关的代谢物减少,支链氨基酸(BCAAs)和脂质相关代谢物减少。对分离乳酸菌培养上清的分析表明,这些共生乳酸菌产生蛋氨酸、蛋氨酸相关代谢物和支链氨基酸,强调了断奶应激下蛋氨酸与共生乳酸菌丰度之间的密切关系。此外,在蛋氨酸缺乏的情况下,肠上皮细胞补充蛋氨酸会导致蛋氨酸和丙酮酸代谢相关基因的上调。结论断奶应激导致仔猪肠道共生乳酸菌丰度和蛋氨酸水平同时降低,且两者之间存在显著的相关关系。补充蛋氨酸显示出减轻断奶应激引起的肠道生态失调和代谢紊乱的潜力。图形抽象
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来源期刊
Chemical and Biological Technologies in Agriculture
Chemical and Biological Technologies in Agriculture Biochemistry, Genetics and Molecular Biology-Biotechnology
CiteScore
6.80
自引率
3.00%
发文量
83
审稿时长
15 weeks
期刊介绍: Chemical and Biological Technologies in Agriculture is an international, interdisciplinary, peer-reviewed forum for the advancement and application to all fields of agriculture of modern chemical, biochemical and molecular technologies. The scope of this journal includes chemical and biochemical processes aimed to increase sustainable agricultural and food production, the evaluation of quality and origin of raw primary products and their transformation into foods and chemicals, as well as environmental monitoring and remediation. Of special interest are the effects of chemical and biochemical technologies, also at the nano and supramolecular scale, on the relationships between soil, plants, microorganisms and their environment, with the help of modern bioinformatics. Another special focus is the use of modern bioorganic and biological chemistry to develop new technologies for plant nutrition and bio-stimulation, advancement of biorefineries from biomasses, safe and traceable food products, carbon storage in soil and plants and restoration of contaminated soils to agriculture. This journal presents the first opportunity to bring together researchers from a wide number of disciplines within the agricultural chemical and biological sciences, from both industry and academia. The principle aim of Chemical and Biological Technologies in Agriculture is to allow the exchange of the most advanced chemical and biochemical knowledge to develop technologies which address one of the most pressing challenges of our times - sustaining a growing world population. Chemical and Biological Technologies in Agriculture publishes original research articles, short letters and invited reviews. Articles from scientists in industry, academia as well as private research institutes, non-governmental and environmental organizations are encouraged.
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