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
{"title":"Commensal Lactobacillus stimulates the intestinal methionine metabolism of weaning piglets by reshaping gut microbiota and metabolites","authors":"Woong Ji Lee,&nbsp;Anna Kang,&nbsp;Min-Jin Kwak,&nbsp;Sangdon Ryu,&nbsp;Hyeon-Jin Kim,&nbsp;Minho Song,&nbsp;Younghoon Kim","doi":"10.1186/s40538-025-00771-5","DOIUrl":null,"url":null,"abstract":"<div><h3>Background</h3><p>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.</p><h3>Results</h3><p>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 <i>Lactobacillus</i> species, such as <i>L. mucosae</i>, <i>L. reuteri</i>, and <i>L. amylovorus</i>. 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 <i>Lactobacillus</i> isolates demonstrated that these commensal <i>Lactobacillus</i> produced methionine, methionine-related metabolites, and BCAAs, highlighting a close relationship between methionine and commensal <i>Lactobacillus</i> 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.</p><h3>Conclusions</h3><p>Weaning stress results in the simultaneous reduction of both commensal <i>Lactobacillus</i> 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.</p><h3>Graphical abstract</h3>\n<div><figure><div><div><picture><source><img></source></picture></div></div></figure></div></div>","PeriodicalId":512,"journal":{"name":"Chemical and Biological Technologies in Agriculture","volume":"12 1","pages":""},"PeriodicalIF":5.2000,"publicationDate":"2025-04-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://chembioagro.springeropen.com/counter/pdf/10.1186/s40538-025-00771-5","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Chemical and Biological Technologies in Agriculture","FirstCategoryId":"97","ListUrlMain":"https://link.springer.com/article/10.1186/s40538-025-00771-5","RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"AGRICULTURE, MULTIDISCIPLINARY","Score":null,"Total":0}
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

求助全文
约1分钟内获得全文 求助全文
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.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信