Effects of post-adulthood environmental hygiene improvement on gut microbiota and immune tolerance in mice.

IF 3.9 2区 生物学 Q2 BIOTECHNOLOGY & APPLIED MICROBIOLOGY Applied and Environmental Microbiology Pub Date : 2025-03-06 DOI:10.1128/aem.02477-24
Na Li, Mengjie Li, Honglin Zhang, Zhimao Bai, Zhongjie Fei, Yangyang Dong, Xinting Zhang, Pengfeng Xiao, Xiao Sun, Dongrui Zhou
{"title":"Effects of post-adulthood environmental hygiene improvement on gut microbiota and immune tolerance in mice.","authors":"Na Li, Mengjie Li, Honglin Zhang, Zhimao Bai, Zhongjie Fei, Yangyang Dong, Xinting Zhang, Pengfeng Xiao, Xiao Sun, Dongrui Zhou","doi":"10.1128/aem.02477-24","DOIUrl":null,"url":null,"abstract":"<p><p>Changes in diet, cleanliness, stress, and exercise patterns may contribute to the disappearance of various gut microbes in humans who relocate to developed countries from developing countries. To explore the impact of environmental cleanliness on the gut microbiota, adult mice housed in a general animal room were divided into three groups. The control group was subjected to an unchanged living environment, SPF mice were moved to a specific pathogen-free (SPF) animal room with higher environmental cleanliness, and SPFL (specific pathogen-free specific with a fecal leakage grid) mice were moved to the SPF animal room and reared in cages with the function of preventing mice from eating feces as much as possible. Metagenome sequencing results showed that the gut microbial diversity decreased after the environmental change, accompanied by a substantial loss in gut microbiota, including genera known to have protective effects against allergies and those involved in short-chain fatty acid production. Additionally, the abundance of functional genes involved in short-chain fatty acid metabolism, amino acid synthesis, vitamin metabolism, flagellar assembly, and bacterial chemotaxis decreased. The environmental hygiene improvement also resulted in significant increases in total serum IgE, IL-4, IL-5, and IL-13 levels in mice with artificially induced chronic inflammatory dermatosis. Compared with SPF mice, preventing mice from eating feces as much as possible decreased the gut microbial diversity but did not markedly change functional gene expression or total serum cytokine levels.</p><p><strong>Importance: </strong>Research has indicated that the human gut microbial diversity gradually decreases, while the prevalence of allergic diseases increases after movement from developing countries to developed countries. A healthy gut microbiota is necessary for proper human immune function. Movement from undeveloped to developed regions is often accompanied by an increase in environmental cleanliness. However, whether changes in environmental cleanliness are an important factor contributing to the decreased gut microbial diversity and increased prevalence of allergic diseases has not been reported. This study demonstrates the impact of increased environmental cleanliness on gut microbiota and susceptibility to allergic diseases and contributes to a better understanding of the increased incidence rate of various chronic diseases.</p>","PeriodicalId":8002,"journal":{"name":"Applied and Environmental Microbiology","volume":" ","pages":"e0247724"},"PeriodicalIF":3.9000,"publicationDate":"2025-03-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Applied and Environmental Microbiology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1128/aem.02477-24","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"BIOTECHNOLOGY & APPLIED MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0

Abstract

Changes in diet, cleanliness, stress, and exercise patterns may contribute to the disappearance of various gut microbes in humans who relocate to developed countries from developing countries. To explore the impact of environmental cleanliness on the gut microbiota, adult mice housed in a general animal room were divided into three groups. The control group was subjected to an unchanged living environment, SPF mice were moved to a specific pathogen-free (SPF) animal room with higher environmental cleanliness, and SPFL (specific pathogen-free specific with a fecal leakage grid) mice were moved to the SPF animal room and reared in cages with the function of preventing mice from eating feces as much as possible. Metagenome sequencing results showed that the gut microbial diversity decreased after the environmental change, accompanied by a substantial loss in gut microbiota, including genera known to have protective effects against allergies and those involved in short-chain fatty acid production. Additionally, the abundance of functional genes involved in short-chain fatty acid metabolism, amino acid synthesis, vitamin metabolism, flagellar assembly, and bacterial chemotaxis decreased. The environmental hygiene improvement also resulted in significant increases in total serum IgE, IL-4, IL-5, and IL-13 levels in mice with artificially induced chronic inflammatory dermatosis. Compared with SPF mice, preventing mice from eating feces as much as possible decreased the gut microbial diversity but did not markedly change functional gene expression or total serum cytokine levels.

Importance: Research has indicated that the human gut microbial diversity gradually decreases, while the prevalence of allergic diseases increases after movement from developing countries to developed countries. A healthy gut microbiota is necessary for proper human immune function. Movement from undeveloped to developed regions is often accompanied by an increase in environmental cleanliness. However, whether changes in environmental cleanliness are an important factor contributing to the decreased gut microbial diversity and increased prevalence of allergic diseases has not been reported. This study demonstrates the impact of increased environmental cleanliness on gut microbiota and susceptibility to allergic diseases and contributes to a better understanding of the increased incidence rate of various chronic diseases.

查看原文
分享 分享
微信好友 朋友圈 QQ好友 复制链接
本刊更多论文
求助全文
约1分钟内获得全文 去求助
来源期刊
Applied and Environmental Microbiology
Applied and Environmental Microbiology 生物-生物工程与应用微生物
CiteScore
7.70
自引率
2.30%
发文量
730
审稿时长
1.9 months
期刊介绍: Applied and Environmental Microbiology (AEM) publishes papers that make significant contributions to (a) applied microbiology, including biotechnology, protein engineering, bioremediation, and food microbiology, (b) microbial ecology, including environmental, organismic, and genomic microbiology, and (c) interdisciplinary microbiology, including invertebrate microbiology, plant microbiology, aquatic microbiology, and geomicrobiology.
期刊最新文献
Comparative analysis of environmental persistence of SARS-CoV-2 variants and seasonal coronaviruses. Deletion of Re-citrate synthase allows for analysis of contributions of tricarboxylic acid cycle directionality to the growth of Heliomicrobium modesticaldum. Effects of post-adulthood environmental hygiene improvement on gut microbiota and immune tolerance in mice. Sulfate assimilation regulates antioxidant defense response of the cyanobacterium Synechococcus elongatus PCC 7942 to high concentrations of carbon dioxide. Computer-directed rational engineering of dioxygenase TcsAB for triclosan biodegradation under cold conditions.
×
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
现在去查看 取消
×
提示
确定
0
微信
客服QQ
Book学术公众号 扫码关注我们
反馈
×
意见反馈
请填写您的意见或建议
请填写您的手机或邮箱
已复制链接
已复制链接
快去分享给好友吧!
我知道了
×
扫码分享
扫码分享
Book学术官方微信
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术
文献互助 智能选刊 最新文献 互助须知 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 Book学术 All rights reserved.
ghs 京公网安备 11010802042870号 京ICP备2023020795号-1