{"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.
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.