Rural environment reduces allergic inflammation by modulating the gut microbiota
Zhaowei Yang,
Zhong Chen,
Xinliu Lin,
Siyang Yao,
Mo Xian,
Xiaoping Ning,
Wanyi Fu,
Mei Jiang,
Naijian Li,
Xiaojun Xiao,
Mulin Feng,
Zexuan Lian,
Wenqing Yang,
Xia Ren,
Zhenyu Zheng,
Jiefeng Zhao,
Nili Wei,
Wenju Lu,
Marjut Roponen,
Bianca Schaub,
Gary W. K. Wong,
Zhong Su,
Charles Wang,
Jing Li
Affiliations
Zhaowei Yang
Department of Allergy and Clinical Immunology, State Key Laboratory of Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong, P. R. China
Zhong Chen
Center for Genomics, School of Medicine, Loma Linda University, Loma Linda, CA USA
Xinliu Lin
Department of Allergy and Clinical Immunology, State Key Laboratory of Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong, P. R. China
Siyang Yao
Department of Allergy and Clinical Immunology, State Key Laboratory of Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong, P. R. China
Mo Xian
Department of Allergy and Clinical Immunology, State Key Laboratory of Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong, P. R. China
Xiaoping Ning
Department of Allergy and Clinical Immunology, State Key Laboratory of Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong, P. R. China
Wanyi Fu
Department of Allergy and Clinical Immunology, State Key Laboratory of Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong, P. R. China
Mei Jiang
Department of Allergy and Clinical Immunology, State Key Laboratory of Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong, P. R. China
Naijian Li
Department of Allergy and Clinical Immunology, State Key Laboratory of Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong, P. R. China
Xiaojun Xiao
State Key Laboratory of Respiratory Disease for Allergy at Shenzhen University, Shenzhen Key Laboratory of Allergy and Immunology, Shenzhen University School of Medicine, Shenzhen, China
Mulin Feng
Department of Allergy and Clinical Immunology, State Key Laboratory of Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong, P. R. China
Zexuan Lian
Department of Allergy and Clinical Immunology, State Key Laboratory of Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong, P. R. China
Wenqing Yang
Department of Allergy and Clinical Immunology, State Key Laboratory of Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong, P. R. China
Xia Ren
Department of Allergy and Clinical Immunology, State Key Laboratory of Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong, P. R. China
Zhenyu Zheng
Department of Allergy and Clinical Immunology, State Key Laboratory of Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong, P. R. China
Jiefeng Zhao
Department of Allergy and Clinical Immunology, State Key Laboratory of Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong, P. R. China
Nili Wei
Department of Allergy and Clinical Immunology, State Key Laboratory of Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong, P. R. China
Wenju Lu
Department of Allergy and Clinical Immunology, State Key Laboratory of Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong, P. R. China
Marjut Roponen
Department of Environmental Science, University of Eastern Finland, Kuopio, Finland
Bianca Schaub
Department of Pulmonary and Allergy, University Children’s Hospital Munich, LMU Munich, Munich, Germany
Gary W. K. Wong
Department of Paediatrics, Prince of Wales Hospital, the Chinese University of Hong Kong, Hong Kong, China
Zhong Su
State Key Laboratory of Respiratory Disease, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, Guangzhou, China
Charles Wang
Center for Genomics, School of Medicine, Loma Linda University, Loma Linda, CA USA
Jing Li
Department of Allergy and Clinical Immunology, State Key Laboratory of Respiratory Disease, Guangzhou Institute of Respiratory Health, the First Affiliated Hospital of Guangzhou Medical University, Guangzhou, Guangdong, P. R. China
Rural environments and microbiota are linked to a reduction in the prevalence of allergies. However, the mechanism underlying the reduced allergies modulated by rural residency is unclear. Here, we assessed gut bacterial composition and metagenomics in urban and rural children in the EuroPrevall-INCO cohort. Airborne dusts, including mattress and rural henhouse dusts, were profiled for bacterial and fungal composition by amplicon sequencing. Mice were repeatedly exposed to intranasal dust extracts and evaluated for their effects on ovalbumin (OVA)-induced allergic airway inflammation, and gut microbiota restoration was validated by fecal microbiota transplant (FMT) from dust-exposed donor mice. We found that rural children had fewer allergies and unique gut microbiota with fewer Bacteroides and more Prevotella. Indoor dusts in rural environments harbored higher endotoxin level and diversity of bacteria and fungi, whereas indoor urban dusts were enriched with Aspergillus and contained elevated pathogenic bacteria. Intranasal administration of rural dusts before OVA sensitization reduced respiratory eosinophils and blood IgE level in mice and also led to a recovery of gut bacterial diversity and Ruminiclostridium in the mouse model. FMT restored the protective effect by reducing OVA-induced lung eosinophils in recipient mice. Together, these results support a cause-effect relationship between exposure to dust microbiota and allergy susceptibility in children and mice. Specifically, rural environmental exposure modulated the gut microbiota, which was essential in reducing allergy in children from Southern China. Our findings support the notion that the modulation of gut microbiota by exposure to rural indoor dust may improve allergy prevention.
