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Background  Studies in developed countries have reported that the prevalence of asthma and rhinitis is higher in urban areas than in rural areas, and this phenomenon is associated with urbanization and changing indoor microbiome exposure. Developing countries such as China have experienced rapid urbanization in past years, but no study has investigated microbiome exposure and urban-rural health effects in these countries.    Methods  Nine high schools from urban and rural areas were randomly selected in Shanxi Province, China, and classroom vacuum dust was collected for shotgun metagenomic sequencing. A self-administered questionnaire was collected from 1332 students for personal information and health data. Three-level logistic regression was performed between microbial richness/abundance/functional pathways and the occurrence of asthma and rhinitis symptoms.    Results  Consistent with developed countries, the prevalence of wheeze and rhinitis was higher in urban areas than in rural areas (p < 0.05). Metagenomic profiling revealed 8302 bacterial, 395 archaeal, 744 fungal, 524 protist and 1103 viral species in classroom dust. Actinobacteria (mean relative abundance 49.7%), Gammaproteobacteria (18.4%) and Alphaproteobacteria (10.0%) were the most abundant bacterial classes. The overall microbiome composition was significantly different between urban and rural schools (p = 0.001, Adonis). Species from Betaproteobactera, Gammaproteobacteria and Bacilli were enriched in urban schools, and species from Actinobacteria and Cyanobacteria were enriched in rural schools. Potential pathogens were present in higher abundance in urban schools than in rural schools (p < 0.05).  Pseudoalteromonas ,  Neospora caninum  and  Microbacterium foliorum  were positively associated with the occurrence of wheeze, rhinitis and rhinoconjunctivitis, and  Brachybacterium  was protectively (negatively) associated with rhinitis (p < 0.01). The abundance of human endocrine and metabolic disease pathways was positively associated with rhinitis (p = 0.008), and butyrate and propionate metabolic genes and pathways were significantly enriched in rural schools (p < 0.005), in line with previous findings that these short-chain fatty acids protect against inflammatory diseases in the human gut.    Conclusions  We conducted the first indoor microbiome survey in urban/rural environments with shotgun metagenomics, and the results revealed high-resolution microbial taxonomic and functional profiling and potential health effects.Video abstractSupplementary Information  The online version contains supplementary material available at 10.1186/s40168-021-01091-0.

microbiome

Indoor bacterial, fungal and viral species and functional genes in urban and rural schools in Shanxi Province, China–association with asthma, rhinitis and rhinoconjunctivitis in high school students