Noora Ottman1, Lasse Ruokolainen2, Alina Suomalainen3, Hanna Sinkko4, Piia Karisola3, Jenni Lehtimäki2, Maili Lehto5, Ilkka Hanski2, Harri Alenius6, Nanna Fyhrquist7. 1. Department of Biosciences, University of Helsinki, Helsinki, Finland; Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden. 2. Department of Biosciences, University of Helsinki, Helsinki, Finland. 3. Department of Bacteriology and Immunology, University of Helsinki, Helsinki, Finland. 4. Faculty of Veterinary Medicine, Department of Equine and Small Animal Medicine, University of Helsinki, Helsinki, Finland. 5. Finnish Institute of Occupational Health, Helsinki, Finland. 6. Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden; Department of Bacteriology and Immunology, University of Helsinki, Helsinki, Finland. 7. Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden; Department of Bacteriology and Immunology, University of Helsinki, Helsinki, Finland. Electronic address: nanna.fyhrquist@ki.se.
Abstract
BACKGROUND: Sufficient exposure to natural environments, in particular soil and its microbes, has been suggested to be protective against allergies. OBJECTIVE: We aim at gaining more direct evidence of the environment-microbiota-health axis by studying the colonization of gut microbiota in mice after exposure to soil and by examining immune status in both a steady-state situation and during allergic inflammation. METHODS: The gastrointestinal microbiota of mice housed on clean bedding or in contact with soil was analyzed by using 16S rRNA gene sequencing, and the data were combined with immune parameters measured in the gut mucosa, lung tissue, and serum samples. RESULTS: We observed marked differences in the small intestinal and fecal microbiota composition between mice housed on clean bedding or in contact with soil, with a higher proportion of Bacteroidetes relative to Firmicutes in the soil group. The housing environment also influenced mouse intestinal gene expression, as shown by upregulated expression of the immunoregulatory markers IL-10, forkhead box P3, and cytotoxic T lymphocyte-associated protein 4 in the soil group. Importantly, using the murine asthma model, we found that exposure to soil polarizes the immune system toward TH1 and a higher level of anti-inflammatory signaling, alleviating TH2-type allergic responses. The inflammatory status of the mice had a marked influence on the composition of the gut microbiota, suggesting bidirectional communication along the gut-lung axis. CONCLUSION: Our results provide evidence of the role of environmentally acquired microbes in alleviating against TH2-driven inflammation, which relates to allergic diseases.
BACKGROUND: Sufficient exposure to natural environments, in particular soil and its microbes, has been suggested to be protective against allergies. OBJECTIVE: We aim at gaining more direct evidence of the environment-microbiota-health axis by studying the colonization of gut microbiota in mice after exposure to soil and by examining immune status in both a steady-state situation and during allergic inflammation. METHODS: The gastrointestinal microbiota of mice housed on clean bedding or in contact with soil was analyzed by using 16S rRNA gene sequencing, and the data were combined with immune parameters measured in the gut mucosa, lung tissue, and serum samples. RESULTS: We observed marked differences in the small intestinal and fecal microbiota composition between mice housed on clean bedding or in contact with soil, with a higher proportion of Bacteroidetes relative to Firmicutes in the soil group. The housing environment also influenced mouse intestinal gene expression, as shown by upregulated expression of the immunoregulatory markers IL-10, forkhead box P3, and cytotoxic T lymphocyte-associated protein 4 in the soil group. Importantly, using the murine asthma model, we found that exposure to soil polarizes the immune system toward TH1 and a higher level of anti-inflammatory signaling, alleviating TH2-type allergic responses. The inflammatory status of the mice had a marked influence on the composition of the gut microbiota, suggesting bidirectional communication along the gut-lung axis. CONCLUSION: Our results provide evidence of the role of environmentally acquired microbes in alleviating against TH2-driven inflammation, which relates to allergic diseases.
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