Soil exposure modifies the gut microbiota and supports immune tolerance in a mouse model

Publication date: Available online 7 August 2018

Source: Journal of Allergy and Clinical Immunology

Author(s): Noora Ottman, Lasse Ruokolainen, Alina Suomalainen, Hanna Sinkko, Piia Karisola, Jenni Lehtimäki, Maili Lehto, Ilkka Hanski, Harri Alenius, Nanna Fyhrquist

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 T_H1 and a higher level of anti-inflammatory signaling, alleviating T_H2-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 T_H2-driven inflammation, which relates to allergic diseases.

Graphical abstract

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