Environmental biodiversity, human microbiota, and allergy are interrelated

Abstract

Rapidly declining biodiversity may be a contributing factor to another global megatrend--the rapidly increasing prevalence of allergies and other chronic inflammatory diseases among urban populations worldwide. According to the "biodiversity hypothesis," reduced contact of people with natural environmental features and biodiversity may adversely affect the human commensal microbiota and its immunomodulatory capacity. Analyzing atopic sensitization (i.e., allergic disposition) in a random sample of adolescents living in a heterogeneous region of 100 × 150 km, we show that environmental biodiversity in the surroundings of the study subjects' homes influenced the composition of the bacterial classes on their skin. Compared with healthy individuals, atopic individuals had lower environmental biodiversity in the surroundings of their homes and significantly lower generic diversity of gammaproteobacteria on their skin. The functional role of the gram-negative gammaproteobacteria is supported by in vitro measurements of expression of IL-10, a key anti-inflammatory cytokine in immunologic tolerance, in peripheral blood mononuclear cells. In healthy, but not in atopic, individuals, IL-10 expression was positively correlated with the abundance of the gammaproteobacterial genus Acinetobacter on the skin. These results raise fundamental questions about the consequences of biodiversity loss for both allergic conditions and public health in general.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Relationship between the generic composition of skin microbiota and land use types around the home. The vertical axis shows PC2bac, which correlates positively with the generic diversity of proteobacteria and negatively with the diversity of all other bacterial classes (SI Appendix, Table S2). The horizontal axis shows PC1env, which summarizes variation in land use types within a 3-km radius of the homes of the study subjects and is positively correlated with forests and agricultural land (SI Appendix, Table S1). Regression: F = 9.12, df = 1.93, P = 0.0033.

Fig. 2.

Relationships among environmental biodiversity, skin microbiota, and atopy in the study subjects. (A) The number of uncommon native flowering plant species plotted against the total number of plant species in the yard of atopic individuals (solid symbols) and healthy individuals (open symbols). The number of plant species on the vertical axis is the residual accounting for variation in the results of five pairs of field assistants. The effect of atopy is significant (t = −3.14, P = 0.0022, n = 94; without correcting for the effect of field assistants, t = −2.83, P = 0.0058). (B) The number of genera of gammaproteobacteria plotted against the total number of bacterial genera in the skin microbiota of atopic individuals (solid symbols) and healthy individuals (open symbols). The effect of atopy is highly significant (t = −3.72, P = 0.0003, n = 112).

Fig. 3.

Cytokine IL-10 expression against the relative abundance of Acinetobacter in the skin community of healthy (open symbols) and atopic individuals (filled dots). The interaction term is highly significant (P = 0.0009 in a linear regression model, with adjusted R2 = 0.23) (SI Appendix, Table S8).

Fig. 4.

Summary graph of the associations among environmental biodiversity, skin microbiota, and atopy. The solid arrows refer to the results in Figs. 1–3 and Table 2. The dashed-line arrow indicates a less significant effect of PC1env on the generic diversity of gammaproteobacteria (t = 1.91, P = 0.059, n = 95, with total number of bacterial genera as a covariate as in Fig. 2B).