Microbial communities on dry natural rocks are richer and less stressed than those on man-made playgrounds

Abstract

In modern urbanized societies, the incidence of major immune-mediated diseases is several times higher than before World War II. A potential explanation is that these diseases are triggered by limited possibilities to be exposed to rich environmental microbiota. This requires that the urban environment hosts less and poorer microbiota than the natural environment. The current study was designed to test the assumption that urban man-made environments host less and poorer environmental microbiota, compared to natural habitats. We selected two types of dry environments, natural rocks and playground rubber mats, both of which were used daily and extensively by children. In quantitative PCR and next-generation sequencing, bacterial abundance and richness were higher on the natural rocks than the rubber mats. Altogether, 67 amplicon sequence variants (ASVs) belonging mostly to Actinobacteria and Proteobacteria were indicative of rock microbiota, while three ASVs were indicative of rubber mats. Interestingly, bacteria formed more complex networks on rubber mats than natural rocks. Based on the literature, this indicates that the studied artificial dry environment is more challenging and stressful for bacterial communities than dry natural rocks. The results support the hypothesis that urban man-made environments host poor microbial communities, which is in accordance with the biodiversity hypothesis of immune-mediated diseases.IMPORTANCEThe current study provides new evidence that artificial urban play environments host poor microbial communities and provide a stressful environment for microbes, as compared to dry natural rocks. Through this, the current study underlines the need to enhance microbial diversity in urban areas, especially in outdoor play environments, which have a crucial role in providing essential microbial exposure for the development of children's immune system. This research can potentially offer guidance for urban planning and public health strategies that support planetary health.

Keywords: biodiversity hypothesis; microbial community composition; microbial exposure; planetary health; play environments; soil microbiota; urban environment; urban microbiome.

Fig 1

Gene copy numbers in dirt and dust sampled from natural rock (red) and artificial rubber mats (blue) at playgrounds situated in Lahti and Helsinki (Finland). Boxplots with solid outline show 16S rRNA gene copy number in all samples and dotted boxplots in paired samples. Mean (midline), upper and lower hinges (box), and minimum and maximum values (whiskers) are shown.

Fig 2

Co-occurrence networks formed by bacteria genera on (A) artificial rubber mats and (B) natural rocks visualized using co-occurrence network analysis. Statistics are shown in Table S2.

Fig 3

Observed richness of ASVs revealed in dust and dirt sampled from the artificial rubber mats (A1–A19) (blue) and natural rocks (N1–N9) (red). Paired samples (A1–A7 and N1–N7) are highlighted in the figure.

Fig 4

Observed richness of dominating phyla and classes (abundance ≥1%) of bacteria in dust and dirt samples from natural rock- (red) and artificial rubber mat-covered (blue) children’s playgrounds situated in Lahti and Helsinki (Finland). Panels A and B show richness of all samples, and panels C and D show richness of paired samples. Significance codes before P-value correction: *P < 0.05, **P < 0.01, and ***P < 0.001. Statistics are shown in Tables S4 and S5.

Fig 5

Shannon indices of dominating phyla and classes (abundance ≥1%) of bacteria in dust and dirt samples from natural rock- (red) and artificial rubber mat-covered (blue) children’s playgrounds situated in Lahti and Helsinki (Finland). Panels A and B show Shannon indices of all samples, and panels C and D show paired samples. Significance codes before P-value correction: *P < 0.05, **P < 0.01, and ***P < 0.001. Statistics are shown in Tables S7 and S8.

Fig 6

NMDS of the bacterial community composition in the artificial rubber mat samples (blue dots) and the natural rock samples (red dots). Subgroup highlighted with dashed outline (purple). Significance was determined by PERMANOVA (P = 0.487, F = 0.940, R² = 0.035) at the ASV level. Non-metric dimensional scaling ordination based on Bray-Curtis dissimilarity.