Human Health & Plants Research: Contact with the Soil Microbiome during Gardening Alters the Skin Microbiota and Influences IL-10 Cytokine Levels

Dr. Charles Guy

Forest bathing and gardening are suspected of facilitating exposure to environmental volatile organic compounds of biogenic origin and/or the soil microbiome, which may potentially contribute to the therapeutic health benefits of such activities.  However, available empirical evidence relating to the underlying putative therapeutic agents’ identity and mode of action is extremely limited.

The recent double-blinded “placebo”-controlled study by Saarenpää and colleagues1 is a significant milestone in understanding the effects of gardening and soil exposure on human health.  This one-month randomized trial introduced two gardening treatments: a microbially diverse soil medium and a planting “placebo” consisting of a relatively microbially poor soil medium.  The key distinction between the two soil media was the inclusion of a microbial-rich compost in the base treatment medium, which was blended with horticultural peat and clay pebbles.  The bacterial diversity of the placebo soil was estimated to be 1.3 x 108 16S rDNA sequences per gram, while the treatment soil had 3.5 x 109 16S rDNA sequences per gram.

Volunteers for this study underwent a comprehensive exclusion screening, which rigorously covered various health conditions and lifestyle factors.  This included immunological disorders, diabetes, neurological disorders, daily smoking, indoor pet ownership, and living on a farm.  The Placebo group consisted of 13 participants, 10 of whom were female, while the Treatment group had 15 participants, 11 of whom were female.  The stringent screening process was a crucial aspect of the study, helping to reduce variation and reliability despite the small number of participants.

All participants were given the same set of tasks, which included contact with the soil and consuming the harvested produce.  They received a plant palette of the same seven crop species, horticultural supplies, and detailed instructions.  Their daily tasks involved barehanded exposure to the soil, testing the soil moisture level, and consuming the harvested produce. This hands-on approach allowed for a more comprehensive understanding of the effects of gardening and soil exposure on human health.

A trained nurse collected back-of-the-hand skin swab samples at the beginning and end of the indoor gardening period to analyze bacterial DNA abundance and taxonomic diversity.  The V4 region of the 16S rRNA of the bacterial genome was amplified by PCR and then sequenced using the Illumina MiSeq platform.

Participant blood samples were also collected to analyze several cytokines, including IL-1b, IL-6, IL-10, IL-17A, IL-21, TGF-b1, and TNF-α.  These immune system-modulating cytokines were selected to monitor anti-inflammatory, proinflammatory, and multifunctional regulation of immune system cells’ growth, differentiation, and activity.

The Shannon Diversity Index was used to measure the number of different bacterial taxonomic units present in the two types of soil: placebo and treatment.  Of course, the Shannon diversity was markedly greater and increased for the treatment soil compared to the placebo soil, specifically for the phyla Proteobacteria, Bacteroidetes, Planctomycetes, Cyanobacteria, Verrucomicrobia, and class Bacteroidia.  The Shannon Diversity increased during the trial for the treatment soil but showed no difference over time for the placebo soil.  In contrast, the topological patterns of skin bacterial co-occurrence networks increased over time in the trial for participants assigned to the placebo and the treatment soil groups.  However, as the skin bacterial Shannon Diversity and complexity of the co-occurrence networks increased for the treatment group, there was a comparable quantitative increase in the participant IL-10 cytokine levels.  There was a similar response for IL-17A in the treatment group, but the increases did not reach statistical significance.

This study is important because, for the first time, it demonstrated that contact with the soil, while engaged in controlled indoor gardening, can alter the skin’s microbial diversity and influence cytokine levels that may lead to modulation of immune system function.  Therefore, this study begins and justifies the journey of how gardening can lead to changes in a gardener’s microbiome, identifying the taxa responsible for mediating therapeutic benefit and connecting the nature of the mode of action providing the therapeutic benefit.  The impact of this otherwise important study was limited by the small population size that reduced the statistical power to distinguish potential biologically important changes in cytokine levels and immune system modulation.  Nevertheless, the present study’s findings clearly warrant a much larger trial with a more demographically representative participant population to better test the connection of the therapeutic basis of gardening-facilitated contact with soil, its microbiome, and resultant health benefits.

1Saarenpää, M., Roslund, M. I., Nurminen, N., Puhakka, R., Kummola, L., Laitinen, O. H., Hyöty, H., Sinkkonen, A. (2024).  Urban indoor gardening enhances immune regulation and diversifies skin microbiota—A placebo-controlled double-blinded intervention study.  Environment International, 187, 108705.  https://doi.org/10.1016/j.envint.2024.108705

Charles Guy, Emeritus and Courtesy Professor

Department of Environmental Horticulture, University of Florida

Steering Committee, Wilmot Botanical Gardens, University of Florida