Psychophysiological and Metabolomics Responses of Adults during Horticultural Activities Using Soil Inoculated with Streptomyces rimosus: A Pilot Study

Abstract

This study compared the physiological effects at a metabolomics level with autonomic nervous system responses in adults during soil mixing activities, based on the presence or absence of Streptomyces rimosus in the soil. Thirty adult participants performed soil mixing activities for 5 min using sterilized soil with culture media and Streptomyces rimosus, respectively. Blood samples were drawn twice from each participant after each activity. Electroencephalograms were measured during the activity. Serum metabolites underwent metabolite profiling by gas chromatography, followed by multivariate analyses. Serum brain-derived neurotrophic factor and C-reactive protein levels were measured by Enzyme-Linked Immunosorbent Assay. Soil-emitted volatile organic compounds were identified via solid-phase microextraction and gas chromatography-mass spectroscopy, followed by multivariate analyses. The volatile compound analysis revealed that the terpenoid and benzoid compounds, geosmin, and 2-methylisoborneol were greater in soil with Streptomyces rimosus. Serum metabolomics revealed that the treatment group (soil inoculated with Streptomyces rimosus) possessed relatively higher levels of serotonin compared to the control group (soil mixed with culture media), and serum C-reactive protein levels were significantly lower in the treatment group. In the treatment group, the electroencephalogram revealed that alpha band activity of the occipital lobe increased. This study concludes that Streptomyces rimosus soil contact can positively affect human metabolic and autonomic reactions. Therefore, this pilot study confirmed the possible role of soil microorganisms in horticultural activities for psychophysiological effects in humans.

Keywords: 2-methylisoborneol; C-reactive protein; brain-derived neurotrophic factor; electroencephalogram; gardening; geosmin; horticultural therapy; metabolite profiling; soil microorganism; volatile compounds.

Figure 1

Results of headspace solid-phase microextraction gas chromatography–time-of-flight–mass spectrometry datasets for various Streptomyces strain samples.

Figure 2

Room arrangement of the experiment.

Figure 3

Experiment protocol. EEG: electroencephalogram; SDM: comparisons via the Semantic Differential Method; Stress: subjective stress evaluation (NRS: numeral rating scale).

Figure 4

International electrode arrangement [20].

Figure 5

(A) Comparisons of the Semantic Differential Method (SDM) for each soil mixing activity. (B) Subjective stress evaluation. NRS, numeral rating scale. * p < 0.05, *** p < 0.001, ^NS p > 0.05 by the paired t-test, respectively. Values are the mean ± SD.

Figure 6

(A) Principal component analysis (PCA) and (B) partial least square discriminant analysis (PLS-DA) score plot derived from SPME–GC–TOF–MS datasets for various soil samples. Symbols: soil treated with distilled water (S, ▲); soil treated with culture media (SM, ▲); soil inoculated with S. rimosus (SS, ▲). (C) Heat map analysis for the relative abundance of different volatile organic compounds (VOCs) (VIP > 0.7, p < 0.05) derived from the GC–TOF–MS analysis. The colored squares (blue to red) indicate fold changes that are normalized by the average of each metabolite.

Figure 7

(A) Principal component analysis (PCA) and (B) partial least square discriminant analysis (PLS-DA) score plot derived from GC–TOF–MS datasets for serum samples. Symbols: control (soil treated with SM, ●); treatment (SS, ●). (C) Heat map analysis for the relative abundance of different serum metabolites (VIP > 1.0) derived from GC–TOF–MS analysis. The colored squares (blue to red) indicate fold changes that were normalized by the average of each metabolite. * Significantly different metabolite between the control and treatment groups (p < 0.05, Student’s t-test).

Figure 8

Results of (A) BDNF and (B) CRP levels in serum after the soil mixing activity with or without S. rimosus (n = 16 per group). Data were analyzed via paired t-test. * p < 0.05 compared to the sterilized soil group. Values are the mean ± SD.