Naturally-diverse airborne environmental microbial exposures modulate the gut microbiome and may provide anxiolytic benefits in mice

Craig Liddicoat, Harrison Sydnor, Christian Cando-Dumancela, Romy Dresken, Jiajun Liu, Nicholas J.C. Gellie, Jacob G. Mills, Jennifer M. Young, Laura S. Weyrich, Mark R. Hutchinson, Philip Weinstein, Martin F. Breed

Research output: Contribution to journalArticle

Abstract

Growing epidemiological evidence links natural green space exposure with a range of health benefits, including for mental health. Conversely, greater urbanisation associates with increased risk of mental health disorders. Microbiomes are proposed as an important but understudied link that may help explain many green space-human health associations. However, there remains a lack of controlled experimental evidence testing possible beneficial effects from passive exposure to natural biodiversity via airborne microbiota. Previous mouse model studies have used unrealistic environmental microbial exposures—including excessive soil and organic matter contact, feed supplements and injections—to demonstrate host microbiota, immune biomarker, and behavioural changes. Here, in a randomised controlled experiment, we demonstrate that realistic exposures to trace-level dust from a high biodiversity soil can change mouse gut microbiota, in comparison to dust from low biodiversity soil or no soil (control) (n = 54 total mice, comprising 3 treatments × 18 mice, with 9 females + 9 males per group). Furthermore, we found a nominal soil-derived anaerobic spore-forming butyrate-producer, Kineothrix alysoides, was supplemented to a greater extent in the gut microbiomes of high biodiversity treatment mice. Also, increasing relative abundance of this rare organism correlated with reduced anxiety-like behaviour in the most anxious mice. Our results point to an intriguing new hypothesis: that biodiverse soils may represent an important supplementary source of butyrate-producing bacteria capable of resupplying the mammalian gut microbiome, with potential for gut health and mental health benefits. Our findings have potential to inform cost-effective population health interventions through microbiome-conscious green space design and, ultimately, the mainstreaming of biodiversity into health care.

Original languageEnglish (US)
Article number134684
JournalScience of the Total Environment
Volume701
DOIs
StatePublished - Jan 20 2020

Fingerprint

Anti-Anxiety Agents
Biodiversity
Health
biodiversity
mental health
Soils
soil
Butyrates
Dust
dust
health care
Biomarkers
biomarker
exposure
spore
relative abundance
Health care
urbanization
Biological materials
Bacteria

All Science Journal Classification (ASJC) codes

  • Environmental Engineering
  • Environmental Chemistry
  • Waste Management and Disposal
  • Pollution

Cite this

Liddicoat, Craig ; Sydnor, Harrison ; Cando-Dumancela, Christian ; Dresken, Romy ; Liu, Jiajun ; Gellie, Nicholas J.C. ; Mills, Jacob G. ; Young, Jennifer M. ; Weyrich, Laura S. ; Hutchinson, Mark R. ; Weinstein, Philip ; Breed, Martin F. / Naturally-diverse airborne environmental microbial exposures modulate the gut microbiome and may provide anxiolytic benefits in mice. In: Science of the Total Environment. 2020 ; Vol. 701.
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Liddicoat, C, Sydnor, H, Cando-Dumancela, C, Dresken, R, Liu, J, Gellie, NJC, Mills, JG, Young, JM, Weyrich, LS, Hutchinson, MR, Weinstein, P & Breed, MF 2020, 'Naturally-diverse airborne environmental microbial exposures modulate the gut microbiome and may provide anxiolytic benefits in mice', Science of the Total Environment, vol. 701, 134684. https://doi.org/10.1016/j.scitotenv.2019.134684

Naturally-diverse airborne environmental microbial exposures modulate the gut microbiome and may provide anxiolytic benefits in mice. / Liddicoat, Craig; Sydnor, Harrison; Cando-Dumancela, Christian; Dresken, Romy; Liu, Jiajun; Gellie, Nicholas J.C.; Mills, Jacob G.; Young, Jennifer M.; Weyrich, Laura S.; Hutchinson, Mark R.; Weinstein, Philip; Breed, Martin F.

In: Science of the Total Environment, Vol. 701, 134684, 20.01.2020.

Research output: Contribution to journalArticle

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T1 - Naturally-diverse airborne environmental microbial exposures modulate the gut microbiome and may provide anxiolytic benefits in mice

AU - Liddicoat, Craig

AU - Sydnor, Harrison

AU - Cando-Dumancela, Christian

AU - Dresken, Romy

AU - Liu, Jiajun

AU - Gellie, Nicholas J.C.

AU - Mills, Jacob G.

AU - Young, Jennifer M.

AU - Weyrich, Laura S.

AU - Hutchinson, Mark R.

AU - Weinstein, Philip

AU - Breed, Martin F.

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Y1 - 2020/1/20

N2 - Growing epidemiological evidence links natural green space exposure with a range of health benefits, including for mental health. Conversely, greater urbanisation associates with increased risk of mental health disorders. Microbiomes are proposed as an important but understudied link that may help explain many green space-human health associations. However, there remains a lack of controlled experimental evidence testing possible beneficial effects from passive exposure to natural biodiversity via airborne microbiota. Previous mouse model studies have used unrealistic environmental microbial exposures—including excessive soil and organic matter contact, feed supplements and injections—to demonstrate host microbiota, immune biomarker, and behavioural changes. Here, in a randomised controlled experiment, we demonstrate that realistic exposures to trace-level dust from a high biodiversity soil can change mouse gut microbiota, in comparison to dust from low biodiversity soil or no soil (control) (n = 54 total mice, comprising 3 treatments × 18 mice, with 9 females + 9 males per group). Furthermore, we found a nominal soil-derived anaerobic spore-forming butyrate-producer, Kineothrix alysoides, was supplemented to a greater extent in the gut microbiomes of high biodiversity treatment mice. Also, increasing relative abundance of this rare organism correlated with reduced anxiety-like behaviour in the most anxious mice. Our results point to an intriguing new hypothesis: that biodiverse soils may represent an important supplementary source of butyrate-producing bacteria capable of resupplying the mammalian gut microbiome, with potential for gut health and mental health benefits. Our findings have potential to inform cost-effective population health interventions through microbiome-conscious green space design and, ultimately, the mainstreaming of biodiversity into health care.

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