Introducing the Microbiome Rewilding Hypothesis and testing its influence on environmental and human microbiomes

Jacob G. Mills, Andrew J. Lowe, Philip Weinstein, Nicholas J.C. Gellie, Laura S. Weyrich, Caitlin A. Selway, Martin F. Breed 

ABSTRACT

Restoration often aims to return ecosystem services – including human health benefits. Chronic inflammatory diseases have increased remarkably with urbanisation and a growing body of evidence suggests that reduced exposure to healthy environmental microbiomes results in negative health consequences. Reversing this trend may require returning ecosystem services to the urban landscape. However, it is unclear whether restoration of biodiverse urban habitat can rewild the environmental microbiome and influence the human microbiome. We propose the Microbiome Rewilding Hypothesis: planting biodiverse habitat in urban green spaces rewilds the environmental microbiome and benefits human health as a primary prevention ecosystem service. To test this hypothesis, we sampled environments and humans in three replicates of five urban green space ecotypes in the City of Playford, Adelaide, Australia. We generated rarefied bacterial 16S rRNA amplicon data for soil, leaf-surface, air, and human skin and nasal environments for community analysis. We used analysis of composition of microbes (ANCOM) to explore which bacterial OTUs changed significantly in abundance in human microbiomes. We demonstrate that revegetation returns the environmental microbiome to closely resemble that of remnant vegetation. We also show that human microbiomes change with time spent in urban green spaces. Additionally, several important human commensal and pathogenic bacteria were found to significantly differ in human microbiomes after green space exposure (ANCOM FDR-adjusted P < 0.05). Our study provides early evidence to suggest that restoration of urban green spaces can potentially return human health benefits as an ecosystem service, and encourages further testing of the Microbiome Rewilding Hypothesis.