©2018 by Healthy Urban Microbiome Initiative.

Biodiverse green spaces: a prescription for global urban health

The world is urbanizing and chronic health conditions associated with urban living are on the rise. There is mounting evidence that people with a diverse microbiome (bacteria that inhabit the human body) or who interact with green spaces enjoy better health. However, studies have yet to directly examine how biodiverse urban green spaces (BUGS) might modify the human microbiome and reduce chronic disease. Here we highlight the potential for green spaces to improve health by exposing people to environmental microorganisms that diversify human microbiomes and help regulate immune function. We present four international perspectives (from Australia, China, India, and the UK) on the major challenges and benefits of using BUGS to alleviate health burdens. We propose solutions to these challenges and outline studies that can test the connections between BUGS, immune function, and human health and provide the evidence base for effective BUGS design and use. If further studies reinforce this hypothesis, then BUGS may become a viable tool to stem the global burden of urban‐associated chronic diseases.

Urban habitat restoration provides a human health benefit through microbiome rewilding: the Microbiome Rewilding Hypothesis

Restoration aims to return ecosystem services, including the human health benefits of exposure to green space. The loss of such exposure with urbanization and industrialization has arguably contributed to an increase in human immune dysregulation. The Biodiversity and Old Friends hypotheses have described the possible mechanisms of this relationship, and suggest that reduced exposure to diverse, beneficial microorganisms can result in negative health consequences. However, it is unclear whether restoration of biodiverse habitat can reverse this effect, and what role the environmental microbiome might have in such recovery. Here, we propose the Microbiome Rewilding Hypothesis, which specifically outlines that restoring biodiverse habitats in urban green spaces can rewild the environmental microbiome to a state that enhances primary prevention of human disease. We support our hypothesis with examples from allied fields, including a case study of active restoration that reversed the degradation of the soil bacterial microbiome of a former pasture. This case study used high-throughput amplicon sequencing of environmental DNA to assess the quality of a restoration intervention in restoring the soil bacterial microbiome. The method is rapid, scalable, and standardizable, and has great potential as a monitoring tool to assess functional outcomes of green-space restoration. Evidence for the Microbiome Rewilding Hypothesis will help motivate health professionals, urban planners, and restoration practitioners to collaborate and achieve co-benefits. Co-benefits include improved human health outcomes and investment opportunities for biodiversity conservation and restoration.

Revegetation rewilds the soil bacterial microbiome of an old field

Ecological restoration is a globally important and well‐financed management intervention used to combat biodiversity declines and land degradation. Most restoration aims to increase biodiversity towards a reference state, but there are concerns that intended outcomes are not reached due to unsuccessful interventions and land‐use legacy issues. Monitoring biodiversity recovery is essential to measure success; however, most projects remain insufficiently monitored. Current field‐based methods are hard to standardize and are limited in their ability to assess important components of ecosystems, such as bacteria. High‐throughput amplicon sequencing of environmental DNA (metabarcoding of eDNA) has been proposed as a cost‐effective, scalable and uniform ecological monitoring solution, but its application in restoration remains largely untested. Here we show that metabarcoding of soil eDNA is effective at demonstrating the return of the native bacterial community in an old field following native plant revegetation. Bacterial composition shifted significantly after 8 years of revegetation, where younger sites were more similar to cleared sites and older sites were more similar to remnant stands. Revegetation of the native plant community strongly impacted on the belowground bacterial community, despite the revegetated sites having a long and dramatically altered land‐use history (i.e. >100 years grazing). We demonstrate that metabarcoding of eDNA provides an effective way of monitoring changes in bacterial communities that would otherwise go unchecked with conventional monitoring of restoration projects. With further development, awareness of microbial diversity in restoration has significant scope for improving the efficacy of restoration interventions more broadly.

 

Fungi are key functional components of ecosystems (e.g. decomposers, symbionts), but are rarely included in restoration monitoring programs. Many fungi occur belowground, making them difficult to observe directly, but are observable with environmental DNA (eDNA) methods. Although eDNA approaches have been proposed as ecological monitoring tools for microbial diversity, their application to restoration projects is very limited. We used eDNA metabarcoding of fungal ITS barcodes on soil collected across a 10-year restoration chronosequence to explore fungal responses to restoration. We observed a dramatic shift in the fungal community towards that of the natural fungal community after just 10 years of active native plant revegetationAgaricomycetes and other Basidiomycota – involved in wood decay and ectomycorrhizal symbiosis – increased in rarefied sequence abundance in older restored sites. Ascomycota dominated the fungal community, but decreased in rarefied sequence abundance across the restoration chronosequence. Our results highlight eDNA metabarcoding as a useful restoration monitoring tool that allows quantification of changes in important fungal indicator groups linked with functional recovery and, being underground, are normally omitted in restoration monitoring.

Human contact with soil may be important for building and maintaining normal healthy immune defense mechanisms, however this idea remains untested at the population-level. In this continent-wide, cross-sectional study we examine the possible public health benefit of ambient exposures to soil of high cation exchange capacity (CEC), a surrogate for potential immunomodulatory soil microbial diversity. We compare distributions of normalized mean 2011/12–2012/13 age-standardized public hospital admission rates (cumulative incidence) for infectious and parasitic diseases across regional Australia (representing an average of 29,516 patients/year in 228 local government areas), within tertiles of socioeconomic status and soil exposure. To test the significance of soil CEC, we use probabilistic individual-level environmental exposure data (with or without soil), and group-level variables, in robust non-parametric multilevel modelling to predict disease rates in unseen groups. Our results show that in socioeconomically-deprived areas with high CEC soils, rates of infectious and parasitic disease are significantly lower than areas with low CEC soils. Also, health inequality (relative risk) due to socioeconomic status is significantly lower in areas with high CEC soils compared to low CEC soils (Δ relative risk = 0.47; 95% CI: 0.13, 0.82). Including soil exposure when modelling rates of infectious and parasitic disease significantly improves prediction performance, explaining an additional 7.5% (Δ r2 = 0.075; 95% CI: 0.05, 0.10) of variation in disease risk, in local government areas that were not used for model building. Our findings suggest that exposure to high CEC soils (typically high soil biodiversity) associates with reduced risk of infectious and parasitic diseases, particularly in lower socioeconomic areas.

Megatrends of urbanisation and reducing contact with natural environments may pose a largely unappreciated risk to human health, particularly in children, through declining normal (healthy) immunomodulatory environmental exposures. On the other hand, building knowledge of connections between environments, biodiversity and human health may offer new integrated ways of addressing global challenges of rising population health costs and declining biodiversity. In this study we are motivated to build insight and provide context and priority for emerging research into potential protective (e.g. immunomodulatory) environmental exposures. We use respiratory health as a test case to explore whether some types and qualities of environment may be more beneficial than others, and how such exposures may compare to known respiratory health influences, via a cross-sectional ecological epidemiology study for the continent of Australia. Using Lasso penalized regression (to interpret key predictors from many candidate variables) and 10-fold cross-validation modelling (to indicate reproducibility and uncertainty), within different socio-geographic settings, our results show surrogate measures of landscape biodiversity correlate with respiratory health, and rank amongst known predictors. A range of possible drivers for this relationship are discussed. Perhaps most novel and interesting of these is the possibility of protective immunomodulatory influence from microbial diversity (suggested by the understudied ‘biodiversity hypothesis’) and other bioactive agents associated with biodiverse environments. If beneficial influences can be demonstrated from biodiverse environments on immunomodulation and human health, there may be potential to design new cost-effective nature-based health intervention programs to reduce the risk of immune-related disease at a population level. Our approach and findings are also likely to have use in the evaluation of environment and health associations elsewhere.

 

Current evidence suggests that biodiverse environmental microbiomes contribute positively to human health and could account for known associations between urban green space and improved health. We summarise the state of knowledge that could inform the development of healthy urban microbiome initiatives (HUMI) to re-connect urban populations to biodiverse microbial communities.