Exposure to a diverse environmental microbiome is thought to play an important role in "educating" the immune system and facilitating competitive exclusion of pathogens to maintain human health. ...Vegetation and soil are key sources of airborne microbiota--the aerobiome. A limited number of studies have attempted to characterize the dynamics of near surface green space aerobiomes, and no studies to date have investigated these dynamics from a vertical perspective. Vertical stratification in the aerobiome could have important implications for public health and for the design, engineering, and management of urban green spaces.
The primary objectives of this study were to:
) assess whether significant vertical stratification in bacterial species richness and evenness (alpha diversity) of the aerobiome occurred in a parkland habitat in Adelaide, South Australia;
) assess whether significant compositional differences (beta diversity) between sampling heights occurred; and
) to preliminarily assess whether there were significant altitudinal differences in potentially pathogenic and beneficial bacterial taxa.
We combined an innovative columnar sampling method at soil level, 0.0, 0.5, 1.0, and
, using passive petri dish sampling to collect airborne bacteria. We used a geographic information system (GIS) to select study sites, and we used high-throughput sequencing of the bacterial 16S rRNA gene to assess whether significant vertical stratification of the aerobiome occurred.
Our results provide evidence of vertical stratification in both alpha and beta (compositional) diversity of airborne bacterial communities, with diversity decreasing roughly with height. We also found significant vertical stratification in potentially pathogenic and beneficial bacterial taxa.
Although additional research is needed, our preliminary findings point to potentially different exposure attributes that may be contingent on human height and activity type. Our results lay the foundations for further research into the vertical characteristics of urban green space aerobiomes and their implications for public health and urban planning. https://doi.org/10.1289/EHP7807.
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•The effect of biodiverse aerobiomes on gut microbiota was previously untested.•We demonstrate that exposure to biodiverse soil dust modulates mouse gut microbiota.•Biodiverse soil ...exposure may help supplement butyrate-producing bacteria in the gut.•These bacteria appear to moderate anxiety-like behaviour in the most anxious mice.•We suggest a new hypothesis linking biodiverse soils, gut health and mental health.
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.
Exposure to biodiverse aerobiomes supports human health, but it is unclear which ecological factors influence exposure. Few studies have investigated near-surface green space aerobiome dynamics, and ...no studies have reported aerobiome vertical stratification in different urban green spaces. We used columnar sampling and next generation sequencing of the bacterial 16S rRNA gene, combined with geospatial and network analyses to investigate urban green space aerobiome spatio-compositional dynamics. We show a strong effect of habitat on bacterial diversity and network complexity. We observed aerobiome vertical stratification and network complexity that was contingent on habitat type. Tree density, closer proximity, and canopy coverage associated with greater aerobiome alpha diversity. Grassland aerobiomes exhibited greater proportions of putative pathogens compared to scrub, and also stratified vertically. We provide novel insights into the urban ecosystem with potential importance for public health, whereby the possibility of differential aerobiome exposures appears to depend on habitat type and height in the airspace. This has important implications for managing urban landscapes for the regulation of aerobiome exposure.
Understanding how microbial communities change with environmental degradation and restoration may offer new insights into the understudied ecology that connects humans, microbiota, and the natural ...world. Immunomodulatory microbial diversity and ‘Old Friends’ are thought to be supplemented from biodiverse natural environments, yet deficient in anthropogenically disturbed or degraded environments. However, few studies have compared the microbiomes of natural vs. human-altered environments and there is little knowledge of which microbial taxa are representative of ecological restoration—i.e. the assisted recovery of degraded ecosystems typically towards a more natural, biodiverse state. Here we use novel bootstrap-style resampling of site-level soil bacterial 16S rRNA gene environmental DNA data to identify genus-level indicators of restoration from a 10-year grassy eucalypt woodland restoration chronosequence at Mt Bold, South Australia. We found two key indicator groups emerged: ‘opportunistic taxa’ that decreased in relative abundance with restoration and more stable and specialist, ‘niche-adapted taxa’ that increased. We validated these results, finding seven of the top ten opportunists and eight of the top ten niche-adapted taxa displayed consistent differential abundance patterns between human-altered vs. natural samples elsewhere across Australia. Extending this, we propose a two-dimensional mapping for ecosystem condition based on the proportions of these divergent indicator groups. We also show that restoring a more biodiverse ecosystem at Mt Bold has increased the potentially immune-boosting environmental microbial diversity. Furthermore, environmental opportunists including the pathogen-containing genera Bacillus, Clostridium, Enterobacter, Legionella and Pseudomonas associated with disturbed ecosystems. Our approach is generalizable with potential to inform DNA-based methods for ecosystem assessment and help target environmental interventions that may promote microbiota-mediated human health gains.
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•We found bacterial indicators of ecological restoration from soil environmental DNA.•Novel merged-sample bootstrap resampling enabled deeper analysis of microbiome data.•Ecosystem restoration can boost environmental microbial diversity.•Trending taxa from restoration can help discern natural vs. disturbed ecosystems.•Disturbed land favours opportunistic bacteria with potential human health impacts.
A relatively unaccounted ecosystem service from biodiversity is the benefit to human health via symbiotic microbiota from our environment. This benefit occurs because humans evolved alongside ...microbes and have been constantly exposed to diverse microbiota. Plants and animals, including humans, are organised as a host with symbiotic microbiota, whose collective genome and life history form a single holobiont. As such, there are interdependencies between biodiversity, holobionts, and public health which lead us to argue that human health outcomes could be improved by increasing contact with biodiversity in an urban context. We propose that humans, like all holobionts, likely require a diverse microbial habitat to appropriate resources for living healthy, long lives. We discuss how industrial urbanisation likely disrupts the symbiosis between microbiota and their hosts, leading to negative health outcomes. The industrialised urban habitat is low in macro and microbial biodiversity and discourages contact with beneficial environmental microbiota. These habitat factors, alongside diet, antibiotics, and others, are associated with the epidemic of non-communicable diseases in these societies. We suggest that restoration of urban microbial biodiversity and micro-ecological processes through microbiome rewilding can benefit holobiont health and aid in treating the urban non-communicable disease epidemic. Further, we identify research gaps and some solutions to economic and strategic hurdles in applying microbiome rewilding into daily urban life.
Falsified medicines are a major threat to global health. Antimalarial drugs have been particularly targeted by criminals. As DNA analysis has revolutionized forensic criminology, we hypothesized that ...these techniques could also be used to investigate the origins of falsified medicines. Medicines may contain diverse adventitious biological contamination, and the sealed nature of blister-packages may capture and preserve genetic signals from the manufacturing processes allowing identification of production source(s). We conducted a blinded pilot study to determine if such environmental DNA (eDNA) could be detected in eleven samples of falsified and genuine artesunate antimalarial tablets, collected in SE Asia, which could be indicative of origin. Massively Parallel Sequencing (MPS) was used to characterize microbial and eukaryote diversity. Two mitochondrial DNA analysis approaches were explored to detect the presence of human DNA. Trace eDNA from these low biomass samples demonstrated sample specific signals using two target markers. Significant differences in bacterial and eukaryote DNA community structures were observed between genuine and falsified tablets and between different packaging types of falsified artesunate. Human DNA, which was indicative of likely east Asian ancestry, was found in falsified tablets. This pilot study of the 'pharmabiome' shows the potential of environmental DNA as a powerful forensic tool to assist with the identification of the environments, and hence location and timing, of the source and manufacture of falsified medicines, establish links between seizures and complement existing tools to build a more complete picture of criminal trade routes. The finding of human DNA in tablets raises important ethical issues that need to be addressed.
Butyrate‐producing bacteria colonise the gut of humans and non‐human animals, where they produce butyrate, a short‐chain fatty acid with known health benefits. Butyrate‐producing bacteria also reside ...in soils and soil bacteria can drive the assembly of airborne bacterial communities (the aerobiome). Aerobiomes in urban greenspaces are important reservoirs of butyrate‐producing bacteria as they supplement the human microbiome, but soil butyrate producer communities have rarely been examined in detail. Here, we studied soil metagenome taxonomic and functional profiles and soil physicochemical data from two urban greenspace types: sports fields (n = 11) and nature parks (n = 22). We also developed a novel method to quantify soil butyrate and characterised the in situ activity of butyrate‐producing bacteria. We show that soil butyrate was higher in sports fields than nature parks and that sports fields also had significantly higher relative abundances of the terminal butyrate production genes buk and butCoAT than nature parks. Soil butyrate positively correlated with buk gene abundance (but not butCoAT). Soil moisture (r = .50), calcium (r = −.62), iron (ρ = .54), ammonium nitrogen (ρ = .58) and organic carbon (r = .45) had the strongest soil abiotic effects on soil butyrate concentrations and iron (ρ = .56) and calcium (ρ = −.57) had the strongest soil abiotic effects on buk read abundances. Overall, our findings contribute important new insights into the role of sports fields as key exposure reservoirs of butyrate producing bacteria, with important implications for the provision of microbiome‐mediated human health benefits via butyrate.
Soil bacteria in urban greenspaces influence the assembly of airborne bacterial communities, which can supplement the human microbiome. We compared the abundances of soil butyrate‐producing bacteria and in situ soil butyrate concentrations from two urban greenspace types: sports fields (n = 11) and nature parks (n = 22). We show that soil butyrate and the abundances of terminal butyrate production genes were higher in sports fields than nature parks and that soil moisture, calcium, iron, ammonium nitrogen and organic carbon had the strongest abiotic effects on soil butyrate concentrations.
Butyrate‐producing bacteria are found in many outdoor ecosystems and host organisms, including humans, and are vital to ecosystem functionality and human health. These bacteria ferment organic ...matter, producing the short‐chain fatty acid butyrate. However, the macroecological influences on their biogeographical distribution remain poorly resolved. Here we aimed to characterise their global distribution together with key explanatory climatic, geographical and physicochemical variables. We developed new normalised butyrate production capacity (BPC) indices derived from global metagenomic (n = 13,078) and Australia‐wide soil 16S rRNA (n = 1331) data, using Geographic Information System (GIS) and modelling techniques to detail their ecological and biogeographical associations. The highest median BPC scores were found in anoxic and fermentative environments, including the human (BPC = 2.99) and non‐human animal gut (BPC = 2.91), and in some plant–soil systems (BPC = 2.33). Within plant–soil systems, roots (BPC = 2.50) and rhizospheres (BPC = 2.34) had the highest median BPC scores. Among soil samples, geographical and climatic variables had the strongest overall effects on BPC scores (variable importance score range = 0.30–0.03), with human population density also making a notable contribution (variable importance score = 0.20). Higher BPC scores were in soils from seasonally productive sandy rangelands, temperate rural residential areas and sites with moderate‐to‐high soil iron concentrations. Abundances of butyrate‐producing bacteria in outdoor soils followed complex ecological patterns influenced by geography, climate, soil chemistry and hydrological fluctuations. These new macroecological insights further our understanding of the ecological patterns of outdoor butyrate‐producing bacteria, with implications for emerging microbially focused ecological and human health policies.
Butyrate‐producing bacteria produce the short‐chain fatty acid butyrate and are vital to ecosystem functionality and human health, but the macroecological influences on their biogeographical distribution remain poorly resolved. Here we developed new normalised butyrate production capacity (BPC) indices derived from global metagenomic (n = 13,078) and Australia‐wide soil 16S rRNA (n = 1331) to characterise their global distribution together with key explanatory climatic, geographical and physicochemical variables. Abundances of butyrate‐producing bacteria in outdoor soils followed complex ecological patterns influenced by geography, climate, soil chemistry and hydrological fluctuations, and our findings lend new macroecological insights for emerging microbially focused ecological and human health policies.
Soil bacterial taxa have important functional roles in ecosystems (e.g. nutrient cycling, soil formation, plant health). Many factors influence their assembly and regulation, with land cover types ...(e.g. open woodlands, grasslands), land use types (e.g. nature reserves, urban green space) and plant–soil feedbacks being well‐studied factors. However, changes in soil bacterial communities in situ over light–dark cycles have received little attention, despite many plants and some bacteria having endogenous circadian rhythms that could influence soil bacterial communities. We sampled surface soils in situ across 24‐h light–dark cycles (at 00:00, 06:00, 12:00, 18:00) at two land cover types (remnant vegetation vs. cleared, grassy areas) and applied 16S rRNA amplicon sequencing to investigate changes in bacterial communities. We show that land cover type strongly affected soil bacterial diversity, with soils under native vegetation expressing 15.4%–16.4% lower alpha diversity but 4.9%–10.6% greater heterogeneity than soils under cleared vegetation. In addition, we report time‐dependent and site‐specific changes in bacterial network complexity and between 598–922 ASVs showing significant changes in relative abundance across times. Native site node degree (bacterial interactions) at the phylum level was 16.0% higher in the early morning than in the afternoon/evening. Our results demonstrate for the first time that light–dark cycles have subtle yet important effects on soil bacterial communities in situ and that land cover influences these dynamics. We provide a new view of soil microbial ecology and suggest that future studies should consider the time of day when sampling soil bacteria.
This study explores the impact of light–dark cycles and land cover types on soil bacterial communities. It finds that land cover type significantly affects bacterial diversity and that there are time‐dependent variations in bacterial network complexity and relative abundance of individual taxa. These findings highlight the influence of light–dark cycles and land cover on soil bacterial composition, emphasising the importance of considering the time of day in soil bacteria sampling.
Abstract
Biodiversity is widely linked to human health, however, connections between human health and soil biodiversity in urban environments remain poorly understood. Here, we stress that reductions ...in urban soil biodiversity elevate risks to human health, but soil biodiversity can improve human health through pathways including suppressing pathogens, remediating soil, shaping a beneficial human microbiome and promoting immune fitness. We argue that targeted enhancement of urban soil biodiversity could support human health, in both outdoor and indoor settings. The potential of enhanced urban soil biodiversity to benefit human health reflects an important yet understudied field of fundamental and applied research.
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