Urban sports fields support higher levels of soil butyrate and butyrate-producing bacteria than urban nature parks.

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.

Bioenergetic mapping of 'healthy microbiomes' via compound processing potential imprinted in gut and soil metagenomes.

Despite mounting evidence of their importance in human health and ecosystem functioning, the definition and measurement of 'healthy microbiomes' remain unclear. More advanced knowledge exists on health associations for compounds used or produced by microbes. Environmental microbiome exposures (especially via soils) also help shape, and may supplement, the functional capacity of human microbiomes. Given the synchronous interaction between microbes, their feedstocks, and micro-environments, with functional genes facilitating chemical transformations, our objective was to examine microbiomes in terms of their capacity to process compounds relevant to human health. Here we integrate functional genomics and biochemistry frameworks to derive new quantitative measures of in silico potential for human gut and environmental soil metagenomes to process a panel of major compound classes (e.g., lipids, carbohydrates) and selected biomolecules (e.g., vitamins, short-chain fatty acids) linked to human health. Metagenome functional potential profile data were translated into a universal compound mapping 'landscape' based on bioenergetic van Krevelen mapping of function-level meta-compounds and corresponding functional relative abundances, reflecting imprinted genetic capacity of microbiomes to metabolize an array of different compounds. We show that measures of 'compound processing potential' associated with human health and disease (examining atherosclerotic cardiovascular disease, colorectal cancer, type 2 diabetes and anxious-depressive behavior case studies), and displayed seemingly predictable shifts along gradients of ecological disturbance in plant-soil ecosystems (three case studies). Ecosystem quality explained 60-92 % of variation in soil metagenome compound processing potential measures in a post-mining restoration case study dataset. With growing knowledge of the varying proficiency of environmental microbiota to process human health associated compounds, we might design environmental interventions or nature prescriptions to modulate our exposures, thereby advancing microbiota-oriented approaches to human health. Compound processing potential offers a simplified, integrative approach for applying metagenomics in ongoing efforts to understand and quantify the role of microbiota in environmental- and human-health.

The macroecology of butyrate-producing bacteria via metagenomic assessment of butyrate production capacity.

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.

Childcare centre soil microbiomes are influenced by substrate type and surrounding vegetation condition.

Urban development has profoundly reduced human exposure to biodiverse environments, which is linked to a rise in human disease. The 'biodiversity hypothesis' proposes that contact with diverse microbial communities (microbiota) benefits human health, as exposure to microbial diversity promotes immune training and regulates immune function. Soils and sandpits in urban childcare centres may provide exposure to diverse microbiota that support immunoregulation at a critical developmental stage in a child's life. However, the influence of outdoor substrate (i.e., sand vs. soil) and surrounding vegetation on these environmental microbiota in urban childcare centres remains poorly understood. Here, we used 16S rRNA amplicon sequencing to examine the variation in bacterial communities in sandpits and soils across 22 childcare centres in Adelaide, Australia, plus the impact of plant species richness and habitat condition on these bacterial communities. We show that sandpits had distinct bacterial communities and lower alpha diversity than soils. In addition, we found that plant species richness in the centres' yards and habitat condition surrounding the centres influenced the bacterial communities in soils but not sandpits. These results demonstrate that the diversity and composition of childcare centre sandpit and soil bacterial communities are shaped by substrate type, and that the soils are also shaped by the vegetation within and surrounding the centres. Accordingly, there is potential to modulate the exposure of children to health-associated bacterial communities by managing substrates and vegetation in and around childcare centres.

Short-term passive greenspace exposures have little effect on nasal microbiomes: A cross-over exposure study of a Maori cohort.

Indigenous health interventions have emerged in New Zealand aimed at increasing people's interactions with and exposure to macro and microbial diversity. Urban greenspaces provide opportunities for people to gain such exposures. However, the dynamics and pathways of microbial transfer from natural environments onto a person remain poorly understood. Here, we analysed bacterial 16S rRNA amplicons in air samples (n = 7) and pre- and post-exposure nasal samples (n = 238) from 35 participants who had 30-min exposures in an outdoor park. The participants were organised into two groups: over eight days each group had two outdoor park exposures and two indoor office exposures, with a cross-over study design and washout days between exposure days. We investigated the effects of participant group, location (outdoor park vs. indoor office), and exposures (pre vs. post) on the nasal bacterial community composition and three key suspected health-associated bacterial indicators (alpha diversity, generic diversity of Gammaproteobacteria, and read abundances of butyrate-producing bacteria). The participants had distinct nasal bacterial communities, but these communities did not display notable shifts in composition following exposures. The community composition and key health bacterial indicators were stable throughout the trial period, with no clear or consistent effects of group, location, or exposure. We conclude that 30-min exposure periods to urban greenspaces are unlikely to create notable changes in the nasal microbiome of visitors, which contrasts with previous research. Our results suggest that longer exposures or activities that involves closer interaction with microbial rich ecological components (e.g., soil) are required for greenspace exposures to result in noteworthy changes in the nasal microbiome.

Light-dark cycles may influence in situ soil bacterial networks and diurnally-sensitive taxa.

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.

The potential of outdoor environments to supply beneficial butyrate-producing bacteria to humans.

Butyrate is an important mediator of human health and disease. The mechanisms of action of butyrate are becoming increasingly well-known. Many commensal bacteria that inhabit the human gut can synthesise butyrate, which is then absorbed into the human host. Simultaneously, several immune- and inflammatory-mediated diseases are being linked to insufficient exposure to beneficial microbes from our environment, including butyrate-producing bacteria. However, the role of outdoor environmental exposure to butyrate-producing bacteria remains poorly understood. Here we review the literature on the human exposure pathways to butyrate-producing bacteria, with a particular focus on outdoor environmental sources (e.g. associated with plants, plant-based residues, and soil), and the health implications of exposure to them. Emerging evidence suggests that environmental butyrate-producers may help supplement the human gut microbiota and represent an important component of the Biodiversity and Old Friends hypotheses. Improving our understanding of potential sources, precursors, and exposure pathways of environmental butyrate-producers that influence the gut microbiota and butyrate production offers promise to advance multiple disciplines of health and environmental science. We outline research priorities to address knowledge gaps in the outdoor environment-butyrate-health nexus and build knowledge of the potential pathways to help optimise exposure to human-beneficial butyrate-producing bacteria from the outdoor environment during childhood and adulthood.