Food webs in food webs: the micro-macro interplay of multilayered networks.

Food webs are typically defined as being macro-organism-based (e.g., plants, mammals, birds) or microbial (e.g., bacteria, fungi, viruses). However, these characterizations have limits. We propose a multilayered food web conceptual model where microbial food webs are nested within food webs composed of macro-organisms. Nesting occurs through host-microbe interactions, which influence the health and behavior of host macro-organisms, such that host microbiomes likely alter population dynamics of interacting macro-organisms and vice versa. Here, we explore the theoretical underpinnings of multilayered food webs and the implications of this new conceptual model on food web ecology. Our framework opens avenues for new empirical investigations into complex ecological networks and provides a new lens through which to view a network's response to ecosystem changes.

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.

Restoring soil biodiversity.

Soil health is crucial for all terrestrial life, supporting, among other processes, food production, water purification and carbon sequestration. Soil biodiversity - the variety of life within soils - is key to these processes and thus key to soil restoration. Human activities that degrade ecosystems threaten soil biodiversity and associated ecosystem processes. Indeed, 75% of the world's soils are affected by degradation - a figure that could rise to 90% by 2050 if deforestation, overgrazing, urbanisation and other harmful practices persist. Restoring soil biodiversity is a prerequisite for planetary health, and it comes with many challenges and opportunities. Soil directly supports around 60% of all species on Earth, and land degradation poses a major problem for this biodiversity and the ecosystem services that sustain human populations. Indeed, 98% of human calories come from soil, and earthworms alone underpin 6.5% of the world's grain production. Moreover, the total carbon in terrestrial ecosystems is around 3,170 gigatons (1 gigaton (Gt) = 1 billion metric tons), of which approximately 80% (2,500 Gt) is found in soil. Therefore, restoring soil biodiversity is not just a human need but an ecological and Earth-system imperative. It is pivotal for maintaining ecosystem resilience, sustaining agricultural productivity and mitigating climate change impacts.

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.

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.

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.

Probiotic Cities: microbiome-integrated design for healthy urban ecosystems.

Combining microbiome science and biointegrated design offers opportunities to help address the intertwined challenges of urban ecosystem degradation and human disease. Biointegrated materials have the potential to combat superbugs and remediate pollution while inoculating landscape materials with microbiota can promote human immunoregulation and biodiverse green infrastructure, contributing to 'probiotic cities'.

Biodiversity and human health: A scoping review and examples of underrepresented linkages.

Mounting evidence supports the connections between exposure to environmental typologies(such as green and blue spaces)and human health. However, the mechanistic links that connect biodiversity (the variety of life) and human health, and the extent of supporting evidence remain less clear. Here, we undertook a scoping review to map the links between biodiversity and human health and summarise the levels of associated evidence using an established weight of evidence framework. Distinct from other reviews, we provide additional context regarding the environment-microbiome-health axis, evaluate the environmental buffering pathway (e.g., biodiversity impacts on air pollution), and provide examples of three under- or minimally-represented linkages. The examples are (1) biodiversity and Indigenous Peoples' health, (2) biodiversity and urban social equity, and (3) biodiversity and COVID-19. We observed a moderate level of evidence to support the environmental microbiota-human health pathway and a moderate-high level of evidence to support broader nature pathways (e.g., greenspace) to various health outcomes, from stress reduction to enhanced wellbeing and improved social cohesion. However, studies of broader nature pathways did not typically include specific biodiversity metrics, indicating clear research gaps. Further research is required to understand the connections and causative pathways between biodiversity (e.g., using metrics such as taxonomy, diversity/richness, structure, and function) and health outcomes. There are well-established frameworks to assess the effects of broad classifications of nature on human health. These can assist future research in linking biodiversity metrics to human health outcomes. Our examples of underrepresented linkages highlight the roles of biodiversity and its loss on urban lived experiences, infectious diseases, and Indigenous Peoples' sovereignty and livelihoods. More research and awareness of these socioecological interconnections are needed.

Policy implications of the microbiota-gut-brain axis.

The microbiota-gut-brain axis facilitates communication between the gut microbiota and the brain. It has implications for health and environmental policy. Microbiota are linked to neurological and metabolic disorders, and our exposure to health-promoting microbiota depends on environmental quality. Microbiota-gut-brain axis interventions could inform policy initiatives to address systemic health issues.

Opportunities and challenges for microbiomics in ecosystem restoration.

Microbiomics is the science of characterizing microbial community structure, function, and dynamics. It has great potential to advance our understanding of plant-soil-microbe processes and interaction networks which can be applied to improve ecosystem restoration. However, microbiomics may be perceived as complex and the technology is not accessible to all. The opportunities of microbiomics in restoration ecology are considerable, but so are the practical challenges. Applying microbiomics in restoration must move beyond compositional assessments to incorporate tools to study the complexity of ecosystem recovery. Advances in metaomic tools provide unprecedented possibilities to aid restoration interventions. Moreover, complementary non-omic applications, such as microbial inoculants and biopriming, have the potential to improve restoration objectives by enhancing the establishment and health of vegetation communities.

The aerobiome-health axis: a paradigm shift in bioaerosol thinking.

Historically, a primary aim of bioaerosol research has been to understand and prevent 'unhealthy' human exposures to pathogens and allergens. However, there has been a recent paradigm shift in thinking about bioaerosols. Exposure to a diverse aerobiome - the microbiome of the air - is now considered necessary to be healthy.

Urban centre green metrics in Great Britain: A geospatial and socioecological study.

Green infrastructure plays a vital role in urban ecosystems. This includes sustaining biodiversity and human health. Despite a large number of studies investigating greenspace disparities in suburban areas, no known studies have compared the green attributes (e.g., trees, greenness, and greenspaces) of urban centres. Consequently, there may be uncharacterised socioecological disparities between the cores of urban areas (e.g., city centres). This is important because people spend considerable time in urban centres due to employment, retail and leisure opportunities. Therefore, the availability of--and disparities in--green infrastructure in urban centres can affect many lives and potentially underscore a socio-ecological justice issue. To facilitate comparisons between urban centres in Great Britain, we analysed open data of urban centre boundaries with a central business district and population of ≥100,000 (n = 68). Given the various elements that contribute to 'greenness', we combine a range of different measurements (trees, greenness, and accessible greenspaces) into a single indicator. We applied the normalised difference vegetation index (NDVI) to estimate the mean greenness of urban centres and the wider urban area (using a 1 km buffer) and determined the proportion of publicly accessible greenspace within each urban centre with Ordnance Survey Open Greenspace data. Finally, we applied a land cover classification algorithm using i-Tree Canopy to estimate tree coverage. This is the first study to define and rank urban centres based on multiple green attributes. The results suggest important differences in the proportion of green attributes between urban centres. For instance, Exeter scored the highest with a mean NDVI of 0.15, a tree coverage of 11.67%, and an OS Greenspace coverage of 0.05%, and Glasgow the lowest with a mean NDVI of 0.02, a tree cover of 1.95% and an OS Greenspace coverage of 0.00%. We also demonstrated that population size negatively associated with greenness and tree coverage, but not greenspaces, and that green attributes negatively associated with deprivation. This is important because it suggests that health-promoting and biodiversity-supporting resources diminish as population and deprivation increase. Disparities in green infrastructure across the country, along with the population and deprivation-associated trends, are important in terms of socioecological and equity justice. This study provides a baseline and stimulus to help local authorities and urban planners create and monitor equitable greening interventions in urban/city centres.

Ecosystem restoration is integral to humanity's recovery from COVID-19.

COVID-19 has devastated global communities and economies. The pandemic has exposed socioeconomic disparities and weaknesses in health systems worldwide. Long-term health effects and economic recovery are major concerns. Ecosystem restoration-ie, the repair of ecosystems that have been degraded-relates directly to tackling the health and socioeconomic burdens of COVID-19, because stable and resilient ecosystems are fundamental determinants of health and socioeconomic stability. Here, we use COVID-19 as a case study, showing how ecosystem restoration can reduce the risk of infection and adverse sequelae and have an integral role in humanity's recovery from COVID-19. The next decade will be crucial for humanity's recovery from COVID-19 and for ecosystem repair. Indeed, in the absence of effective, large-scale restoration, 95% of the Earth's land could be degraded by 2050. The UN Decade on Ecosystem Restoration (2021-30) declaration reflects the growing urgency and scale at which we should repair ecosystems. Importantly, ecosystem restoration could also help to combat the health and socioeconomic issues that are associated with COVID-19, yet it is poorly integrated into current responses to the disease. Ecosystem restoration can be a core public health intervention and assist in COVID-19 recovery if it is closely integrated with socioeconomic, health, and environmental policies.

Twenty Important Research Questions in Microbial Exposure and Social Equity.

Social and political policy, human activities, and environmental change affect the ways in which microbial communities assemble and interact with people. These factors determine how different social groups are exposed to beneficial and/or harmful microorganisms, meaning microbial exposure has an important socioecological justice context. Therefore, greater consideration of microbial exposure and social equity in research, planning, and policy is imperative. Here, we identify 20 research questions considered fundamentally important to promoting equitable exposure to beneficial microorganisms, along with safeguarding resilient societies and ecosystems. The 20 research questions we identified span seven broad themes, including the following: (i) sociocultural interactions; (ii) Indigenous community health and well-being; (iii) humans, urban ecosystems, and environmental processes; (iv) human psychology and mental health; (v) microbiomes and infectious diseases; (vi) human health and food security; and (vii) microbiome-related planning, policy, and outreach. Our goal was to summarize this growing field and to stimulate impactful research avenues while providing focus for funders and policymakers.

Germaphobia! Does Our Relationship With and Knowledge of Biodiversity Affect Our Attitudes Toward Microbes?

Germaphobia - a pathological aversion to microorganisms - could be contributing to an explosion in human immune-related disorders via mass sterilization of surfaces and reduced exposure to biodiversity. Loss of biodiversity and people's weaker connection to nature, along with poor microbial literacy may be augmenting the negative consequences of germaphobia on ecosystem health. In this study, we created an online questionnaire to acquire data on attitudes toward, and knowledge of microbes. We collected data on nature connectedness and interactions with nature and explored the relationships between these variables. Although the study had an international reach (n = 1,184), the majority of responses came from England, United Kingdom (n = 993). We found a significant association between attitudes toward microbes and both duration and frequency of visits to natural environments. A higher frequency of visits to nature per week, and a longer duration spent in nature per visit, was significantly associated with positive attitudes toward microbes. We found no association between nature connectedness and attitudes toward microbes. We found a significant relationship between knowledge of "lesser known" microbial groups (e.g., identifying that fungi, algae, protozoa, and archaea are microbes) and positive attitudes toward microbes. However, we also found that people who identified viruses as being microbes expressed less positive views of microbes overall-this could potentially be attributed to a "COVID-19 effect." Our results suggest that basic microbial literacy and nature engagement may be important in reducing/preventing germaphobia-associated attitudes. The results also suggest that a virus-centric phenomenon (e.g., COVID-19) could increase broader germaphobia-associated attitudes. As the rise of immune-related disorders and mental health conditions have been linked to germaphobia, reduced biodiversity, and non-targeted sterilization, our findings point to a feasible strategy to potentially help ameliorate these negative consequences. Further research is needed, but greater emphasis on microbial literacy and promoting time spent in nature could potentially be useful in promoting resilience in human health and more positive/constructive attitudes toward the foundations of our ecosystems-the microorganisms.

Introducing the Microbes and Social Equity Working Group: Considering the Microbial Components of Social, Environmental, and Health Justice.

Humans are inextricably linked to each other and our natural world, and microorganisms lie at the nexus of those interactions. Microorganisms form genetically flexible, taxonomically diverse, and biochemically rich communities, i.e., microbiomes that are integral to the health and development of macroorganisms, societies, and ecosystems. Yet engagement with beneficial microbiomes is dictated by access to public resources, such as nutritious food, clean water and air, safe shelter, social interactions, and effective medicine. In this way, microbiomes have sociopolitical contexts that must be considered. The Microbes and Social Equity (MSE) Working Group connects microbiology with social equity research, education, policy, and practice to understand the interplay of microorganisms, individuals, societies, and ecosystems. Here, we outline opportunities for integrating microbiology and social equity work through broadening education and training; diversifying research topics, methods, and perspectives; and advocating for evidence-based public policy that supports sustainable, equitable, and microbial wealth for all.

Exposure to airborne bacteria depends upon vertical stratification and vegetation complexity.

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.

The impact of cross-kingdom molecular forensics on genetic privacy.

Recent advances in metagenomic technology and computational prediction may inadvertently weaken an individual's reasonable expectation of privacy. Through cross-kingdom genetic and metagenomic forensics, we can already predict at least a dozen human phenotypes with varying degrees of accuracy. There is also growing potential to detect a "molecular echo" of an individual's microbiome from cells deposited on public surfaces. At present, host genetic data from somatic or germ cells provide more reliable information than microbiome samples. However, the emerging ability to infer personal details from different microscopic biological materials left behind on surfaces requires in-depth ethical and legal scrutiny. There is potential to identify and track individuals, along with new, surreptitious means of genetic discrimination. This commentary underscores the need to update legal and policy frameworks for genetic privacy with additional considerations for the information that could be acquired from microbiome-derived data. The article also aims to stimulate ubiquitous discourse to ensure the protection of genetic rights and liberties in the post-genomic era. Video abstract.

Nature's Role in Supporting Health during the COVID-19 Pandemic: A Geospatial and Socioecological Study.

The COVID-19 pandemic has brought about unprecedented changes to human lifestyles across the world. The virus and associated social restriction measures have been linked to an increase in mental health conditions. A considerable body of evidence shows that spending time in and engaging with nature can improve human health and wellbeing. Our study explores nature's role in supporting health during the COVID-19 pandemic. We created web-based questionnaires with validated health instruments and conducted spatial analyses in a geographic information system (GIS). We collected data (n = 1184) on people's patterns of nature exposure, associated health and wellbeing responses, and potential socioecological drivers such as relative deprivation, access to greenspaces, and land-cover greenness. The majority of responses came from England, UK (n = 993). We applied a range of statistical analyses including bootstrap-resampled correlations and binomial regression models, adjusting for several potential confounding factors. We found that respondents significantly changed their patterns of visiting nature as a result of the COVID-19 pandemic. People spent more time in nature and visited nature more often during the pandemic. People generally visited nature for a health and wellbeing benefit and felt that nature helped them cope during the pandemic. Greater land-cover greenness within a 250 m radius around a respondent's postcode was important in predicting higher levels of mental wellbeing. There were significantly more food-growing allotments within 100 and 250 m around respondents with high mental wellbeing scores. The need for a mutually-advantageous relationship between humans and the wider biotic community has never been more important. We must conserve, restore and design nature-centric environments to maintain resilient societies and promote planetary health.

The Holobiont Blindspot: Relating Host-Microbiome Interactions to Cognitive Biases and the Concept of the "Umwelt".

Cognitive biases can lead to misinterpretations of human and non-human biology and behavior. The concept of the Umwelt describes phylogenetic contrasts in the sensory realms of different species and has important implications for evolutionary studies of cognition (including biases) and social behavior. It has recently been suggested that the microbiome (the diverse network of microorganisms in a given environment, including those within a host organism such as humans) has an influential role in host behavior and health. In this paper, we discuss the host's microbiome in relation to cognitive biases and the concept of the Umwelt. Failing to consider the role of host-microbiome (collectively termed a "holobiont") interactions in a given behavior, may underpin a potentially important cognitive bias - which we refer to as the Holobiont Blindspot. We also suggest that microbially mediated behavioral responses could augment our understanding of the Umwelt. For example, the potential role of the microbiome in perception and action could be an important component of the system that gives rise to the Umwelt. We also discuss whether microbial symbionts could be considered in System 1 thinking - that is, decisions driven by perception, intuition and associative memory. Recognizing Holobiont Blindspots and considering the microbiome as a key factor in the Umwelt and System 1 thinking has the potential to advance studies of cognition. Furthermore, investigating Holobiont Blindspots could have important implications for our understanding of social behaviors and mental health. Indeed, the way we think about how we think may need to be revisited.