The 4E approach to the human microbiome: Nested interactions between the gut-brain/body system within natural and built environments.

The complexity of the human mind and its interaction with the environment is one of the main epistemological debates throughout history. Recent ideas, framed as the 4E perspective to cognition, highlight that human experience depends causally on both cerebral and extracranial processes, but also is embedded in a particular sociomaterial context and is a product of historical accumulation of trajectory changes throughout life. Accordingly, the human microbiome is one of the most intriguing actors modulating brain function and physiology. Here, we present the 4E approach to the Human Microbiome for understanding mental processes from a broader perspective, encompassing one's body physiology and environment throughout their lifespan, interconnected by microbiome community structure and dynamics. We review evidence supporting the approach theoretically and motivates the study of the global set of microbial ecosystem networks encountered by a person across their lifetime (from skin to gut to natural and built environments). We furthermore trace future empirical implementation of the approach. We finally discuss novel research opportunities and clinical interventions aimed toward developing low-cost/high-benefit integrative and personalized bio-psycho-socio-environmental treatments for mental health and including the brain-gut-microbiome axis.

Temporary establishment of bacteria from indoor plant leaves and soil on human skin.

BACKGROUND: Plants are found in a large percentage of indoor environments, yet the potential for bacteria associated with indoor plant leaves and soil to colonize human skin remains unclear. We report results of experiments in a controlled climate chamber to characterize bacterial communities inhabiting the substrates and leaves of five indoor plant species, and quantify microbial transfer dynamics and residence times on human skin following simulated touch contact events. Controlled bacterial propagule transfer events with soil and leaf donors were applied to the arms of human occupants and repeatedly measured over a 24-h period using 16S rRNA gene amplicon sequencing. RESULTS: Substrate samples had greater biomass and alpha diversity compared to leaves and baseline skin bacterial communities, as well as dissimilar taxonomic compositions. Despite these differences in donor community diversity and biomass, we observed repeatable patterns in the dynamics of transfer events. Recipient human skin bacterial communities increased in alpha diversity and became more similar to donor communities, an effect which, for soil contact only, persisted for at least 24 h. Washing with soap and water effectively returned communities to their pre-perturbed state, although some abundant soil taxa resisted removal through washing. CONCLUSIONS: This study represents an initial characterization of bacterial relationships between humans and indoor plants, which represent a potentially valuable element of biodiversity in the built environment. Although environmental microbiota are unlikely to permanently colonize skin following a single contact event, repeated or continuous exposures to indoor biodiversity may be increasingly relevant for the functioning and diversity of the human microbiome as urbanization continues.

Urban Aerobiomes are Influenced by Season, Vegetation, and Individual Site Characteristics.

Exposure to biodiverse environments such as forests can benefit human well-being, and evidence suggests exposure to high microbial diversity may improve mental and immune health. However, the factors that drive microbial community assembly are poorly understood, as is the relationship between exposure to these communities and human health. We characterized airborne bacterial communities in two disparate types of urban greenspace (forest and grass) in late-spring 2017 at sites previously sampled in late-summer 2015 in Eugene-Springfield, Oregon, using high-throughput metabarcode sequencing. While all sites shared a core aerobiome in late-spring consisting of plant- and soil-associated genera, forests had significantly higher diversity than grass sites (F = 12, P = 0.004). Vegetation type explained 14% of the difference between forest and grass aerobiomes, yet individual site location explained 41% of the variation. These results were similar to but amplified over those from late summer, suggesting that both aerobiome diversity and vegetation-driven effects are higher when deciduous foliage is fresher and more active, temperatures cooler, and humidity higher. Continued exploration and hypothesis-driven research will enable development of mechanistic theory describing key drivers of urban aerobiome assembly and its relationship to human health, which, in turn, will help urban designers and planners create evidence-based salutogenic cities for future generations.

Building upon current knowledge and techniques of indoor microbiology to construct the next era of theory into microorganisms, health, and the built environment.

In the constructed habitat in which we spend up to 90% of our time, architectural design influences occupants' behavioral patterns, interactions with objects, surfaces, rituals, the outside environment, and each other. Within this built environment, human behavior and building design contribute to the accrual and dispersal of microorganisms; it is a collection of fomites that transfer microorganisms; reservoirs that collect biomass; structures that induce human or air movement patterns; and space types that encourage proximity or isolation between humans whose personal microbial clouds disperse cells into buildings. There have been recent calls to incorporate building microbiology into occupant health and exposure research and standards, yet the built environment is largely viewed as a repository for microorganisms which are to be eliminated, instead of a habitat which is inexorably linked to the microbial influences of building inhabitants. Health sectors have re-evaluated the role of microorganisms in health, incorporating microorganisms into prevention and treatment protocols, yet no paradigm shift has occurred with respect to microbiology of the built environment, despite calls to do so. Technological and logistical constraints often preclude our ability to link health outcomes to indoor microbiology, yet sufficient study exists to inform the theory and implementation of the next era of research and intervention in the built environment. This review presents built environment characteristics in relation to human health and disease, explores some of the current experimental strategies and interventions which explore health in the built environment, and discusses an emerging model for fostering indoor microbiology rather than fearing it.