Building on the microbiome rewilding hypothesis, a term that has recently been proposed is ‘microbiome-inspired green infrastructure’ (MIGI) [63
]. MIGI is a collective term for living, multifunctional green spaces that are designed and manipulated to generate health-inducing microbial interactions (Figure 1
). This is based on the premise that biodiverse microbial habitats can be ‘restored’ as per the microbiome rewilding hypothesis.
The ‘inspired’ part of MIGI implies a significant design element. Design considerations include multifunctional roles for social activities and ecosystem services, and both dynamic and static spatial factors within urban settings. For example, understanding how pollution, area, proximity, aspect, and urban physical features such as buildings, roads, and other structures, influence the dynamics of MIGI will be essential. It is also important to extend beyond the domains of localized mechanisms and impacts, and to determine whether interconnected systems of MIGI can “improve the microbial network fragility of larger urban areas such as ‘megacities’, which have been linked to human diseases” [63
]. Furthermore, as a prospective ecological and public health intervention, MIGI should be designed to maximize ecological justice and reduce health inequalities; for example, by ensuring equity of access where public land is concerned. Gaining a detailed understanding of the dynamics between MIGI availability vs. optimal exposure to, and interaction with, health-inducing microbial community assemblages, will play a key role throughout the MIGI design, implementation and monitoring process.
‘Inspired’ also implies a detailed understanding of environmental microbiome dynamics––the functional relationships between microbiota and vegetation, the spatiotemporal and compositional dynamics, and the mechanisms and pathways that facilitate human-microbial exchange and associated benefits. These factors are still poorly understood and a concerted effort to establish research and communication methods is needed to rapidly progress our understanding of what is known as “microbial dark matter” [65
]—the microbial presence, abundance, composition and functionality in the environment. This continual generation of knowledge will allow for informed applications of MIGI, optimized to benefit humans and the environment.
7.1. Microbiome-Inspired Green Infrastructure—Foraging
From a societal evolution perspective, the human microbiome has gradually decreased in community diversity as human populations have passed along the following trajectory:
Foraging → Rural farming → Urban industrial lifestyles [66
A number of studies point to the link between high human microbial diversity and the foraging lifestyle [67
]. Therefore, it is envisaged that the application of MIGI will include foraging-friendly green spaces (Figure 2
). This will require a collaborative effort between landscape architects, ecologists, agriculturalists and urban planners to create innovative food planting schemes that replicate (partially, at least) and promote foraging behavior. The ultimate aim of this strategy is to enhance human–environment microbial interactions and increase the diversity of microbiota residing in and on the human body. Foraging also augments the multisensorial experience (i.e., touch, sight, smell), which brings its own intrinsic advantages as nature-derived health benefits arrive through a variety of senses [70
Foraging is already ubiquitous across the globe; however, it is often prohibited or discouraged in urban areas [72
]. Formal strategies to draw together the benefits of foraging are needed, and with further research, the potential benefits of health-inducing microbial exchange will likely strengthen this approach. Urban foraging manifests in a variety of forms from harvesting the fruit of street trees to participating in community gardening. It would be prudent for researchers to investigate the differences (in terms of microbial exchange and health outcomes) between these foraging methods, as this would help inform the design and management of MIGI in the future. There are also concerns that need to be addressed, such as urban pollutants and perceived ‘mess’ from fallen fruits [73
]. The former calls for innovation in planting design plus plant protection and selection, and broader strategies to reduce pollution. The latter would benefit from a shift in perception of the value of these food sources, mobilized perhaps through community-centric groups such as the Grow Sheffield’s Abundance Project [74
]—an initiative that promotes the harvesting of food plants across the city and redistributes the ‘products’ to food banks and local communities.
Urban foraging schemes may well need to adapt to the intensively dynamic socio-ecological complexities of urbanization; for example, changing ownership of land, building development, and changes to infrastructure. However, recent innovation is helping to address this issue. For example, mobile allotments, such as those created by the arts and environment project Avant Gardening [75
] can be installed on vacant lots to provide communities with a foraging hub, and easily moved if the land status changes. It is also important to note that in addition to the potential of health-inducing microbial exchange, community gardening can generate other health and wellbeing benefits (e.g., through physical exercise, psychological restoration and nature connectedness) and enhance social cohesion [76
These potentially health-inducing interactions with environmental microbiota may also be enhanced via physical engagement with the substrate that supports the food plants. Cutting-edge research by Lowry on the soil microorganism Mycobacterium vaccae
has shown that when injected in mice, this non-pathogenic bacterium can activate 5-hydroxytryptamine (serotonin) in the prefrontal cortex, helping to regulate coping responses to “uncontrollable stress” [78
]. The potential health benefits of M. vaccae
do not end here; the inoculation of this microorganism has also been shown to protect against neuroinflammation and cognitive dysfunction, and to have immune boosting effects [79
]. This is just the story for a single species of bacterium that can influence cognition, behavior and immunity. This speaks volumes for the potential of the other estimated ~1 × 105
genera of bacteria and archaea on the planet, of which only ~11,000 species have been classified [81
]. The possibilities here for MIGI are multitudinous—Are there certain natural habitats that can optimize interactions with health-inducing microbiota? Can we isolate different microbial species and manipulate communities to enhance these interactions? The research is in its infancy, but the potential is immense.
7.3. Microbiome-Inspired Green Infrastructure—Cultural and Ancestral Microbiomes
Due to increasing cultural diversity of western towns and cities [85
], it is essential to emphasize the importance of inclusivity in urban green space designs. It then follows that creating inclusive environments should also be a key consideration for MIGI. Further research into the potential inclusion of inter-ethnic ancestral environments in urban areas to optimize microbial interactions and immune regulation could be important for the development of effective MIGI. Evidence points to ancestry-associated differences in human immune responses, and populations vary in their susceptibility to diseases [86
]. Furthermore, human microbiome composition varies significantly across different ethnic groups [68
], which has only been partially explained by factors such as sociodemographic dynamics and diet [89
From an immune development perspective, it is possible that specific inter-ethnic interactions with ancestral microbial communities in natural environments are important to the health of these populations. It is also possible that functional redundancy between microbiota and widespread human genetic admixture may neutralize the effectiveness of this theory; however, it has been pointed out that there is evidence to question the “universality of microbiome-based therapeutic strategies” based on ethnic and geographical variation [66
]. Ancestry aside, there are also important cultural and generational considerations for MIGI here. For example, in many countries, children are spending less time outdoors and interacting with nature [91
]. This is attributed to a range of factors such as changes in cultural practices and green space accessibility [91
]. MIGI could also be designed with cultural changes in mind; for example, establishing MIGI in areas where children do spend time, or integrating MIGI strategies with cultural trends. An example of the former could be the establishment of MIGI in and around skate parks, and an example of the latter could be to work with developers of location-based augmented reality games such as Pokémon GO to promote spending time in areas where MIGI has already been established or could be established in the future. After all, this kind of technology is unlikely to disappear, and whilst strong arguments can be made to proactively reduce ‘screen time’ and promote contact with nature, this technology–human–nature interface has also been suggested to provide new links between humans and green space and encouraging physical activity [93
]. More research into the potential salutogenic effects of ‘nature exposure’ whilst using this technology is essential.
The prospect of including different cultural and ethnic ancestral environments to promote health-inducing microbial interactions and multicultural inclusivity is a tantalizing one. However, a significant amount of additional research is needed to further understand the relationships between culture, ancestral environments, microbiota and inter-ethnic health. It will also be essential to consider the potential impacts of including novel environmental features in native ecosystems. A network of closed MIGI systems (i.e., cultural and ancestral biomes) could be an option in the future.
7.4. Microbiome-Inspired Green Infrastructure—Plant Microbiome Selection and Engineering
As with humans, plants and their microbiomes form a holobiont, and the interplay between the plant host and its co-evolving microbial assemblages has a substantial role in maintaining the health of these functional ecological units [94
]. Microbial diversity is a key driving factor in maintaining favorable plant health [94
]. Indeed, individual plant genotypes can show distinct microbial diversity, which indicates that some plants have the ability to cultivate a beneficial microbiome and this process may be under natural selection [96
]. Therefore, strategies to enhance microbial diversity to benefit human health also have the potential to generate important co-benefits for plants, with cascading benefits to the wider ecosystem. This further highlights the importance of the interconnectedness of life. Understanding how plant community composition, independent of diversity, affects the microbiome is also an important factor, particularly in ‘designed’ urban environments. For example, specific pairwise and synergistic interactions in plant communities can be selected to influence the soil microbiome structure and pathogen suppression [97
]. Plant microbiomes can also be genetically selected to enhance fitness [98
]; i.e., plant growth promotion, plant health and abiotic stress tolerance [99
]. Genotype-dependent associations between plants and the microbiome could be used to target and establish optimal MIGI dynamics, and careful selection processes may play important roles in the design, implementation and effectiveness of MIGI in the future.