Priorities for Future Research and Recommended Approaches
There is a crucial need for sustainable and equitable design of urban spaces to benefit humans and the environment from local to global scales. To best harness the power of microbial communities to achieve this goal, we have identified the following essential questions in urban microbial ecology and biogeochemistry. Furthermore, addressing these questions will help advance these disciplines more broadly, including in non-urban ecosystems. We summarize the current research providing insight into these questions thus far, and recommend approaches for future research.
Are urban soil microbial communities taxonomically and/or functionally distinct from non-urban soil microbial communities, and how much variation exists within the urban environment?
Microbial phyla most commonly found in soils include: a-Proteobacteria, B-Protobacteria, Acidobacteria, Actinobacteria, Firmicutes, Planctomycetes, Bacteroidetes (Zhang, 2008; Fierer et al. 2007). At the phylum level, taxa dominating urban soils are consistent with those observed in non-urban soils (Lysak et al. 2018; Reeseet al. 2016; Wang et al. , 2018; Huot et al. , 2017). However, relative abundances of these phyla differ within urban soils and along urban-rural gradients (Hui et al. 2017; Tan et al. , 2019; Stoma et al. , 2020). Overall diversity sometimes increases with urbanization (Tan et al., 2019; Naylo, 2019), sometimes decreases (Rai et al. , 2018), and often remains the same but with shifts in composition (Reese et al. , 2016; Joyneret al. , 2019; Yao et al. , 2006; Huot et al., 2017). Understanding how overall microbial diversity and community composition changes within urban soils is an important first step, but it is also important to understand what drives community assembly and the consequences of varying community composition for ecosystem function. Hence the next two questions.
If differences in microbial taxa and function exist, what are the associated drivers? (Arrows B and C, Fig. 1)
Although we are only just starting to determine which microbes reside in urban soils, it is becoming clear that there are differences between urban and rural communities, and soil communities within the urban matrix can also vary. What environmental variables are driving these differences? How do different taxa respond to these drivers? Answers to these questions are essential if we wish to manage soils to promote healthy and beneficial microbial communities. Urban microbes may be affected by the same environmental variables as non-urban microbes, but there may be differences in the magnitude of interactions between the drivers and the microbial taxa present.
Questions 1 and 2 can, and ideally should, be answered in conjunction. With careful sampling design, it is possible to characterize urban soil microbial communities while simultaneously identifying major drivers of community composition. One common approach has been to establish urban-rural gradients using factors like human population density, neighborhood income, and pollution levels (e.g. Azarbad et al. , 2013; Chen et al. , 2010; Xu et al. , 2013). This method allows identification of large-scale effects of urbanization on soil function. However, gradients may be less effective at fine-to-medium scales due to the high levels of heterogeneity and patchiness across the urban landscape.
A second major approach has been to focus on particular land use types within the urban matrix, e.g. soils along roads, under impervious surfaces, or beneath turfgrass lawns and parks (e.g. Hu et al. , 2018; Zhao et al. , 2012; Law & Patton, 2017; Yao et al. , 2006; Lorenz & Kandeler, 2006; Papa et al. , 2010). Since factors such as dominant plant cover, pH, moisture content, and nutrient content can be among the largest drivers of microbial community composition and may differ drastically across these sites, this approach may be helpful to link microbial taxa and functioning with multiple environmental factors. Focusing on particular land-use types may also enable researchers to generate more site-specific management recommendations to improve urban soil function.
How much does taxonomic composition vs. functional plasticity play a role in urban soil microbial community function? (Arrow C, Fig. 1)
A major topic of interest in microbial ecology is the link between taxonomic composition and function. If composition is sufficient to predict microbial community function, then sequencing communities and measuring microbial biomass would facilitate prediction of microbial community impacts on ecosystem dynamics. To an extent, metagenomic analysis has been useful for understanding and predicting a microbial community’s functional roles (e.g. Fierer et al. , 2012; Grahamet al. , 2016). While some functions are phylogenetically conserved, studies have also found that soil microbial communities exhibit functional plasticity and can shift ecological and resource acquisition strategies depending on pressures from the environment (Martiny et al. , 2015; Evans & Wallenstein, 2013; Morrisseyet al. , 2017). Microbial taxa may also be redundant, where the loss of one taxon can be compensated by the function of another (Allison & Martiny, 2008). This research is still developing, and we do not yet understand the direct consequences of most microbial taxa in any ecosystem.
In urban soils, no research explicitly linking specific microbial taxa to functioning has been conducted to our knowledge. To manage urban soils and boost ecosystem services, it will be important to understand the functional limitations of the microbial communities currently inhabiting urban soils. This knowledge will have implications for how soil communities can be manipulated by managing environmental factors, or whether inoculation of the soil with novel microbes will be needed to achieve desirable results. Furthermore, urban soils can serve as model systems for studying fundamental questions about structure-function relationships in microbiomes.
There are other ways in which studies of urban microbiomes could enhance the understanding and societal relevance of ecological science as a whole (Foreman, 2016). Urban areas experience many environmental extremes within a small geographic area. This variation provides an opportunity to study how variables like pH, heavy metals, and precipitation impact organisms while controlling for other state factors like geography, elevation, and seasonality (Jenny, 2012). With many major research labs located in urban areas, there is scientific expertise and infrastructure available to set up local observational networks and sample more frequently to capture long-term urban ecosystem dynamics (Sparrow et al. , 2020; Wang et al. , 2021). Urban ecosystem health, including soil microbiome health, could also be monitored through partnerships with community organizations and volunteers (Bliss et al. , 2001). As part of this urban ecosystem monitoring effort, it would be feasible to combine field, common garden, and laboratory studies to more explicitly link microbial taxa to function and better understand how microbial communities respond to changes over time.
What consequences do soil microbial communities have for urban ecosystem function and human well-being? (Fig 1, Arrows C and D)
Urban microbial communities may have significant effects on urban ecosystem processes, including greenhouse gas fluxes, soil nutrient dynamics, and plant growth. However, it remains unclear to what extent microbial communities drive these processes as opposed to plants and other organisms. Studies that parse out the functions of soil microbes will help clarify where to invest management efforts to improve soil services.
Soil microbial communities drive ecosystem processes that in turn affect human populations. On regional and global scales, soil microbes have the potential to help mitigate or exacerbate the climate crisis by regulating soil carbon uptake and release (Cavicchioli et al. , 2019). On the scale of a city or a neighborhood, however, little is known about how soil microbes affect human communities. Some human health studies have recently found that exposure early in life to a diverse environmental microbiome can reduce asthma and allergy rates, and there has been a push to “rewild” cities with diverse plant- and soil-associated microbes (Sandifer et al. , 2015; Rook, 2013; Selway et al. , 2020; Mills et al. , 2020; Mills et al. , 2017). In cities, green spaces are generally the source of diverse environmental microbiomes. Green spaces are not evenly distributed throughout cities and tend to be more common in wealthier neighborhoods. On the other hand, urban soils can also house pathogenic microbes and may serve as reservoirs for antibiotic resistomes (Xiang et al. , 2018; Li et al. , 2018). Therefore, urban soil microbiomes have the potential to help or harm humans, and these benefits and burdens may not be evenly distributed across cities.
Microbiome services raise a question of environmental justice: are wealthier, often white, communities benefitting more from access to green space microbiomes than low-income and minoritized communities? And are there other microbial community functions that benefit or harm some human communities over others? A recent analysis by Schell et al.(2020) found that a history of systemic racism in cities remains a strong determinant of how urban ecosystems are structured. The urban environment may have a patchy distribution of goods and harms that continue to correlate with race and income. Understanding how microbial functioning is different across the urban landscape and how that affects human communities should be a priority in urban microbial ecology. This research would benefit from collaborations with human geographers, social and environmental justice experts, city officials, and community members to identify impacts of urban soil microbiomes on human communities and develop ways to improve the urban environment through understanding of microbial functioning.
How might urban areas be better designed/managed to boost ecosystem services by soil microbial communities while minimizing harms? (Arrow A, Fig. 1)
Efforts are being made to improve ecosystem benefits in cities. Much of this work focuses on conserving or restoring native habitat (e.g. Marzluff & Ewing, 2008; De Sousa, 2003). While restoring urban land to a pre-development state may provide ecological benefits, there has been a recent push to investigate the ecological roles that novel urban ecosystems play and to consider whether they might also be providing important ecosystem services, acting as reservoirs for biodiversity, and conveying other environmental benefits (Klaus & Kiehl, 2021; Kowarik, 2011; Planchuelo et al. , 2019). Pavao-Zuckerman (2008) points out that urban soils can be deliberately manipulated as part of ecosystem management and restoration. While habitat restoration may be the preferred and conventional way to manage ecosystem processes in some locations, it is worth considering whether fostering a novel but more functionally beneficial ecosystem is a better use of management effort and resources.
Cities have already been taking advantage of novel ecosystems to improve sustainability and promote ecosystem services. For instance, green roofs have been designed to help cool buildings and reduce air conditioning needs (Takebayashi & Moriyama, 2007). Bioswales filter debris and pollution out of storm water and recharge groundwater sources (Li & Davis, 2009). Phytoremediation takes advantage of plant uptake of heavy metals in order to clean up polluted soils (e.g. Cheng, 2003; Aliet al. , 2013). Only recently has attention been paid to the role of microbes in these processes (e.g. Cui et al. , 2017; Hrynkiewicz & Baum, 2014), and a better understanding of microbial function could allow us to improve on green infrastructure technologies. It is possible that urban greenspace cover may be underestimated (Zhouet al. , 2018), so there might be opportunities to boost greenspace ecosystem services in cities.
While most green infrastructure has focused heavily on plants, microbes themselves may have the potential to reduce the negative impacts of urbanization, either independently or in conjunction with plants. For example, microbial communities in green roof soils help plants tolerate and recover from environmental stress (Hoch et al. , 2019; Fulthorpe et al. , 2018). Additionally, permeable reactive barriers have been designed to intercept and remove nitrates from groundwater by promoting microbial denitrification within the barriers (Vallino & Foreman, 2008). Soil microbes also influence the breakdown of pesticides, although the efficacy of this microbial degradation depends on community composition and environmental conditions (Reedich, Millican & Koch, 2017). Several studies have tracked and modeled microbial pesticide degradation to address and prevent pesticides and their harmful breakdown products from leaching into groundwater and aquatic systems (e.g. Yale et al. , 2017; Verma et al. , 2014; Soulas & Lagacherie, 2001). A more thorough understanding of microbial communities and their functions may allow us to “micromanage” microbial services (Peralta et al. , 2014) and develop new technologies, infrastructure, and land management practices to improve urban soil health and ecosystem processes.