Altered Resources and Soil Chemistry
The resources that microbial communities need to survive and grow may be altered in an urban setting (Figure 2). From non-urban systems, we know that a shift in resource availability, whether to the microbes’ benefit or detriment, will often cause microbial communities to change in activity, and this change can have ecosystem consequences (Maliket al. , 2020; Tieman & Billings, 2011; Chung et al. , 2007). Among the most important soil chemical characteristics and resources for microbial growth are pH, carbon, nitrogen, phosphorus, and water. In many urban soils, levels of these resources are considerably different from native rural or unmanaged soils. Urban landscapes are also exposed to higher heavy metal deposition, pesticides, and soil sealing. Here we explore the impacts that these factors may have on the urban soil microbiome. Interactions between these variables make it challenging to predict their combined impact on microbial communities and activity. Teasing apart the individual and combined effects of these variables will be important in order to appropriately manage urban soils and promote healthy soil microbiomes.
pH – Due to the narrow optimal pH range for many taxa, soil pH is a strong driver of microbial community composition and function (Rousk et al. , 2010; Glassman et al. , 2017; Zhalninaet al. , 2015; Mukherjee et al. , 2014; Kaiser et al. , 2016; Pietri & Brookes, 2008). Generally, bacterial communities are more diverse and enzymatically active in neutral soils than more acidic soils (Fierer et al. , 2006; Liu et al. , 2014; Acosta-Martinez & Tabatabai, 2000). However, lower pH may promote some desirable microbial functions such as increased carbon storage (Maliket al. , 2018). While natural soils are generally neutral or slightly acidic, urban soils are often alkalized (Lorenz & Kandeler, 2006). This increased pH in urban soil has been associated with decreased microbial function (Caracava et al. , 2017). However, the role of pH in driving microbial community structure and function in urban soils is largely unknown and requires further study.
Carbon - Carbon content in urban soils is frequently altered. Particularly in urban turfgrass systems, frequent mowing and clipping may alter soil organic matter dynamics and microbial function (Thompson & Kao-Kniffen 2019). Mowing lawns and leaving the trimmings versus removing them can have consequences for nutrient cycling. Grass clipping can stimulate microbial activity by increasing root exudation. Returning the clippings to the soil can provide nutrients to soil microbes as the clippings decompose, reducing the need to fertilize. Removing the clippings, on the other hand, may cause microbes to rely more on existing SOM and decrease the soil’s ability to act as a nitrogen sink. Removal of plant biomass has also been shown to decrease microbial biomass and respiration and cause microbes to rely on more recalcitrant forms of carbon, increasing the abundance of recalcitrant carbon and nitrogen cycling genes in the community (Wang et al. , 2011; Xueet al. , 2016).
Carbon availability in urban areas is also affected by the ‘CO2 dome’, which is an area of increased atmospheric CO2 concentration due to the local and concentrated burning of fossil fuels. Atmospheric CO2 levels can impact soil microbes, mainly indirectly through changing plant inputs. Carney et al. (2007) found that doubling CO2levels resulted in higher activity of microbial carbon-degrading enzymes. Although CO2 fertilization can be beneficial for plant growth, Carney et al. (2007) found that soils still lost carbon overall after long-term exposure to increased CO2. Likewise, He et al. (2014) observed that CO2 enrichment in soybean agricultural soil resulted in increased abundance of functional genes for carbon and nitrogen cycling, although this study did not look at the downstream impacts of these changes on soil carbon and nitrogen dynamics. Together, these two studies have implications for microbial carbon cycling in cities, with the concern that carbon loss could be accelerated in urban soils due to increased microbial enzyme activity, and nitrogen cycling may be altered. To our knowledge, though, no studies have specifically investigated the impact of urban CO2 domes on microbial function. We recommend this topic as a priority for future studies.
Nitrogen – Nutrients such as nitrogen and phosphorus are often added directly to urban greenspaces as fertilizer or are unintentionally added from runoff and atmospheric deposition. These nitrogen inputs may be high enough to trigger symptoms of nitrogen saturation in urban soils (Chen et al. , 2010; Yang & Toor, 2016; Taylor et al. , 2005). In studies of non-urban systems, nitrogen amendments generally reduce microbial respiration, biomass, and extracellular enzyme activity while altering community composition (Ramirez et al. , 2012; Treseder, 2008). Consequently, nitrogen deposition may promote soil carbon storage, although the mechanisms for this observation are unclear (Zak et al. , 2016). What effect does added nitrogen have on urban soil microbes? Urban systems are capable of cycling nitrogen at rates comparable to non-urban systems (Reisinger et al. , 2016) and may have increased rates of nitrogen mineralization and nitrification (Reisinger et al. , 2016; Pouyat et al. , 1997; Enloeet al. , 2015). Microbial genes related to nitrogen-cycling are abundant in urban park soils (Wang et al. , 2018). These findings indicate that urban soil microbes are highly active in nitrogen cycling. Additionally, in an urban-rural gradient study, soil nitrogen was found to be a better predictor of microbial enzyme activity than carbon or pH (Cusack, 2013), adding further evidence that nitrogen is an important factor influencing microbial communities in urban soils.
Despite the high nitrogen cycling activity of their microbial communities, urban soils remain significant sources of nitrogen runoff (Yang & Toor, 2016; Taylor et al. , 2005) and nitrous oxide (van Delden et al. , 2016; Townsend-Small and Czimczik, 2010; Kayeet al. , 2004). Microbes may reach a stoichiometric limit to the amount of nitrogen they can take up. Bird and Bonnett (2018) found that additional nitrogen stimulated microbial extracellular enzyme activity related to carbon acquisition, indicating that carbon may be a more limiting nutrient once nitrogen is readily available. Therefore, to improve microbial denitrification and nitrogen uptake, it may be necessary to supplement fertilized soils with additional carbon sources.
Water – Variation in water availability may impact the activity and function of urban soil microbes. Many urban soils are irrigated, and some receive substantial irrigation in order to support lush greenery in an otherwise arid setting. Meanwhile, urban soils in more mesic regions tend to be drier due to increased runoff from features like impervious surfaces and drainage systems (Picket & Cadenasso 2009). Green and Oleksyszyn (2002) compared irrigated lawns, xeriscaped (reduced irrigation) lawns, and unmanaged desert patches and found that irrigated lawns showed the highest invertase and cellulase activities, indicating that irrigation promotes microbial breakdown of carbon sources. This result is consistent with Orchard and Cook’s (1983) findings that wetter soils contribute to higher microbial respiration and soil carbon loss. Irrigation also makes nitrogen more accessible to microbes, while drier soils decrease diffusion of substrates through the soil, limiting microbial activity (Stark & Firestone, 1995). The combination of irrigation and fertilization results in greater N2O and NO fluxes from urban soils (Hall et al. , 2008; Kaye et al. , 2004). Balancing the combined use of fertilizer and irrigation may therefore be important for managing urban green spaces while minimizing greenhouse gas efflux (Bijoor et al. , 2008).
Heavy Metals – Heavy metal pollution is an unfortunate consequence of human activities such as smelting and fossil fuel combustion (Martín et al. , 2015; Luo et al. , 2015; Beninet al. , 1999). Roadsides and industrial areas are hotspots for heavy metal pollution in soils. As soil toxicity from heavy metals increases, microbial biomass and activity generally decrease (Azarbadet al. , 2013; Oliveira & Pampulha 2006; Papa et al. , 2010). Some microbial taxa are impacted more than others by heavy metals (Oliveira & Pampulha 2006). It will be important to determine whether the impacted taxa have consequences for ecosystem function and, if so, how we might reduce soil pollutants to restore vital microbial processes.
Pesticides - To maintain idyllic urban greenspaces and reduce damage from insects and weeds, pesticides (primarily herbicides and insecticides) are often applied to urban soils. There have been recent efforts to understand the impacts of these chemicals on soil health, including the functioning of soil microorganisms. Several reviews have found mixed effects of pesticides on microbial communities and their functions (Riah et al. , 2014; Imfeld & Vuilleumier, 2012; Kalia & Gosal, 2010). Depending on the pesticide, impacts on microbial biomass and enzyme activity may be negative, neutral, or positive. Effects may be short-lived or more long-term, and microbial interactions with pesticides may depend on other factors such as temperature, soil fertilization, and soil carbon content (Reedich, Millican & Koch, 2017; Munoz-Leoz et al. , 2012; Garcia-Delgado et al. , 2018). Additionally, because the majority of pesticide studies focused on agricultural systems or lab microcosms, little is known about how in situ urban microbial communities respond to pesticide application and what this may mean for soil health and function.
Impervious Surfaces - A considerable amount of urban land is covered by impervious surfaces such as buildings, roads, sidewalks, and other paved areas. Therefore, studies on open urban soils may not be sufficient to gain a comprehensive understanding of urban ecosystem functioning. Impervious surfaces serve as a barrier that alters or prevents the exchange of substances between the soil, surrounding environment, and atmosphere. Soils beneath impervious surfaces have been found to contain less carbon and nitrogen than open soils and have reduced microbial activity (Raciti et al. , 2012; Wei et al. , 2014; Lu et al. , 2020). Sealed soils may also have decreased microbial diversity and altered community structure (Huet al. , 2018; Yu et al. , 2019). Sealed soils were largely ignored until recently, but now researchers are emphasizing the need to include them in overall urban carbon budgets and models of urban geochemical dynamics (e.g. Bae & Ryu, 2020; Hu et al. , 2018; Weiet al. , 2014).
Novel Plant Communities – As in non-urban systems, soil microbial communities in urban greenspaces appear to be shaped, at least in part, by plant inputs and diversity (Hui et al. , 2017). Urban ecosystems are often home to novel plant communities, including many non-native plant species (Kowarik, 2011). Since plants can be major drivers of microbial community assembly, novel plant communities may foster microbial communities different from those typical in soils with native vegetation. Urbanization also facilitates the spread of invasive plant species (Skultety & Matthews, 2017; Santana Marques et al. , 2020; Lechuga-Lago et al. , 2017), and invasive plants have been shown to alter the soil microbiome, in turn impacting native plant survival and causing shifts in ecosystem processes (e.g. Batten et al. , 2006). Even non-invasive exotic plants can alter the soil microbiome, shifting microbial community structure and function (Kourtevet al. , 2002). More research should be done on the impact of common non-native and invasive urban plants compared to native plants on soil microbial communities and soil function. The impact of overall plant diversity on microbial communities should also be studied within urban systems.