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.