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.