How Urban Microbiomes Contribute to the Ecology of City Life
Every city has a microbiome. In fact, urban landscapes are home to resident and transient microbial communities that populate everything from the soil and air to wastewater and building interiors and exteriors. The composition of these communities varies from one city to the next. Importantly, city-dwelling microbes play numerous, largely unexplored, roles in the structure and function of urban spaces and the health of those who inhabit them. A better understanding of urban microbiomes could facilitate the design of cities with microbes and their importance for city and citizen well-being in mind.
Like the human microbiome consists of microbial consortia inhabiting regions throughout the body (i.e., the gut, skin, lungs, etc.), urban microbiomes are a collection of microbial communities that occupy diverse reservoirs throughout city landscapes, from the depths of sewers to the tops of buildings. As such, there are several reservoirs with known and emerging roles in the health and function of cities and their residents.
Soil is one of the most microbially dense and diverse substances on the planet, and microbial ecologists have been uncovering the wonders of the soil microbiome for decades. Urban soils (particularly those in green spaces, like parks) contain considerable biodiversity—in fact, New York City's Central Park maintains a degree of microbial diversity on par with that of natural landscapes across the world, including tropical and desert soils. As in natural settings, soil microbes perform important biochemical functions for the urban ecosystem, including facilitating nutrient cycling and carbon storage.
Beyond these functions, urban soil microbes may affect the health of city inhabitants. It is well established that interactions with environmental microbes, including those in soil, are necessary for proper immune system development and function. Urban soils can also harbor pathogens from contamination by sewage and other waste, as well as novel microbe-derived natural products with therapeutic potential. Microbial genes predicted to encode a number of therapeutically relevant natural products, including the anti-cancer agent epothilone and the antibiotic erythromycin, were identified within park soils throughout New York City.
The air contains transient microbial populations whose compositions vary depending on land use (e.g., how much of the landscape is covered by vegetation versus concrete). Microbes that occupy plant surfaces can be swept into the atmosphere and help shape "aerobiome" composition. As such, bacterial communities hovering above urban parks are compositionally distinct from, and more diverse than, those over parking lots. Moreover, the type of vegetation within urban areas influences the diversity of urban aerobiomes, with greater microbial diversity observed in tree-rich regions compared to grassy areas.
From a health standpoint, studies have linked city aerobiomes with worse health outcomes relative to rural areas, including an increased prevalence of conditions like asthma and allergies. This may be due to the increased microbial abundance and diversity in rural air relative to urban areas, though only a few studies have experimentally assessed the link between rural/urban aerobiomes and human health. These studies suggest that, relative to urban spaces, rural aerobiomes direct the immune response toward a T-regulatory and Th1-type response rather than an allergy/asthma-associated Th2 response. Nevertheless, there is a greater need for mechanistic explorations into factors shaping airborne microbial communities and their effects on city-dwellers.
Beneath bustling cities lie networks of sewage pipes; through these pipes flows human waste, chemicals and street runoff. Sewage systems contain microbial consortia that maintain taxa of source communities (e.g., microbes derived from human feces), yet also differ from such sources, suggesting adaptation of microbes to the nutritionally and chemically distinct environment of the sewage system. Moreover, bacterial biofilms along pipe interiors are compositionally unique from transient populations within flowing waste, emphasizing habitat diversity within the sewage system itself. Notably, sewage can be used to monitor the prevalence and spread of disease-causing microbes, including SARS-CoV-2, as well as antibiotic-resistant organisms. Microbes are also beneficial when it comes to waste purification; wastewater treatment plants enrich for microorganisms that digest sludge (i.e., sewage filtered to remove grit) for subsequent water purification steps.
Cities are not called "concrete jungles" for nothing—man-made surfaces are the foundations of urban living. Building interiors host assemblages of microbes largely derived from humans, like those on the skin, as well as those introduced via air, soil and water. Interactions with these microbes can potentially lead to acquisition of pathogenic and beneficial microbes alike.
Building exteriors, which interface with the air and other reservoirs, harbor microbial communities that influence the structural integrity of the city. For instance, sulfide oxidizing bacteria deposited on building surfaces can produce acids that degrade metals, whereas certain fungi can wheedle into stone and produce metabolites that cause physical and biochemical damage. On the other hand, microbes can also be protective against such degradation and destruction. For example, some non-corrosive microbes produce antimicrobials that inhibit growth of corrosion-causing species. Better insight into structural and functional attributes of communities inhabiting the 'built' environment may promote the application of microbiological methods for preserving city architecture, including valuable fixtures like monuments.
Although each of the above reservoirs is characterized by its own microbial profile, the urban microbiome as a whole is a collection of those associated with its soil, atmosphere, water and surfaces. Microbial communities within reservoirs intersect with one another to shape the city-wide microbial ecosystem. Moreover, there are reservoirs beyond those discussed here, such as animals and humans, that contribute to the microbial assemblages of urban landscapes.
The Composition of Urban Microbiomes Is City-Specific
There is considerable variation in the composition of urban microbiomes throughout the world. Factors like the abundance of green space and soil exposure, city architecture and wastewater composition vary between cities. Other factors like geography and climate also influence the type of microbes that survive within urban landscapes. As a result, no 2 cities have the same microbiome. When scientists conducted microbiome analyses on samples collected from various surfaces in office buildings throughout Toronto, Canada; Flagstaff, Ariz.; and San Diego, Calif., they found that each exhibited a city-specific bacterial community structure.
More recently, (and on a broader scale), metagenomic sequencing of samples swabbed from public transit stations in 60 cities across the world, from Denver to Tokyo, revealed that each city had a unique microbial fingerprint. Importantly, such fingerprints were not direct reflections of human or soil microbiomes, illustrating that the urban microbiome as a whole is more than the sum of its parts. Moreover, the researchers identified 750 bacteria and more than 10,900 viruses whose sequences did not match any reference database, underscoring that much of the microbial life inhabiting urban spaces, and their functional implications in terms of city structure and resident health, remains to be explored. This microbial variation provides an excellent opportunity to understand how city location, design and operations influence its microbiome, which could lend insight into how cities can shape their microbiomes for maximum functional benefit.
Moving Toward a Functional Understanding of Urban Microbiomes
Technological advancements have made the complexity, dynamism and potential significance of urban microbiomes increasingly apparent, and there are numerous questions that remain to be answered. For example, does the relative importance of specific microbial reservoirs (e.g., soil, air, etc.) within the urban landscape vary depending on city and time? How do microbial populations within these reservoirs interact with and influence one another? A greater understanding of these interactions would provide a more nuanced view of the complex microbial networks that define urban microbiomes as a whole.
Additionally, much of what is known about urban microbiomes comes from analyses of microbial (primarily bacterial) nucleic acids scattered throughout urban spaces. While this approach provides insight into the composition and potential functions of microbial communities, it does little to reveal the actual biological and ecological functions of urban microbes and what they mean for human health. Detecting the DNA fragments of pathogens, for example, does not necessarily mean they are widely prevalent, or even alive. Indeed, a metagenomic analysis of the New York City subway detected Yersinia pestis and Bacillus anthracis (bacteria that cause plague and anthrax, respectively), though the lack of reported plague or anthrax cases in the city suggests that these pathogens do not pose a clear health risk to humans. Ultimately, gaining phenotypic insights into urban microbial communities, coupled with comprehensive investigations into if and how they interact with humans and infrastructure, would shed light on the role and potential use of such microbes in modulating the health of our cities.