Microbes don't generally endear themselves to most of us from the handrail of the subway, but some researchers have come to know them all the same. The MetaSUB consortium, co-founded by Christopher Mason and Evan Afshin at Weill Cornell in 2015, is one example of a growing body of microbiologists interested in the smallest inhabitants of our urban spaces. MetaSUB currently coordinates across more than 100 cities to descend upon metros, buses and other busy places to sample high-traffic surfaces for metagenomic testing. This global subterranean invasion occurs on all 7 continents on precisely the same day each year (June 21st to be exact), a collaboration of Herculean proportions.
So what have such studies taught us about the urban microbiome, particularly in some of the most densely populated cities of the world? What can a rail that has seen so many storied hands in the course of an hour, let alone days or weeks, tell us about the microbial world existing on public surfaces? Should we fear those metro microbes as much as we feel that we should?
Microbiomes of Public Transit
The very first study from what has grown into the MetaSUB team demonstrated that nearly half of the DNA from subway surfaces didn't match any known organism. The data paint a picture of a diverse ecology that we know relatively little about, spanning the tree of life to include prokaryotes, fungi, eukaryotes, protists and viruses (mostly bacteriophages) adapted to live in our human-made spaces. Moreover, these microbial communities seem to carry an ecological fingerprint of the events their habitat has been through. This was demonstrated by marine-associated microbes still identifiable on a subway platform that had flooded during Hurricane Sandy.
The good news is that most of the known bacterial subway passengers from the same study were deemed to be generally safe, although potential opportunistic pathogens were also present. A smaller portion of definitive pathogens were also identified, though the authors have taken a step back from their original findings, which suggested some heavy hitters such as Yersinia pestis, or bubonic plague. Following outcry from scientists and public health officials, the authors have issued a correction stating that the evidence is not very strong that this particular organism is present, though the rest of the paper is considered robust.
Subsequent studies, within and from outside the consortium, have explored subways from Boston to Mexico City, Oslo to Hong Kong. While each city is unique, they share common patterns of microbial life. The available data describe a subway microbiome that varies by surface type, and across seasons and even by time of day. Air and surface microbiomes are each their own unique fingerprint of our shared public space. Transit surfaces are recolonized within minutes of cleaning, and passenger hand microbiomes increase in diversity and species richness following a ride. The floor is the most diverse microbial space, compared to handrails which are surprisingly one of the least diverse. One study across 60 major urban areas even describes a "core microbiome" for cities.
It is as though microbes really do reflect back to us a living, respiring image of ourselves en masse. They mirror the choreography of our minute everyday choices as imprints into their own existence, putting into living art the effects of our actions. The microbiome of cities is the microbiome of our collective selves.
Urban Microbiomes and Human Health
As more and more people reside in cities, the impact of city life on human health becomes increasingly important to understand. Microbes-which are generally shared more readily in densely populated spaces-are a large part of that. As suggested by the 'core microbiome' concept for cities, the microbiome of a city and its relative impact may be specific city to city and sector to sector, particularly across international borders with varying sanitation practices or public health resources. Some core species such as Cutibacterium acnes (a skin commensal) are ubiquitous across most large cities, whereas others are unique to the opportunities afforded by climate, population, sanitation, weather patterns, pollution and civil policy.
One question on the minds of many researchers relates to antibiotic resistance genes and their prevalence on such highly-trafficked surfaces. Organisms that possess such genes pose the growing danger of increasingly untreatable infections. While cities present a high number of antimicrobial resistance genes, and antimicrobial resistant organisms have certainly been found in public transit, the evidence does not necessarily point to cities being more dangerous than other areas for transmission or development of resistance genes.
By contrast, a study assessing antibiotic-resistant E. coli in rural and urban patients found that it was the rural patients who were more likely to have 2 different classes of antimicrobial resistance genes. Similarly, a study from the U.K. suggested that agricultural land was significantly more enriched with antibiotic-resistant bacteria than urban soils. The study posited that the use of animal manure in soils was a likely contributor, as the use of antibiotics in livestock animals is affiliated with increased antibiotic resistance genes. However, such patterns of antimicrobial resistance genes in rural spaces are likely to vary by region and land use.
There is also the question of how urban environments impact our own internal microbiomes, which is a topic of growing interest. We know that industrialization at the broad societal level is affiliated with losses to bacterial diversity in the human gut, and changes to the composition of the microbiome, relative to more traditional societal structures. These changes are likely to have many overlapping lifestyle causes beyond the strict microbiome of the built environment, from the nutrition transition toward processed foods, changes to the type and quantity of physical activity from traditional societies, to greater access to medications which may impact the microbiome. From the perspective of the human microbiome and chronic disease, urbanization and industrialization have potentially led to an increased state of vulnerability due to an onslaught of lifestyle modifications that may have collaterally damaged our gut communities. However, these observations relate to societies at large; less is known about the specific city-associated impact on the human microbiome compared to other individuals within the same society, though the topic is beginning to be explored.
Microbes are everywhere: riding with us on the subway, on our lunch break at work, in our homes and in our neighborhoods. They are a fingerprint of how we have stewarded our spaces and ourselves. They also carry imprints of the other life around us, the other creatures we share our space with and their realities, the natural environment surrounding us and the climate. Sometimes they make us sick, or harbor genes that pose a danger to us. Most of the time they are harmless, and sometimes even beneficial. The beauty of the microbiome of cities is that it shows us an intimate picture of how we share our lives with them.
Work by the MetaSUB Consortium was presented at the ASM Microbe 2022 Conference, during the session entitled, "Metros to Monuments: Microbiomes of Built Environment Surfaces."
