New microbes thrive in the concrete jungle

New research shows that city microbes have adapted to survive on disinfectants

Even on our loneliest day, no person is ever truly alone, because our bodies shelter trillions of microbes; everything from single-celled organisms called archaea to fungi, bacteria and viruses. Together, they inhabit almost every surface on – and crevice within – us beyond our own cells. 10 to 1. While it might sound a little strange to be immersed in a microbial “soup,” it’s generally not harmful to us. And in fact, they provide functions that are vital to our health, such as supporting our immune response and our digestive system. Each human microbiome is entirely unique, slightly influenced by our genetics, but especially our surroundings.

Like humans, every city on Earth has its own microbiome; its microbial community shaped by residents and visitors of all species and the lives they lead in the built environment. Geography, weather and climate, building materials, infrastructure design and ventilation are just some of the factors that influence the urban microbial landscape. Location also plays a role – the diversity of microbes present will differ greatly between the soil of an urban park, a sewage pipe or a concrete covered parking lot. But no matter where you go in a city, you’ll interact with organisms too small to see.

Scientists have studied urban microbiomes with increasing interest for decades. As more of Earth’s human population moves into cities, understanding the relationships we have—whether harmful, benign, or beneficial—with these microbial communities will become increasingly important.

A global research consortium called MetaSUB (International metagenome and Metadesign of Subways and Urban Biomes) is leading the charge in this effort. Launched in 2015 to address the knowledge gap in urban microbial ecosystems, members are now participating in a synchronized sampling event on the 21st.^St June every year. During this “Global City Sampling Day,” researchers are collecting samples of DNA, RNA, and microbes from surfaces in subways, buses, airports, and other public spaces in cities around the world.

In 2021, MetaSUB published what they describe as “the first large-scale global metagenomic study of urban microbiomes.” It involved researchers from 60 cities, who together collected and processed 4,728 samples from at least three common surfaces (railings, benches and ticket kiosks) in their local mass transit systems; these locations were used as proxies for the microbiome of the city as a whole. The study revealed a “core” urban microbiome in all cities, with the same 31 microbes present – ​​in varying amounts – in more than 97% of the samples. However, they also found “distinct geographic variations” between cities, as well as “regional signatures,” suggesting that each city’s microbiome is unique.

Resistant to cleaning

A member of the MetaSUB consortium is Dr Xinzhao Tong, Assistant Professor at Xi’an Jiaotong-Liverpool University (XJTLU), China. In her latest studyshe reports that some of the microbes found in urban environments are evolving to resist the cleaning agents we typically use to remove them.

“I’ve been studying the microbiome of the built environment since my PhD,” she says, speaking to me on Zoom. “I started looking at the diversity of microbes present in different types of urban environments, such as residences, malls, subways. But I found myself wondering how these microbes survive. Many of the areas we study are already poor in traditional nutrients, and our use of cleaning products adds additional stress. This differentiates the built environment from other microbial habitats.”

To investigate how so many types of microorganisms have adapted to life in the concrete jungle, Tong and her team took 738 samples from a variety of locations in Hong Kong; one of the most densely populated regions on the planet. Samples included subway air, commonly touched surfaces in platforms, private residences, subways and public facilities, as well as from the skin surfaces of human participants.

They then used an advanced technique called shogun metagenomics to identify all the genes (short pieces of DNA) from all the microorganisms present in each sample. By comparing these DNA fragments to a vast database of known genes, Tong was able to confirm which were known and which were new. In addition, says Tong, “Because each gene encodes specific functions, the technique allows us to characterize the functions of these uncharacterized species and understand a little more about how they adapt to their environment.”

From this, the team identified 373 microbial strains that had never been previously reported in an urban environment. Two new strains of a microbe named Pathescibacteria were recovered from skin samples. This microbe is considered a “parasite” because it usually relies on bacterial hosts to provide its nutrients. But these new strains appear to have the ability to produce two antioxidants – carotenoids and ubiquinone – that we humans need to survive. “We typically get them, especially carotenoids, through our diet,” says Tong. This suggests “a possible mutualistic relationship between the bacteria and us as hosts.”

The most surprising discovery was a new strain of Eremiobacterota on skin samples and from a private residence. This microbe is more often associated with the harsh and acidic environmental conditions of Antarctic soil. First attracted attention in 2021 when it was discovered that it could “fix” carbon by oxidizing trace gases in the atmosphere and using them as an energy source. The Eremiobacterota the strain found in the city’s samples had genes capable of using a different fuel source, as Tong explains, “We noticed that this microbe seems to be able to metabolize some of the traditional disinfectant ingredients that are widely used in cleaning. Things like alcohols some inorganic salts. We know we want to create a clean built environment, especially after the COVID pandemic, but I feel like microbes are very smart. They are trying to evolve to resist our cleaning strategy.”

Clinical environments

Tong was quick to assure me that none of the microbes identified in her study have been shown to be pathogenic—that is, capable of causing human disease. She also explained that shogun metagenomics does not distinguish between living and dead microbes, “it is difficult to confirm the viability of microbes from the results. But if a microbe has the genes, we can say it has the potential to survive and adapt to the built environment, outperforming other strains.”

While research by Tong, and others, suggests that cities contain large number of antimicrobial resistant genesand many surfaces in transit systems are recolonized with microbes within minutes of cleaningthis does not necessarily mean that cities are more microbially “dangerous” for healthy people than other areas.

However, as she sees it, there are risks for immunocompromised people that should not be ignored, “There is a phenomenon we call cross-resistance, which means that if this microbe is resistant to disinfectants, it can also develop resistance to antibiotics. And if this microbe is able to affect humans, then that resistance is a problem, especially for those with compromised immune systems.” If that’s you, she says, “it might be a good idea to protect yourself by wearing a mask, especially in crowded indoor areas because pathogens are opportunistic.”

In clinical settings such as hospitals, these opportunistic pathogens can be life-threatening. Rates of hospital-acquired infections associated with antimicrobial resistance have increased significantly during the COVID pandemic and are still raised today. This led Tong and his colleagues to begin a new research project focused on hospital surfaces frequently touched by healthcare workers. Her analysis is still ongoing and the research has yet to be published, but she says they have found some genes that show resistance to disinfectants and heavy metals (factors that have been linked to antibiotic resistance). “Even though we put so much effort into cleaning hospitals, it seems we can’t eradicate all pathogens. My hypothesis is that some microbes have adapted to the hospital environment, and the pressures we exert to clean or kill those pathogens may actually promote their resistant development. We need to do something about the disinfection strategies that hospitals use, or we’ll just keep isolating resistant microbes.”