What’s in the microbiome of your city? Bees might be able to tell us

In 2010, a beekeeper in Brooklyn, New York, noticed something weird: his bees were starting to produce red honey. And not just rusty red, but a shocking shade of scarlet.

It came to be known as the mystery of the red honey, and a clue to the answer, says Kevin Slavin, an independent researcher formerly at Massachusetts Institute of Technology, came when investigators realized there was a maraschino cherry factory about a mile from the hives. The bees, it turned out were stealing syrup from the plant, and the dye used in making maraschino cherries was making its way into their honey.

It was, of course, a problem for the beekeeper (the maraschino honey reportedly tasted awful), but years later, Slavin and other researchers got to wondering if it might be possible to take advantage of the foraging behavior of bees to use them to probe urban environments in ways not previously possible.

Bees, of course, are only interested in collecting materials of use to bees. “But in the meantime,” Slavin says, “they’re also picking up everything else they touch.”

In a paper in last week’s issue of Environmental Microbiome, a team spearheaded by Slavin and Dr Elizabeth Hénaff of New York University’s Tandon School of Engineering, collected samples from rooftop beehives not only in New York, but in Tokyo, Venice, Sydney, and Melbourne, in an effort to see what they might reveal about the urban microbiome.

We usually think of the microbiome in terms of the human microbiome, the collection of microbes living in us and on us. But, Hénaff says, “the human microbiome interacts with the environmental microbiome. So, it’s important to be able to characterize the microbiomes of the cities we live in, work in, and sleep in.”

“The human microbiome interacts with the environmental microbiome. So, it’s important to be able to characterize the microbiomes of the cities we live in, work in, and sleep in.”

Elizabeth Hénaff

Historically, she says, the best tool for doing this has been the swab — something years of COVID-19 have made many of us uncomfortably familiar with. But you can’t swab everything. And in addition to microbes living on various surfaces, there is also what microbial ecologist Professor Jack Gilbert of the University of California, San Diego, has dubbed: “the microbial cloud” in the air surrounding everything we encounter.

Beehives have tens of thousands of bees, typically foraging over ranges of one to three kilometres — flying swabs that not only crawl into all kinds of nooks and crannies, but obligingly bring back to the hive whatever microorganisms they’ve inadvertently collected along the way. Including those from whatever microbial clouds they’ve flown through.

Hénaff’s and Slavin’s team initially presumed that the best place to look for traces of this would be in the honey. After all, the maraschino honey had been laden with the red dye used in maraschino cherries.

Bees are flying swabs that not only crawl into all kinds of nooks and crannies, but obligingly bring back to the hive whatever microorganisms they’ve inadvertently collected along the way.

But when it comes to microorganisms, it turns out, that doesn’t work. Instead, the team found, bees are very good at keeping unwanted microorganisms out of it. Instead, they tend to shake them off with other debris they’ve collected along the way.

Slavin has an apt analogy. “It’s basically like, when the bees get home, they kind of wipe their feet on the mat,” he says. Except that in this case, rather than collecting on the doormat, the debris falls to the bottom of the hive, forming a thin layer of fine particles, which the researchers were able to collect via specially installed trays.

One early finding, Hénaff says, was that different cities really do have distinct microbial signatures and that these do show up in the materials collected by the bees.

Different cities really do have distinct microbial signatures and that these do show up in the materials collected by the bees.

“For example,” she says, “in Venice, one of the main species we found were fungi related to wood rot — which makes sense because Venice is built on rotting pylons. And in Japan we found the species that’s responsible for fermentation products [such as soy sauce]. So, it didn’t feel like a disjoint from all the other things we know about these cities and their culture and history.”

For some reason, though, the samples from Sydney were full of a bacteria known to degrade rubber.

Slavin and Hénaff didn’t offer an explanation for this, but maybe their Sydney beehive was close to a big pile of old tires. One of the goals of the study, they say, is to find a way to determine how the microbiome varies not just from city to city but across different parts of a single city. “Does it change from East London to West London?” Slavin asks. “Does it change block by block?” As of now, nobody knows.

“The goal is more one of understanding the breadth of diversity of microbiomes we’re interacting with in urban environments.”

Elizabeth Hénaff

Also of interest is using bees to monitor the prevalence of human pathogens and to test the detected pathogens for genes related to their virulence.

That, in fact, is exactly what the researchers did in Tokyo, where, by happenstance, they detected Rickettsia felis. Unfortunately, they muddled their finding by mistakenly referring to it as the pathogen that causes cat scratch fever (it is actually a flea-borne pathogen spread by cat fleas that causes a form of spotted fever) but the key point is that they were able not only to identify it, but to measure its virulence for humans.

Read more: Varroa – and the threat of bee decimation – has now arrived. What have we learned from other nations’ devastation?

Not that the authors were specifically interested in pathogen surveillance. “The goal is more one of understanding the breadth of diversity of microbiomes we’re interacting with in urban environments,” Hénaff says. “Most microbes out there are not pathogenic. A lot are beneficial to human health, and even more are neutral from our perspective but may be very important for other species.”

In fact, she says, a growing body of research shows that exposure to diverse microbiomes is important for heath, especially for children in urban environments, where more natural microbiomes might be excluded. For example, she says, one study found that when the flooring material in outside playgrounds was changed from synthetic materials to wood chips, the resulting diversification of the microbiome was associated with an improvement in the health of the kids using it.

“Exposure to diverse environmental microbiomes is a key element of environmental justice.”

Elizabeth Hénaff

“Exposure to diverse environmental microbiomes is a key element of environmental justice,” she says, adding that from an urban planning perspective, one of the overarching goals of the study was to find a way to quantify this.

Gilbert (who was not part of the study team) warns, however, that there is a long way to go before any of the study’s goals can be accomplished.

To start with, he says, “if you wanted to prove that honeybees could be used to surveil the environment for microbial diversity or pathogens, then you would set up a series of microbial markers within a two-mile radius and determine the ability of the hive to ‘collect’ those signals. If you wanted to prove a link between detected [pathogens] and health, you would need to perform an epidemiological analysis at the same time.”

There is a long way to go before any of the study’s goals can be accomplished.

Hénaff agrees that this type of benchmarking—what other fields of research would call “ground truthing” is an issue. It is, in fact, exactly the type of challenge faced by public health officials when they first started using sewage to trace the spread of diseases like COVID-19 (and more recently, polio).

“We’ve thought long and hard about that,” she says.

Meanwhile, next time you see a honeybee buzzing around you, don’t panic. It might just be monitoring the health of your microbial cloud.