Microbes are everywhere.
On door knobs, in your mouth, covering the New York City Subway, and festering on the kitchen sponge. The world is teeming with microbes—bustling communities of invisible organisms, including bacteria and fungi. Scientists are hard at work cataloging the microbial communities of people, buildings, and entire ecosystems. Many discoveries have shed light on how culture and behavior shape these communities. For example, we now know some interesting things about human skin microbes: hand microbes can be transplanted to other people and objects, wearing deodorant changes the microbes that live in our armpits, and people are more similar (in terms of microbe composition) to their own dogs than to other dogs.
Indeed, microbes are everywhere.
However, the majority of what we know about human-microbe interactions comes from studies in industrialized settings like the US and Europe, where people spend most of their time indoors and disconnected from the natural environment. This lifestyle is drastically different from those of early humans. Whereas we used to run across the savanna to hunt game, we now run on the treadmill to burn off that extra slice of pizza. Because our culture evolves faster than our bodies, we can become mismatched to our new environment, which often has direct consequences for our health. It is easy to imagine that our contact with the outside world, and its microbes, has changed since the era of our ancestors. What is less clear, though, is if these changes create microbial mismatches that influence health.
Many human populations still live in close contact with the natural environment, and skin microbe communities in these settings often reflect regular interactions with the outdoors. Studies of these communities are important for considering mismatch, as this setting more closely resembles the environment in which humans evolved. With this in mind, I traveled to Mandena, a rural village in Madagascar, to investigate how contact with the natural environment affects skin microbes. Here, rice and vanilla farming is common, and many farmers use zebu (domesticated cattle) to work in the fields. We wondered if humans in close contact with zebu display a “microbial fingerprint” of interacting with livestock, similar to what would be expected in Westerners that interact closely with pets.
To research this question, we obtained skin swab samples from twenty men living in Mandena, supported by Duke University’s Bass Connections and the Duke Global Health Institute. We sampled four sites on each person (back of hand, outside of ankle, inside of forearm, and armpit) and the back of each zebu. We predicted that the skin microbes of the ten men who work with zebu would be different than those of the ten men who do not. We also expected to find differences in skin microbe communities across body sites. For example, dry, bare feet that are exposed to the outside environment should harbor different microbes than warm, unexposed armpits.
We were surprised to discover that despite close contact with zebu, the skin microbe communities of zebu owners were not markedly different from those of men who did not own zebu. It may be that other factors, such as host genetics and skin pH, are important in determining whether or not a given body site is a good home for microbes. However, there were clear differences in microbe communities across body sites. Ankle samples were the most similar to zebu samples, which is likely due to the shared environment of zebu and human feet (often without shoes) in the fields. Sure enough, zebu owner ankles harbored soil bacteria, including taxa that include pathogens for humans, plants, and animals.
We also tested the hypothesis that there would be microbial similarities between a given zebu and its owner (remember the dog study?). Interestingly, we found that a zebu was no more similar to its owner than to other owners. We think these results indicate a type of environmental mismatch. Aspects of the built environment, like the use of cleaning products and air conditioning units, affect which microbes are present alongside humans and their indoor pets. The variability across home microbial communities likely amplifies microbial similarities within each cohabiting dog-owner pair. In other words, you and your dog are exposed to the same indoor microbes, which are likely different from the ones that your neighbor contacts in his home. In contrast, all homes in Mandena are constructed from plant material and more closely resemble the outside “home” environment of zebu. Thus, it is likely that all humans and all zebu have ample opportunities to contact similar types of environmentally-derived microbes.
Our results indicate that contact with the environment, not solely with zebu, is one driver of skin microbial communities in Mandena. Thinking about lifestyle differences that influence contact with environmental microbes can help to tackle issues of health disparities. If certain microbes are linked to disease, are people living or working in environments rich with those microbes more susceptible to getting sick? If so, how can we use our understanding of microbes and mismatches to tackle these problems? Incorporating the microbiomes of non-industrialized populations can help us understand how associated health outcomes differ across the world, especially in populations that are typically targeted for other global public health initiatives. Answering these types of questions is critical if we wish to use microbiome research to improve health, and will require interdisciplinary efforts across microbial ecology, evolution, and global public health.