Microorganisms, such as bacteria, live in almost every habitat on the planet. These include habitats in the environment such as soil and water, as well as habitats on animals and humans (i.e. on the skin or in the guts). Commensal microbes, those that live on animal hosts, are vital to the host’s ecology, behaviour, and health.
These microbial communities, collectively known as microbiomes, are not only omnipresent but can move rather freely between habitats. Bacteria can also exchange their genetic material in a unique way called lateral gene transfer, whereby they can share genes without reproducing (Imagine being able to give your genes to a friend just through a handshake, pretty convenient!). Thus, certain genes can easily spread within bacterial populations. So, what happens when the genes that are being spread are helpful to the microbes but potentially harmful to the animal host?
Microbes and mobile genes
One example is the spread of antibiotic resistance (ABR). In bacteria, ABR is the ability to resist the effects of antibiotics that would normally kill the bacteria. The genes that code for resistance occurs naturally at low levels as a response to natural antibiotics produced by other bacteria and fungi. These genes are numerous and can be spread between bacteria via lateral gene transfer. In other words, ABR genes are hugely beneficial to the microbes that harbour them, almost like a genetic ‘get out of jail free card’. But, what about the host? And what happens when man-made antibiotics are introduced into this system?
The global spread of ABR is a severe threats to human health. Bacteria are evolving resistance to man-made antibiotics at a staggering rate and so-called ‘super bugs’, diseases that are resistant to many antibiotics, are increasingly common. But we know very little about the dynamics of ABR in the environment. With the widespread use of antibiotics in agriculture, industry, and medicine, antibiotics and ABR have polluted natural environments all over the world. Wildlife living in habitats that are contaminated with these anthropogenic, or man-made, pollutants are at risk of picking up ABR that can propagate in the animal’s microbiomes. Scientists are recognizing that to better understand and improve the health and conservation of wild animals, we need to study the impact of ABR on animals and their environments. Here, we present two case studies, one from Madagascar and one from the Galapagos, and each about our own research on ABR in the environment.
Antibiotic resistance in lemurs of Madagascar (Sally Bornbusch)
Wild lemurs live in only one place on the planet; the island of Madagascar. Madagascar, a biodiversity hotspot, is home to some of the most fantastical creatures in the world, including over 100 species of lemurs. And, as primates, lemurs are some of our closest genetic relatives. But sadly, they are also one of the most endangered groups of animals on the planet. Habitat destruction threatens lemurs all across the island, including the most easily recognized of all lemurs, the ring-tailed lemur (think King Julien from the Madagascar movies).
These charismatic lemurs are one of the ‘hardiest’ lemur species and, unlike many lemur species, they can live in close proximity to humans. This ability to survive in tough environments is also why ring-tailed lemurs are often one of the only lemurs that you may see in a zoo. But what this means for wild ring-tailed lemurs is that they inhabit ‘degraded’ habitats that are strongly influenced by humans. Our research focuses on understanding how these anthropogenic factors can impact the microbiomes of lemurs living in Madagascar, specifically through the transmission of microbes and ABR between lemurs and their environments.
At this point you may be asking, why lemurs and why Madagascar? Well, Madagascar is a unique place to study antimicrobial resistance for a very specific reason: It is one of the only countries in the world that still experiences outbreaks of bacterial plague (yes, like the black plague). Because the plague impacts the health of thousands of Malagasy people, the specific antibiotics used to treat the plague are widely distributed and used across the country.
Furthermore, in Madagascar, antibiotics are often viewed as a ‘panacea’ and are widely sought after for any number of ailments (including those that would not be helped by antibiotics). But does this widespread usage of antibiotics by people have an impact on the lemurs? We now know that ABR is present in the gut microbiomes of wild ring-tailed lemurs. And, the types of resistance genes we find in the lemurs are those that reflect the antibiotics specifically used to treat the plague. These findings show that despite never having been given antibiotics, wild lemurs have developed ABR in their microbiomes. So, where they are getting it from? My hunch is that they are likely picking it up from their environments. The next steps will be to analyze soil and water samples from the lemurs’ environments and look for those same ABR genes (check back in a year or two for more results!).
Antibiotic resistance in Darwin’s Laboratory (Alyssa Grube)
Now let’s jump to another island system on the other side of the globe: the Galapagos! Treasured for their unique plant and animal species found nowhere else in the world, the Galapagos Islands of Ecuador are famous for inspiring Charles Darwin’s theory of evolution by natural selection. Every year, hundreds of thousands of tourists visit the Galapagos to walk among giant tortoises, dance with blue-footed boobies and sunbathe alongside sea lions (all at the appropriate 2-meter distance, of course!).
While it’s great that so many people appreciate these natural wonders, increasing tourism along with the resident population pose significant challenges for conservation. One of these challenges, in parallel to the situation that lemurs face in Madagascar, is the introduction of antibiotics and antibiotic-resistant bacteria into the Galapagos. Tourists travelling to the Galapagos carry not only passports and cameras, but also antibiotic-resistant bacteria in their gut microbiomes – and in some cases antibiotics that they use to in response to traveller’s diarrhoea.
We think that these factors, along with poor wastewater management in the Galapagos, could mean that human settlements are ‘hot spots’ for the introduction of ABR into the environment. This has us asking several questions: Does proximity to human settlements influence the type of ABR showing up in environmental samples, including wildlife gut microbiomes? Do different wildlife species carry different types of ABR genes? What does this all mean for the health and conservation of dear Lonesome George?
To get at answering these questions, my research takes advantage of a special characteristic of the Galapagos: across the islands, human settlements are restricted to 3% of the landmass, with the remaining 97% protected by the Galapagos National Park. This means we can compare samples from areas with intense human impact to remote areas that people can only visit by boat.
In this way, we can also begin to elucidate what kind of ABR might occur naturally in environments without significant anthropogenic inputs. So far, our analyses include environmental samples (freshwater, wastewater, marine water, soil, sand) and wildlife gut microbiome samples from marine iguanas, land iguanas, giant tortoises, sea turtles, red-footed boobies, and sea lions.
Although most of the wildlife samples have been generously collected by amazing collaborators, I’ve had the opportunity to go along on some fun field sampling days. Fun fact: marine iguanas are incredibly quick and agile over slippery lava rocks; we humans are not.
Finally, in recognition that bacteria and their genes can move freely between humans, animals, and the environment, we are also starting to look at the gut microbiomes of human residents on San Cristobal Island for a “One Health” survey of ABR in the Galapagos. All in all, I’m beyond grateful that I get to conduct my graduate research in this special place, and hope that our work can be used to prevent the spread of antibiotic resistance in the Galapagos and help preserve this unique ecosystem for generations to come.
You might be thinking that the spread of ABR presents a rather dire situation, and you would not be wrong. But it’s not all doom-and-gloom; by studying antimicrobial resistance in the environment, we can better understand how to prevent it from causing harm to the environment and animals, including humans. Because anthropogenic disturbance is the greatest modern threat that all wildlife face, understanding how ABR affects animal health and well-being will be vital to future conservation strategies.
For example, assessments of habitat quality could include analyses of pollutants such as ABR. This would allow scientists to better assess environmental and wildlife health. Furthermore, by characterizing ABR in wildlife and natural environments, we will gain a better understanding of how resistance genes move between bacterial communities, which is extremely important for minimizing the spread of ABR between animals, humans, and their environments.
Sally Bornbusch is Ph.D. student in Evolutionary Anthropology at Duke University. She loves to work with animals of all shapes and sizes, but her current research focuses on lemurs and their microbiomes. Her goal is to better understand how anthropogenic factors impact wildlife and their microbes. She is also an artist and avid nature photographer and hopes to use her art and photography to teach about the importance of the natural world and to show that science and art go hand-in-hand.
Alyssa Grube is a PhD student in Environmental Sciences & Engineering at the University of North Carolina Chapel Hill. With a background in microbiology, she loves to think about all the ways microbes shape environments both in and around us. Her research in the Galapagos aims to improve our understanding of antibiotic resistance in the environment, both naturally occurring and the result of human influence. Outside of lab, Alyssa is an avid bread baker and occasional quilter.