Each of us is home to a complex ecosystem of microbes that took up residence on or in us as soon as we emerged from our mother’s womb. In fact, our passage to the outside world — whether via vaginal birth or C-section — makes a significant contribution to the bacteria, fungi and viruses that become our constant life companions. Collectively, they are known as our microbiota, and by the age of three, the ecosystems that we harbour on every patch of skin and turn of the intestine are very similar to those of our parents.
While it may not be surprising that parents share microbes with their kids, researchers at Macquarie University in Sydney have found that animal handlers may be sharing their microbes with their furry captive charges. In doing so, keepers working in captive breeding programs could be unwittingly releasing more back into the wild than they had planned. Top on the list of unintended releases are antibiotic resistance genes.
Captive breeding programs have become the modern preserve of the otherwise outdated institution, the zoo. And many endangered species would long be extinct if it weren’t for the regular injection of new individuals born in captivity. But in the process of breeding endangered animals in captivity, the animals are exposed to humans and other domesticated and captive animals to a far greater extent than if they were in the wild. This close proximity brings with it the potential for pathogens, as well as non-pathogenic commensal microbes, to be shared between animals and their handlers.
The brush-tailed rock wallaby (Petrogale penicillata) stands around half a meter tall and weighs between 5 and 10 kg. But you wouldn’t get much of a measure of one if you saw it in the wild: rock wallabies dart across steep rocky outcrops along the Great Dividing Range in South Eastern Australia, their long tails balancing their agile hops. Rock wallabies are classified as a threatened species in Australia, and a species recovery program has been instigated to help bolster wild populations. Captive-bred wallabies are released into the wild, and translocations of wallabies between wild populations also help to ensure that each population maintains a diverse and robust gene pool.
With all of this movement and co-mingling between wallabies and their handlers, there is ample opportunity for microbes to be spread from one population — even one species — to the next. Michelle Power and her colleagues were curious to know how much microbial movement was taking place. Of particular interest was whether captive wallabies were picking up antibiotic resistance genes during their tenure at the wildlife park where they were bred.
Antibiotic resistance genes thwart many of our efforts to curb the spread of bacterial diseases. Bacteria are notorious for eagerly sharing genetic elements that contain antibiotic resistance genes, enabling the rapid spread of antibiotic resistance in human, as well as animal pathogens. One such genetic element is the integron, a highly mobile stretch of DNA that contains a simple set of instructions that allow it to cut and paste itself between the genome of one bacterial cell and that of the next. Central to the integron is a gene coding for integrase, an enzyme that carries out the cut/paste function. Integrons also frequently carry a gene coding for resistance to a particular antibiotic.
Power and her colleagues collected faecal samples from captive rock wallabies and five populations of wild wallabies and tested them for the presence of class I integrons, the most common type of integron in clinical pathogens, as well as human commensals. (Class I integrons are also common in molecular biology labs, where researchers use the simple genetic elements as markers for genetic cut/paste experiments carried out in lab strains of bacteria.)
Faecal samples from the wild wallabies came up clean — no integrons were detected in any of the samples from 65 individuals tested. Their captive counterparts were a different story. Half of the faecal samples contained integrons, bearing genes that conferred resistance to up to three antibiotics: streptomycin, spectinomycin and trimethoprim.
By directly sequencing the DNA present in the faecal samples — searching the faecal microbiomes — for the integron sequences, the team were able to detect the genes they were looking for in samples that might not have yielded viable bacterial cultures in the lab. One drawback, however, is that without having isolated the integron-containing bacteria from the wallaby poo, they aren’t able to tell where the integrons come from. Perhaps the wallabies’ guts have been colonised by human integron-carrying microbes. But animals and their microbiota have co-evolved for millenia, and studies of inter-species poo transplants indicate that microbes can be pretty finicky when it comes to choosing a home.
Another possibility is that wallaby and human microbes have co-mingled, allowing for the transfer of integrons from the human microbes to the wallaby microbes. A final possibility, which to me seems most likely, is that other captive and domesticated animals within the wildlife sanctuary have picked up integron-containing microbes over time, and the faeces from these animals is the source of the antibiotic resistance elements. All three antibiotics are commonly used in veterinary practice, and resistance to them would readily evolve in the microbiota at a wildlife sanctuary or zoo that uses them. Human beings, perhaps working in molecular biology labs, may have been the original source of the antibiotic resistance genes, but intermediaries were likely involved.
Wherever the resistance genes came from, the study highlights the potential for unintended consequences in captive breeding campaigns. It also suggests that careful management practices are required to prevent the spread of genes and pathogens from captive animals to wild populations, and between wild populations in the case of translocations.
Reference: Power, Emery & Gillings. (2013). Into the wild: dissemination of antibiotic resistance determinants via a species recovery program. PLoS ONE 8(5): e63017. doi:10.1371/journal.pone.0063017