This is the first time FEMS Microbiology Reviews has presented such an award, and the decision of the three Editors-in-Chief was unanimous. The paper recieved the most citations in 2019 of all recent papers (2017 – now) and moreover, it clearly outlines an important aspect of the global AMR health problem. We interviewed Johan to find out more about the inspiration behind this paper:
Johan Bengtsson-Palme, Assistant Professor at the Sahlgrenska Academy at the University of Gothenburg (Sweden).
Could you provide a brief, simple overview of the topic your paper covers?
This review essentially covers how the environment influences the development of antibiotic resistance in bacteria. In the paper, we look both at transmission of resistant bacteria and how the environment can act as a source for novel resistance genes. Since the environment hosts a super-diverse set of bacteria, it is likely that many many more resistance factors exist in nature than those we have seen this far in human pathogens.
However, unless there is selection favouring that these genes make the jump into human-associated bacteria, that is unlikely to happen. We therefore also look at how we can prevent different selection scenarios from occurring. Finally, we discuss which consequences exposure to antibiotics in the environment can have in addition to selecting for resistance.”
Have environmental factors been neglected in the global conversation about antibiotic resistance?
Traditionally, yes, but that is starting to change. I think that I personally now see a development towards a greater attention to that not only the clinical and agricultural sectors are important in resistance development. The antibiotic resistance conversation is definitely more diverse now than it was ten years ago, when essentially only clinical and – to some extent – agricultural interventions were discussed.”
The role of the environment in the recruitment of antibiotic resistance genes (ARGs) to human pathogens includes four major steps: (1) emergence of novel resistance factors in the environment, (2) mobilization onto mobile genetic elements, (3) transfer of ARGs to human pathogens, and (4) dissemination of ARGs into the human microbiome.
What encouraged you to review research this area of microbiology?
One of the main motivations for writing this review paper is that I think that much of the conversation about the environment’s role in antibiotic resistance development has been misinformed and that the focus often ends up being on the wrong questions. For example, while the environment can definitely serve as a dissemination route for resistant bacteria, spread through the environment of bacteria that already are common in the clinics and in human populations are probably not our greatest concern. Those bacteria are simply much more likely to spread directly between humans rather than through environmental compartments, so every dissemination event via the environment has relatively minor consequences in a global perspective.
Compare that to the role the environment plays in the development of novel types of resistance, never seen before in human pathogens. Every individual such event has consequences that are extremely hard to predict, but in the worst case they can lead to dramatically reduced treatment ability globally, if the new resistance gene is sufficiently well spread among bacterial populations. The risks here are hard to assess, but very often these two very different scenarios are muddied into the same concept of “risk”. In this paper, we wanted to be more concise about the different roles the environment can play in resistance development and the different types of risks that those roles are associated with.”
What do you see as the next steps in this area of research?
What we describe in this review is pretty much the concepts of how antibiotic resistance develops and spreads in the environment. This conceptual understanding is fairly established – what is missing, however, is numbers. We have very little knowledge of how relatively
important the different processes for resistance development are and therefore any model-building in this area largely becomes a guesswork.Here, I see the logical next step in environmental resistance research: to find out the concentrations of antibiotics needed to select for resistance in complex systems, the concentrations that drive transfer of resistance genes between bacteria and the magnitude of different dispersal routes for resistant bacteria. Another understudied subject that is also related to resistance development is the study of other effects of antibiotic exposure. Could exposure to antibiotics in the environment lead to that genes conferring other traits are mobilized and spread in bacterial communities, such as virulence genes or genes involved in persistence mechanisms? That is still an open question which I think warrants more research.”
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