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  • Review Article
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Call of the wild: antibiotic resistance genes in natural environments

Key Points

  • Antibiotic-resistant bacteria, which are a serious threat to the treatment of bacterial diseases, arise as a result of exposure to antibiotics in clinical and agricultural settings. However, antibiotic resistance genes are also naturally present in microbial communities regardless of human influence. Research is needed to understand the emergence and spread of resistance genes among all environments.

  • Antibiotic resistance in bacteria that are associated with wild animals is correlated with the proximity of the animals (and the bacteria) to human populations. Wild animals, and migratory wild birds in particular, are important contributors to the widespread dissemination of antibiotic resistance genes.

  • Microbial communities harbour antibiotic-resistant bacteria regardless of the human use of antibiotics, as evidenced by the presence of novel mechanisms of resistance and phylogenetically divergent resistance genes in unpolluted soil microbial communities.

  • Resistance to antibiotics may be a side effect of the original function of certain gene products, such as efflux pumps. Understanding the function of these gene products in natural microbial communities may uncover new ways of inhibiting the development of resistance in pathogens.

  • The roles of so-called antibiotic resistance genes in natural microbial communities is unknown, although potential roles include antibiotic resistance, metabolic diversification and signal disruption. The fitness conferred by resistance genes to bacteria in their native hosts and habitats needs further study.

  • Future work should focus on standardizing the methods used to acquire data about environmental antibiotic resistance genes and on understanding the many factors affecting the spread of antibiotic resistance genes.

Abstract

Antibiotic-resistant pathogens are profoundly important to human health, but the environmental reservoirs of resistance determinants are poorly understood. The origins of antibiotic resistance in the environment is relevant to human health because of the increasing importance of zoonotic diseases as well as the need for predicting emerging resistant pathogens. This Review explores the presence and spread of antibiotic resistance in non-agricultural, non-clinical environments and demonstrates the need for more intensive investigation on this subject.

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Figure 1: Mechanisms of antibiotic resistance in a Gram-negative bacterium.
Figure 2: Sources and movement of antibiotic resistance genes in the environment.
Figure 3: Detecting antibiotic genes in natural samples.

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Acknowledgements

J. Handelsman was supported by the US Department of Agriculture Microbial Observatories Program and J. Donato was supported by the US National Institutes of Health (grant GM876102).

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Burkholderia cepacia

Escherichia coli

Pseudomonas aeruginosa

Pseudomonas fluorescens

Shewanella oneidensis

Staphylococus aureus

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Glossary

Resistotype

The antibiotic resistance genotype and phenotypeof a bacterium.

Pristine

Unspoiled or unpolluted by human activities.

Parvome

The range of biologically active, low-molecular-mass (< 5 kDa) compounds that are produced by defined biosynthetic pathways in bacteria, yeast, plants and other organisms.

Antibiosis

An interaction between microorganisms involving a small molecule that is produced by one organism and detrimental to the other.

Hormesis

A dose-dependent response phenomenon shown by bioactive compounds and drugs, such that they have contrasting activities at low (subinhibitory) and high (inhibitory) concentrations.

Potentiator

A compound or molecule that augments the activity of an antibiotic.

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Allen, H., Donato, J., Wang, H. et al. Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Microbiol 8, 251–259 (2010). https://doi.org/10.1038/nrmicro2312

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