Phages rarely encode antibiotic resistance genes: a cautionary tale for virome analyses

Antibiotic resistance genes (ARGs) are pervasive in gut microbiota, but it remains unclear how often ARGs are transferred, particularly to pathogens. Traditionally, ARG spread is attributed to horizontal transfer mediated either by DNA transformation, bacterial conjugation or generalized transductio...

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Bibliographic Details
Published in:The ISME Journal Vol. 11; no. 1; pp. 237 - 247
Main Authors: Enault, François, Briet, Arnaud, Bouteille, Léa, Roux, Simon, Sullivan, Matthew B, Petit, Marie-Agnès
Format: Journal Article
Language:English
Published: London Nature Publishing Group UK 01.01.2017
Oxford University Press
Nature Publishing Group
Subjects:
45
631/326/22/1290
704/158/855
Anti-Bacterial Agents - pharmacology
Antibiotic resistance
Bacteriophages - genetics
Bacteriophages - metabolism
Biomedical and Life Sciences
Drug Resistance, Bacterial
E coli
Ecology
Escherichia coli
Escherichia coli - drug effects
Escherichia coli - genetics
Escherichia coli - virology
Evolutionary Biology
Genome, Viral
Life Sciences
Metagenome
Microbial Ecology
Microbial Genetics and Genomics
Microbiology
Original
original-article
Quantitative Methods
Viral Proteins - genetics
Viral Proteins - metabolism
ISSN:1751-7362, 1751-7370
Online Access:Get full text
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Summary:Antibiotic resistance genes (ARGs) are pervasive in gut microbiota, but it remains unclear how often ARGs are transferred, particularly to pathogens. Traditionally, ARG spread is attributed to horizontal transfer mediated either by DNA transformation, bacterial conjugation or generalized transduction. However, recent viral metagenome (virome) analyses suggest that ARGs are frequently carried by phages, which is inconsistent with the traditional view that phage genomes rarely encode ARGs. Here we used exploratory and conservative bioinformatic strategies found in the literature to detect ARGs in phage genomes, and experimentally assessed a subset of ARG predicted using exploratory thresholds. ARG abundances in 1181 phage genomes were vastly overestimated using exploratory thresholds (421 predicted vs 2 known), due to low similarities and matches to protein unrelated to antibiotic resistance. Consistent with this, four ARGs predicted using exploratory thresholds were experimentally evaluated and failed to confer antibiotic resistance in Escherichia coli . Reanalysis of available human- or mouse-associated viromes for ARGs and their genomic context suggested that bona fide ARG attributed to phages in viromes were previously overestimated. These findings provide guidance for documentation of ARG in viromes, and reassert that ARGs are rarely encoded in phages.
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PMCID: PMC5315482
ISSN:1751-7362
1751-7370
DOI:10.1038/ismej.2016.90