Abstract
The emergence of antibiotic resistant bacteria is a major threat to modern medicine. Rapid adaptation to antibiotics is often mediated by the acquisition of plasmids carrying antibiotic resistance (ABR) genes. Nonetheless, the determinants of plasmid-mediated ABR gene transfer remain debated. Here, we show that the propensity of ABR gene transfer via plasmids is higher for accessory chromosomal ABR genes in comparison with core chromosomal ABR genes, regardless of the resistance mechanism. Analysing the pattern of ABR gene occurrence in the genomes of 2635 Enterobacteriaceae isolates, we find that 33% of the 416 ABR genes are shared between chromosomes and plasmids. Phylogenetic reconstruction of ABR genes occurring on both plasmids and chromosomes supports their evolution by lateral gene transfer. Furthermore, accessory ABR genes (encoded in less than 10% of the chromosomes) occur more abundantly in plasmids in comparison with core ABR genes (encoded in greater than or equal to 90% of the chromosomes). The pattern of ABR gene occurrence in plasmids and chromosomes is similar to that in the total Escherichia genome. Our results thus indicate that the previously recognized barriers for gene acquisition by lateral gene transfer apply also to ABR genes. We propose that the functional complexity of the underlying ABR mechanism is an important determinant of ABR gene transferability.This article is part of the theme issue ‘The secret lives of microbial mobile genetic elements’.
Highlights
Bacteria harbour vast potential to rapidly adapt to different selective environments, including environments defined by antibiotics
The results show that the antibiotic resistance (ABR) gene occurrence in plasmids and chromosomes bears similarity to the distribution of the total gene families in Escherichia genomes: in both datasets homologues of core chromosomal genes found in greater than or equal to 90% of the chromosomes are less abundant in plasmids in comparison with homologues of accessory chromosomal genes found in fewer than or equal to 10% of the chromosomes
We performed a comprehensive ABR gene analysis across 2635 complete genome sequences in the related bacterial genera Escherichia, Salmonella and Klebsiella, and identified an inverse association between ABR gene prevalence in plasmids and chromosomes. This inverse association strongly suggests that the presence of a homologous gene in the chromosome poses a barrier to plasmid-mediated ABR gene acquisition
Summary
Bacteria harbour vast potential to rapidly adapt to different selective environments, including environments defined by antibiotics. The acquisition of novel laterally transferred genes may have deleterious effects on the recipient owing to diverse reasons ranging from the consequences of foreign DNA integration into the genome to proper expression and function of the protein product in the cell ABR mechanisms that rely on drug inactivation may require a lower energetic investment (i.e. in ATP) of the cell in comparison with efflux pumps [24] Such trade-offs in the adaptation of ABR plasmids in newly colonized hosts are expected to have consequences for the evolution of plasmid ABR gene content. A recent study suggests that the evolution of plasmid ABR gene content depends on the level of genetic conflicts with chromosomally encoded genes, which is strongest for ABR genes encoding efflux pumps and weakest for ABR genes encoding antibiotic target inactivation mechanisms [7]. We further assess whether ABR gene occurrence on plasmids and chromosomes is associated with the resistance mechanism and inferred ABR gene transfer events using phylogenetics and the temporal pattern of gene occurrence in plasmids and chromosomes
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