Abstract
Plasmids are key drivers of bacterial evolution because they are crucial agents for the horizontal transfer of adaptive traits, such as antibiotic resistance. Most plasmids entail a metabolic burden that reduces the fitness of their host if there is no selection for plasmid-encoded genes. It has been hypothesized that the translational demand imposed by plasmid-encoded genes is a major mechanism driving the fitness cost of plasmids. Plasmid-encoded genes typically present a different codon usage from host chromosomal genes. As a consequence, the translation of plasmid-encoded genes might sequestrate ribosomes on plasmid transcripts, overwhelming the translation machinery of the cell. However, the pervasiveness and origins of the translation-derived costs of plasmids are yet to be assessed. Here, we systematically altered translation efficiency in the host cell to disentangle the fitness effects produced by six natural antibiotic resistance plasmids. We show that limiting translation efficiency either by reducing the number of available ribosomes or their processivity does not increase plasmid costs. Overall, our results suggest that ribosomal paucity is not a major contributor to plasmid fitness costs.This article is part of the theme issue ‘The secret lives of microbial mobile genetic elements’.
Highlights
Horizontal gene transfer (HGT) shapes bacterial evolution, allowing bacteria to expand to new ecological niches and thrive in a plethora of different environmental conditions [1]
Plasmid carriage and reduced translational capability should show negative epistasis for fitness. This hypothesis is based on the following three premises: (i) the translation machinery of wild-type E. coli is highly optimized to maximize growth rate in different environments and metabolic states [18,19]; (ii) exogenous genes compete with housekeeping genes for the translational apparatus, and the production of plasmid proteins diverts resources from the synthesis of essential proteins [20,21]; and (iii) bacterial growth rates are proportional to the available ribosomes and their peptide chain elongation rate [22]
Our results suggest that the translational demand of plasmid genes is not enough to account for their cost, suggesting that additional mechanisms might explain why plasmids tend to be costly in the absence of direct selection
Summary
Horizontal gene transfer (HGT) shapes bacterial evolution, allowing bacteria to expand to new ecological niches and thrive in a plethora of different environmental conditions [1]. Plasmid carriage and reduced translational capability should show negative (synergistic) epistasis for fitness This hypothesis is based on the following three premises: (i) the translation machinery of wild-type E. coli is highly optimized to maximize growth rate in different environments and metabolic states [18,19]; (ii) exogenous genes compete with housekeeping genes for the translational apparatus, and the production of plasmid proteins diverts resources from the synthesis of essential proteins [20,21]; and (iii) bacterial growth rates are proportional to the available ribosomes and their peptide chain elongation rate [22]. Our results suggest that the translational demand of plasmid genes is not enough to account for their cost, suggesting that additional mechanisms might explain why plasmids tend to be costly in the absence of direct selection
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