Evolutionary barriers to horizontal gene transfer in macrophage-associated Salmonella

Horizontal gene transfer (HGT) is a powerful evolutionary force facilitating bacterial adaptation and emergence of novel phenotypes. Several factors, including environmental ones, are predicted to restrict HGT, but we lack systematic and experimental data supporting these predictions. Here, we address this gap by measuring the relative fitness of 44 genes horizontally transferred from Escherichia coli to Salmonella enterica in infection-relevant environments. We estimated the distribution of fitness effects in each environment and identified that dosage-dependent effects across different environments are a significant barrier to HGT. The majority of genes were found to be deleterious. We also found longer genes had stronger negative fitness consequences than shorter ones, showing that gene length was negatively associated with HGT. Furthermore, fitness effects of transferred genes were found to be environmentally dependent. In summary, a substantial fraction of transferred genes had a significant fitness cost on the recipient, with both gene characteristics and the environment acting as evolutionary barriers to HGT.

Automated summary

Horizontal gene transfer is a powerful evolutionary force in bacterial adaptation, but it is constrained by environmental factors and gene characteristics. This study examines the fitness effects of 44 genes transferred from Escherichia coli to Salmonella enterica in infection-relevant environments, and finds that dosage-dependent effects and gene length are important barriers to HGT. Most transferred genes have deleterious effects, with longer genes having stronger negative fitness consequences. Additionally, the fitness effects of transferred genes vary in different environments. Overall, HGT incurs significant fitness costs on the recipient, with gene characteristics and the environment acting as evolutionary barriers.