A network approach to decipher the dynamics of Lysobacteraceae plasmid gene sharing

Plasmids provide an efficient vehicle for gene sharing among bacterial populations, playing a key role in bacterial evolution. Network approaches are particularly suitable to represent multipartite relationships and are useful tools to characterize plasmid-mediated gene sharing events. The bacterial family Lysobacteraceae includes plant commensal, plant pathogenic and opportunistic human pathogens for which plasmid-mediated adaptation has been reported. We searched for homologues of plasmid gene sequences from this family in the entire diversity of available bacterial genome sequences and built a network of plasmid gene sharing from the results. While plasmid genes are openly shared between the bacteria of the family Lysobacteraceae, taxonomy strongly defined the boundaries of these exchanges, which only barely reached other families. Most inferred plasmid gene sharing events involved a few genes only, and evidence of full plasmid transfers were restricted to taxonomically closely related taxa. We detected multiple plasmid-chromosome gene transfers, including the known sharing of a heavy metal resistance transposon. In the network, bacterial lifestyles shaped substructures of isolates colonizing specific ecological niches and harbouring specific types of resistance genes. Genes associated with pathogenicity or antibiotic and metal resistance were among those that most importantly structured the network, highlighting the imprints of human-mediated selective pressure on pathogenic populations. A massive sequencing effort on environmental Lysobacteraceae is therefore required to refine our understanding of how this reservoir fuels the emergence and the spread of genes among this family and its potential impact on plant, animal and human health.

Automated summary

Plasmids play a key role in bacterial evolution by providing an efficient means for gene sharing among bacterial populations. Network approaches are useful tools for characterizing plasmid-mediated gene sharing events. In the bacterial family Lysobacteraceae, plasmid-mediated adaptation has been reported. Through a comprehensive analysis of bacterial genome sequences, we found that plasmid genes were predominantly shared within the family Lysobacteraceae, with limited exchanges occurring with other families. These sharing events mostly involved a small number of genes and complete plasmid transfers were restricted to closely related taxa. Our findings also revealed multiple plasmid-chromosome gene transfers, including the sharing of heavy metal resistance genes. The network analysis showed that bacterial lifestyles and the presence of specific resistance genes influenced the structure of the network, highlighting the impact of human-mediated selective pressures on pathogenic populations. To better understand how this reservoir contributes to the emergence and spread of genes within the family and its potential impact on plant, animal, and human health, a large-scale sequencing effort on environmental Lysobacteraceae is necessary.