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The evolution of antibiotic resistance islands occurs within the framework of plasmid lineages

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  • Yiqing Wang

    (Kiel University)

  • Tal Dagan

    (Kiel University)

Abstract

Bacterial pathogens carrying multidrug resistance (MDR) plasmids are a major threat to human health. The acquisition of antibiotic resistance genes (ARGs) in plasmids is often facilitated by mobile genetic elements that copy or translocate ARGs between DNA molecules. The agglomeration of mobile elements in plasmids generates resistance islands comprising multiple ARGs. However, whether the emergence of resistance islands is restricted to specific MDR plasmid lineages remains understudied. Here we show that the agglomeration of ARGs in resistance islands is biased towards specific large plasmid lineages. Analyzing 6784 plasmids in 2441 Escherichia, Salmonella, and Klebsiella isolates, we quantify that 84% of the ARGs in MDR plasmids are found in resistance islands. We furthermore observe rapid evolution of ARG combinations in resistance islands. Most regions identified as resistance islands are shared among closely related plasmids but rarely among distantly related plasmids. Our results suggest the presence of barriers for the dissemination of ARGs between plasmid lineages, which are related to plasmid genetic properties, host range and the plasmid evolutionary history. The agglomeration of ARGs in plasmids is attributed to the workings of mobile genetic elements that operate within the framework of existing plasmid lineages.

Suggested Citation

  • Yiqing Wang & Tal Dagan, 2024. "The evolution of antibiotic resistance islands occurs within the framework of plasmid lineages," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48352-8
    DOI: 10.1038/s41467-024-48352-8
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    References listed on IDEAS

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    1. Santiago Redondo-Salvo & Raúl Fernández-López & Raúl Ruiz & Luis Vielva & María de Toro & Eduardo P. C. Rocha & M. Pilar Garcillán-Barcia & Fernando de la Cruz, 2020. "Pathways for horizontal gene transfer in bacteria revealed by a global map of their plasmids," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    2. Mislav Acman & Ruobing Wang & Lucy Dorp & Liam P. Shaw & Qi Wang & Nina Luhmann & Yuyao Yin & Shijun Sun & Hongbin Chen & Hui Wang & Francois Balloux, 2022. "Role of mobile genetic elements in the global dissemination of the carbapenem resistance gene blaNDM," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. Manuel Ares-Arroyo & Eduardo P C Rocha & Bruno Gonzalez-Zorn, 2021. "Evolution of ColE1-like plasmids across γ-Proteobacteria: From bacteriocin production to antimicrobial resistance," PLOS Genetics, Public Library of Science, vol. 17(11), pages 1-24, November.
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