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An antiplasmid system drives antibiotic resistance gene integration in carbapenemase-producing Escherichia coli lineages

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  • Pengdbamba Dieudonné Zongo

    (Institut Pasteur
    Sorbonne Université
    Université Paris Cité)

  • Nicolas Cabanel

    (Institut Pasteur
    Université Paris Cité)

  • Guilhem Royer

    (Institut Pasteur
    Université Paris Cité)

  • Florence Depardieu

    (Université Paris Cité
    Institut Pasteur)

  • Alain Hartmann

    (Université Bourgogne Franche-Comté)

  • Thierry Naas

    (Paris-Saclay University
    Bicêtre Hospital, APHP
    Bicêtre Hospital)

  • Philippe Glaser

    (Institut Pasteur
    Université Paris Cité)

  • Isabelle Rosinski-Chupin

    (Institut Pasteur
    Université Paris Cité)

Abstract

Plasmids carrying antibiotic resistance genes (ARG) are the main mechanism of resistance dissemination in Enterobacterales. However, the fitness-resistance trade-off may result in their elimination. Chromosomal integration of ARGs preserves resistance advantage while relieving the selective pressure for keeping costly plasmids. In some bacterial lineages, such as carbapenemase producing sequence type ST38 Escherichia coli, most ARGs are chromosomally integrated. Here we reproduce by experimental evolution the mobilisation of the carbapenemase blaOXA-48 gene from the pOXA-48 plasmid into the chromosome. We demonstrate that this integration depends on a plasmid-induced fitness cost, a mobile genetic structure embedding the ARG and a novel antiplasmid system ApsAB actively involved in pOXA-48 destabilization. We show that ApsAB targets high and low-copy number plasmids. ApsAB combines a nuclease/helicase protein and a novel type of Argonaute-like protein. It belongs to a family of defense systems broadly distributed among bacteria, which might have a strong ecological impact on plasmid diffusion.

Suggested Citation

  • Pengdbamba Dieudonné Zongo & Nicolas Cabanel & Guilhem Royer & Florence Depardieu & Alain Hartmann & Thierry Naas & Philippe Glaser & Isabelle Rosinski-Chupin, 2024. "An antiplasmid system drives antibiotic resistance gene integration in carbapenemase-producing Escherichia coli lineages," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48219-y
    DOI: 10.1038/s41467-024-48219-y
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    1. Kathryn Tunyasuvunakool & Jonas Adler & Zachary Wu & Tim Green & Michal Zielinski & Augustin Žídek & Alex Bridgland & Andrew Cowie & Clemens Meyer & Agata Laydon & Sameer Velankar & Gerard J. Kleywegt, 2021. "Highly accurate protein structure prediction for the human proteome," Nature, Nature, vol. 596(7873), pages 590-596, August.
    2. Lidiya Lisitskaya & Alexei A. Aravin & Andrey Kulbachinskiy, 2018. "DNA interference and beyond: structure and functions of prokaryotic Argonaute proteins," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    3. Aida Alonso-del Valle & Ricardo León-Sampedro & Jerónimo Rodríguez-Beltrán & Javier DelaFuente & Marta Hernández-García & Patricia Ruiz-Garbajosa & Rafael Cantón & Rafael Peña-Miller & Alvaro San Mill, 2021. "Variability of plasmid fitness effects contributes to plasmid persistence in bacterial communities," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    4. Allison J. Lopatkin & Hannah R. Meredith & Jaydeep K. Srimani & Connor Pfeiffer & Rick Durrett & Lingchong You, 2017. "Persistence and reversal of plasmid-mediated antibiotic resistance," Nature Communications, Nature, vol. 8(1), pages 1-10, December.
    5. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
    6. Tomohiro Miyoshi & Kosuke Ito & Ryo Murakami & Toshio Uchiumi, 2016. "Structural basis for the recognition of guide RNA and target DNA heteroduplex by Argonaute," Nature Communications, Nature, vol. 7(1), pages 1-12, September.
    7. Xinmi Song & Sheng Lei & Shunhang Liu & Yanqiu Liu & Pan Fu & Zhifeng Zeng & Ke Yang & Yu Chen & Ming Li & Qunxin She & Wenyuan Han, 2023. "Catalytically inactive long prokaryotic Argonaute systems employ distinct effectors to confer immunity via abortive infection," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
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    1. Laura Toribio-Celestino & Alicia Calvo-Villamañán & Cristina Herencias & Aida Alonso-del Valle & Jorge Sastre-Dominguez & Susana Quesada & Didier Mazel & Eduardo P. C. Rocha & Ariadna Fernández-Calvet, 2024. "A plasmid-chromosome crosstalk in multidrug resistant enterobacteria," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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