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A plasmid-chromosome crosstalk in multidrug resistant enterobacteria

Author

Listed:
  • Laura Toribio-Celestino

    (Centro Nacional de Biotecnología (CNB-CSIC))

  • Alicia Calvo-Villamañán

    (Centro Nacional de Biotecnología (CNB-CSIC))

  • Cristina Herencias

    (Hospital Universitario Ramón y Cajal and Instituto Ramón y Cajal de Investigación Sanitaria
    Instituto de Salud Carlos III)

  • Aida Alonso-del Valle

    (Centro Nacional de Biotecnología (CNB-CSIC))

  • Jorge Sastre-Dominguez

    (Centro Nacional de Biotecnología (CNB-CSIC))

  • Susana Quesada

    (Centro Nacional de Biotecnología (CNB-CSIC))

  • Didier Mazel

    (Bacterial Genome Plasticity)

  • Eduardo P. C. Rocha

    (Microbial Evolutionary Genomics)

  • Ariadna Fernández-Calvet

    (Centro Nacional de Biotecnología (CNB-CSIC))

  • Alvaro San Millan

    (Centro Nacional de Biotecnología (CNB-CSIC)
    Instituto de Salud Carlos III)

Abstract

Conjugative plasmids promote the dissemination and evolution of antimicrobial resistance in bacterial pathogens. However, plasmid acquisition can produce physiological alterations in the bacterial host, leading to potential fitness costs that determine the clinical success of bacteria-plasmid associations. In this study, we use a transcriptomic approach to characterize the interactions between a globally disseminated carbapenem resistance plasmid, pOXA-48, and a diverse collection of multidrug resistant (MDR) enterobacteria. Although pOXA-48 produces mostly strain-specific transcriptional alterations, it also leads to the common overexpression of a small chromosomal operon present in Klebsiella spp. and Citrobacter freundii strains. This operon includes two genes coding for a pirin and an isochorismatase family proteins (pfp and ifp), and shows evidence of horizontal mobilization across Proteobacteria species. Combining genetic engineering, transcriptomics, and CRISPRi gene silencing, we show that a pOXA-48-encoded LysR regulator is responsible for the plasmid-chromosome crosstalk. Crucially, the operon overexpression produces a fitness benefit in a pOXA-48-carrying MDR K. pneumoniae strain, suggesting that this crosstalk promotes the dissemination of carbapenem resistance in clinical settings.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-55169-y
    DOI: 10.1038/s41467-024-55169-y
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    References listed on IDEAS

    as
    1. Alvaro San Millan & Macarena Toll-Riera & Qin Qi & R. Craig MacLean, 2015. "Interactions between horizontally acquired genes create a fitness cost in Pseudomonas aeruginosa," Nature Communications, Nature, vol. 6(1), pages 1-8, November.
    2. 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.
    3. 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.
    4. Sophie S Abby & Bertrand Néron & Hervé Ménager & Marie Touchon & Eduardo P C Rocha, 2014. "MacSyFinder: A Program to Mine Genomes for Molecular Systems with an Application to CRISPR-Cas Systems," PLOS ONE, Public Library of Science, vol. 9(10), pages 1-9, October.
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