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Evolution of triclosan resistance modulates bacterial permissiveness to multidrug resistance plasmids and phages

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Listed:
  • Qiu E. Yang

    (Fujian Agriculture and Forestry University)

  • Xiaodan Ma

    (Fujian Agriculture and Forestry University)

  • Minchun Li

    (Fujian Agriculture and Forestry University)

  • Mengshi Zhao

    (Fujian Agriculture and Forestry University)

  • Lingshuang Zeng

    (Fujian Agriculture and Forestry University)

  • Minzhen He

    (Fujian Agriculture and Forestry University)

  • Hui Deng

    (Fujian Agriculture and Forestry University)

  • Hanpeng Liao

    (Fujian Agriculture and Forestry University)

  • Christopher Rensing

    (Fujian Agriculture and Forestry University)

  • Ville-Petri Friman

    (University of Helsinki)

  • Shungui Zhou

    (Fujian Agriculture and Forestry University)

  • Timothy R. Walsh

    (University of Oxford)

Abstract

The horizontal transfer of plasmids has been recognized as one of the key drivers for the worldwide spread of antimicrobial resistance (AMR) across bacterial pathogens. However, knowledge remain limited about the contribution made by environmental stress on the evolution of bacterial AMR by modulating horizontal acquisition of AMR plasmids and other mobile genetic elements. Here we combined experimental evolution, whole genome sequencing, reverse genetic engineering, and transcriptomics to examine if the evolution of chromosomal AMR to triclosan (TCS) disinfectant has correlated effects on modulating bacterial pathogen (Klebsiella pneumoniae) permissiveness to AMR plasmids and phage susceptibility. Herein, we show that TCS exposure increases the evolvability of K. pneumoniae to evolve TCS-resistant mutants (TRMs) by acquiring mutations and altered expression of several genes previously associated with TCS and antibiotic resistance. Notably, nsrR deletion increases conjugation permissiveness of K. pneumoniae to four AMR plasmids, and enhances susceptibility to various Klebsiella-specific phages through the downregulation of several bacterial defense systems and changes in membrane potential with altered reactive oxygen species response. Our findings suggest that unrestricted use of TCS disinfectant imposes a dual impact on bacterial antibiotic resistance by augmenting both chromosomally and horizontally acquired AMR mechanisms.

Suggested Citation

  • Qiu E. Yang & Xiaodan Ma & Minchun Li & Mengshi Zhao & Lingshuang Zeng & Minzhen He & Hui Deng & Hanpeng Liao & Christopher Rensing & Ville-Petri Friman & Shungui Zhou & Timothy R. Walsh, 2024. "Evolution of triclosan resistance modulates bacterial permissiveness to multidrug resistance plasmids and phages," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48006-9
    DOI: 10.1038/s41467-024-48006-9
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    1. Jianan Zhang & Morgan E. Walker & Katherine Z. Sanidad & Hongna Zhang & Yanshan Liang & Ermin Zhao & Katherine Chacon-Vargas & Vladimir Yeliseyev & Julie Parsonnet & Thomas D. Haggerty & Guangqiang Wa, 2022. "Microbial enzymes induce colitis by reactivating triclosan in the mouse gastrointestinal tract," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Pauline C. Göller & Tabea Elsener & Dominic Lorgé & Natasa Radulovic & Viona Bernardi & Annika Naumann & Nesrine Amri & Ekaterina Khatchatourova & Felipe Hernandes Coutinho & Martin J. Loessner & Elen, 2021. "Multi-species host range of staphylococcal phages isolated from wastewater," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    3. Laura M. McMurry & Margret Oethinger & Stuart B. Levy, 1998. "Triclosan targets lipid synthesis," Nature, Nature, vol. 394(6693), pages 531-532, August.
    4. Tanita Wein & Nils F. Hülter & Itzhak Mizrahi & Tal Dagan, 2019. "Emergence of plasmid stability under non-selective conditions maintains antibiotic resistance," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    5. Samuel C. Forster & Junyan Liu & Nitin Kumar & Emily L. Gulliver & Jodee A. Gould & Alejandra Escobar-Zepeda & Tapoka Mkandawire & Lindsay J. Pike & Yan Shao & Mark D. Stares & Hilary P. Browne & B. A, 2022. "Strain-level characterization of broad host range mobile genetic elements transferring antibiotic resistance from the human microbiome," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
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