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

Qiu E. Yang, Xiaodan Ma, Minchun Li, Mengshi Zhao, Lingshuang Zeng, Minzhen He, Hui Deng, Hanpeng Liao, Christopher Rensing, Ville-Petri Friman, Shungui Zhou () and Timothy R. Walsh ()
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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

Nature Communications, 2024, vol. 15, issue 1, 1-13

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-48006-9

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