Exploiting a conjugative endogenous CRISPR-Cas3 system to tackle multidrug-resistant Klebsiella pneumoniae

EBioMedicine. 2023 Feb:88:104445. doi: 10.1016/j.ebiom.2023.104445. Epub 2023 Jan 23.

Abstract

Background: Mobile plasmids play a key role in spurring the global dissemination of multidrug-resistant (MDR) K. pneumoniae, while plasmid curing has been recognized as a promising strategy to combat antimicrobial resistance. Here we exploited a K. pneumoniae native CRISPR system to cure the high-risk IncFII plasmids.

Methods: We examined matched protospacers in 725 completely sequenced IncFII plasmids from K. pneumoniae genomes. Then, we re-engineered a native CRISPR-Cas3 system and deliver the CRISPR-Cas3 system via conjugation. Plasmid killing efficiency and G. mellonella infection model were applied to evaluate the CRISPR-Cas3 immunity in vitro and in vivo.

Findings: Genomic analysis revealed that most IncFII plasmids could be targeted by the native CRISPR-Cas3 system with multiple matched protospacers, and the targeting regions were highly conserved across different IncFII plasmids. This conjugative endogenous CRISPR-Cas3 system demonstrated high plasmid curing efficiency in vitro (8-log decrease) and in vivo (∼100% curing) in a Galleria mellonella infection model, as well as provided immunization against the invasion of IncFII plasmids once the system entering a susceptible bacterial host.

Interpretation: Overall, our work demonstrated the applicability of using native CRISPR-mediated plasmid curing to re-sensitize drug-resistant K. pneumoniae to multiple antibiotics. This work provided strong support for the idea of utilizing native CRISPR-Cas systems to tackle AMR in K. pneumoniae.

Funding: This work was supported by research grants National Natural Science Foundation of China [grant numbers 81871692, 82172315, 82102439, and 82202564], the Shanghai Science and Technology Commission [grant number 19JC1413002], and Shanghai Sailing Program [grant number 22YF1437500].

Keywords: Antimicrobial resistance; CRISPR-Cas system; IncFII plasmid; K. pneumoniae.

MeSH terms

  • Anti-Bacterial Agents
  • Bacterial Proteins* / genetics
  • Bacterial Proteins* / metabolism
  • CRISPR-Cas Systems
  • China
  • Humans
  • Klebsiella pneumoniae* / genetics
  • Plasmids / genetics
  • beta-Lactamases / genetics

Substances

  • Bacterial Proteins
  • Anti-Bacterial Agents
  • beta-Lactamases