Intercellular Transfer of Chromosomal Antimicrobial Resistance Genes between Acinetobacter baumannii Strains Mediated
Jun-Ichi Wachino1, Wanchun Jin2, Kouji Kimura2
1Department of Bacteriology, Nagoya University Graduate School of Medicine, Nagoya, Aichi, Japan wachino@med.nagoya-u.ac.jp.
Abstract:
The spread of antimicrobial resistance genes (ARGs) among Gram-negative pathogens, including Acinetobacter baumannii, is primarily mediated by transferable plasmids; however, ARGs are frequently integrated into its chromosome. How ARG gets horizontally incorporated into the chromosome of A. baumannii, and whether it functions as a cause for further spread of ARG, remains unknown. Here, we demonstrated intercellular prophage-mediated transfer of chromosomal ARGs without direct cell-cell interaction in A. baumannii We prepared ARG-harboring extracellular DNA (eDNA) components from the culture supernatant of a multidrug-resistant (MDR) A. baumannii NU-60 strain and exposed an antimicrobial-susceptible (AS) A. baumannii ATCC 17978 strain to the eDNA components. The antimicrobial-resistant (AR) A. baumannii ATCC 17978 derivatives appeared to acquire various ARGs, originating from dispersed loci of the MDR A. baumannii chromosome, along with their surrounding regions, by homologous recombination, with the ARGs including armA (aminoglycoside resistance), blaTEM-1 (β-lactam resistance), tet(B) (tetracycline resistance), and gyrA-81L (nalidixic acid resistance) genes. Notably, the eDNAs conferring antimicrobial resistance were enveloped in specific capsid proteins consisting of phage particles, thereby protecting the eDNAs from detergent and DNase treatments. The phages containing ARGs were likely released into the extracellular space from MDR A. baumannii, thereby transducing ARGs into AS A. baumannii, resulting in the acquisition of AR properties by the recipient. We concluded that the generalized transduction, in which phages were capable of carrying random pieces of A. baumannii genomic DNAs, enabled efficacious intercellular transfer of chromosomal ARGs between A. baumannii strains without direct cell-cell interaction.
Insights
Antimicrobial resistance genes (ARGs) spread between Acinetobacter baumannii strains via phages carrying chromosomal DNA. This study shows phages transfer ARGs without direct cell contact, contributing to antimicrobial resistance.
Area of Science:
- Microbiology
- Genetics
- Molecular Biology
Background:
- Antimicrobial resistance genes (ARGs) spread via plasmids, but chromosomal integration in Gram-negative pathogens like Acinetobacter baumannii is significant.
- Mechanisms of horizontal ARG incorporation into bacterial chromosomes and their role in further dissemination remain largely unknown.
- Understanding ARG chromosomal transfer is crucial for combating multidrug-resistant (MDR) bacterial infections.
Purpose of the Study:
- To investigate the intercellular transfer of chromosomal ARGs in Acinetobacter baumannii.
- To determine if phages mediate the spread of chromosomal ARGs without direct cell-cell contact.
- To identify the specific ARGs and mechanisms involved in this chromosomal transfer process.
Main Methods:
- Preparation of ARG-harboring extracellular DNA (eDNA) from a multidrug-resistant (MDR) Acinetobacter baumannii strain.
- Exposure of an antimicrobial-susceptible (AS) Acinetobacter baumannii strain to the prepared eDNA components.
- Analysis of acquired ARGs and surrounding genomic regions in recipient strains using homologous recombination and identification of phage particles.
Main Results:
- Antimicrobial-susceptible Acinetobacter baumannii acquired chromosomal ARGs (e.g., armA, blaTEM-1, tet(B), gyrA-81L) from MDR strains.
- Acquired ARGs originated from dispersed chromosomal loci and were transferred with flanking regions via homologous recombination.
- Extracellular DNA conferring resistance was protected within phage particles, facilitating transduction of chromosomal ARGs.
Conclusions:
- Phage-mediated generalized transduction enables intercellular transfer of chromosomal ARGs between Acinetobacter baumannii strains.
- This process occurs without direct cell-cell interaction, highlighting a novel mechanism for ARG dissemination.
- The findings reveal a significant pathway for the spread of antimicrobial resistance in Acinetobacter baumannii.
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