Genomic dissection of endemic carbapenem resistance reveals metallo-beta-lactamase dissemination through clonal, plasmid and integron transfer

Nenad Macesic, Jane Hawkey, Ben Vezina, Jessica A. Wisniewski, Hugh Cottingham, Luke V. Blakeway, Taylor Harshegyi, Katherine Pragastis, Gnei Zweena Badoordeen, Amanda Dennison, Denis W. Spelman, Adam W. J. Jenney and Anton Y. Peleg ()
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Nenad Macesic: Monash University
Jane Hawkey: Monash University
Ben Vezina: Monash University
Jessica A. Wisniewski: Monash University
Hugh Cottingham: Monash University
Luke V. Blakeway: Monash University
Taylor Harshegyi: Monash University
Katherine Pragastis: Monash University
Gnei Zweena Badoordeen: Monash University
Amanda Dennison: Microbiology Unit, Alfred Hospital
Denis W. Spelman: Monash University
Adam W. J. Jenney: Monash University
Anton Y. Peleg: Monash University

Nature Communications, 2023, vol. 14, issue 1, 1-12

Abstract: Abstract Infections caused by metallo-beta-lactamase-producing organisms (MBLs) are a global health threat. Our understanding of transmission dynamics and how MBLs establish endemicity remains limited. We analysed two decades of blaIMP-4 evolution in a hospital using sequence data from 270 clinical and environmental isolates (including 169 completed genomes) and identified the blaIMP-4 gene across 7 Gram-negative genera, 68 bacterial strains and 7 distinct plasmid types. We showed how an initial multi-species outbreak of conserved IncC plasmids (95 genomes across 37 strains) allowed endemicity to be established through the ability of blaIMP-4 to disseminate in successful strain-genetic setting pairs we termed propagators, in particular Serratia marcescens and Enterobacter hormaechei. From this reservoir, blaIMP-4 persisted through diversification of genetic settings that resulted from transfer of blaIMP-4 plasmids between bacterial hosts and of the integron carrying blaIMP-4 between plasmids. Our findings provide a framework for understanding endemicity and spread of MBLs and may have broader applicability to other carbapenemase-producing organisms.

Date: 2023
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DOI: 10.1038/s41467-023-39915-2

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