Unravelling bla_IMP carbapenemase gene genetic context in dairy cattle and environmental metagenomes

INTRODUCTION: Carbapenemase-producing organisms (CPOs) pose a major global health threat. According to EARS-Net, Greece has one of Europe’s highest CPO-incidences in healthcare-associated infections, endemic for KPC, NDM, VIM, and OXA-48-like-carrying CPOs, but not for IMP. This study was conducted on metagenomes recovered from intensive dairy farms in Greece and harbored bla_IMP-determinants to explore their genetic context and dynamics underlying bla_IMP-dissemination, adopting a One Health-related approach.

METHODS: Short reads and contigs were comparatively analyzed using BLASTn, MEGA, and Easyfig software; assembled with MEGAHIT; and mapped to references (MZ816709.1, AJ550807.1) using Burrows-Wheeler-Aligner and SAMtools.

RESULTS: Analyses revealed that bla_IMP-associated reads were identical or highly similar to bla_IMP-13. Numerous reads and contigs covered the entire length of a Tn402-like transposon, including transposase (tnpA/R/M, tniA/B) and mercury-resistance (merRTPCADE) genes and a class-1 integron harboring bla_IMP-13 variant, aac(6′), aadA1, qacEdelta1, and sul1, but lacking qacG2 genes.

DISCUSSION/CONCLUSIONS: Tn402-like transposons as carriers of class-1 integrons harboring bla_IMP-13 variants have mainly been restricted to isolates from human clinical settings, promoted by the intensive use of carbapenems in these environments. Since carbapenems are banned from use in food-producing animals, it is surprising to note this highly mobile genetic element to be recovered from dairy cattle feces and environments. This suggests that any associated horizontal transfer could introduce bla_IMP-13 variants into novel hosts, with the human–agricultural interface being a critical hotspot for spillovers. Given that bla_IMP has not yet been reported in human clinical settings in Greece, moving personnel from areas with high bla_IMP-13-carrying CPO incidence could be a potential source, creating secondary reservoirs and forming a cycle that changes traditional epidemiological boundaries. This is highly concerning, as widely used veterinary antibiotics could provide co-selection pressure, favoring the spread of bla_IMP-13-variant-carrying CPOs. Our findings highlight the need for proactive metagenomic surveillance and strengthened monitoring strategies.