Antimicrobial resistance is a critical issue that is no longer restricted to hospital settings, but also represents a growing problem involving intensive animal production systems. In this study, we have performed a microbiological and molecular investigation of priority pathogens carrying transferable resistance genes to critical antimicrobials in one-day-old chickens imported from Brazil to Uruguay. Bacterial identification was performed by MALDI-TOF mass spectrometry and antibiotic susceptibility was determined by Sensititre. Antimicrobial resistance genes were sought by polymerase chain reaction and clonality was assessed by PFGE. Four multidrug-resistant (MDR) representative strains were sequenced by Illumina and/or Oxford Nanopore Technologies. Twenty-eight MDR isolates identified as
Escherichia coli
(
n
= 14),
Enterobacter cloacae
(
n
= 11) and
Klebsiella pneumoniae
(
n
= 3). While resistance to oxyiminocephalosporins was due to
bla
CTX-M-2
,
bla
CTX-M-8
,
bla
CTX-M-15
,
bla
CTX-M-55
and
bla
CMY-2
, plasmid-mediated quinolone resistance was associated with
qnrB19
,
qnrE1
, and
qnrB2
genes. Finally, resistance to aminoglycosides and fosfomycin was due to the presence of 16S rRNA methyltransferase
rmtG
and
fosA
-type genes, respectively. Short and long-read genome sequencing of
E. cloacae
ODC-Eclo3 strain revealed the presence of IncQ/
rmtG
(pUR-EC3.1, 7400-pb), IncHI2A/
mcr-9.1
/
bla
CTX-M-2
[pUR-EC3.2, ST16 (pMLST), 408,436-bp] and IncN2/
qnrB19
/
aacC3
/
aph(3’’)-Ib
(pUR-EC3.3) resistance plasmids. Strikingly, the
bla
CTX-M-2
gene was carried by a novel Tn
1696
-like composite transposon designated Tn
7337
. In summary, we report that imported one-day-old chicks can act as Trojan horses for the hidden spread of WHO critical priority MDR pathogens harboring
mcr-9
,
rmtG
and extended-spectrum β-lactamase genes in poultry farms, which is a critical issue within a One Health perspective.
Importance section
Antimicrobial resistance is considered a significant problem for global health, including within the concept of "One Health", therefore, the food chain is a link that connects human and animal health directly. In this work, we searched for microorganisms resistant to antibiotics considered critical for human health in intestinal microbiota of one-day-old baby chicks imported to Uruguay from Brazil. We described antibiotic-resistant genes to antibiotics named as to watch or reserve for the WHO, such as
rmtG
or
mcr9.1
, which confers resistance to all the aminoglycosides and colistin, respectively, among others genes, and their presence in new mobile genetic elements that favor its dissemination.
The sustained entry of these microorganisms evades the sanitary measures implemented by the countries and production establishments to reduce the selection of resistant microorganisms. These silently imported resistant microorganisms could explain a considerable part of the antimicrobial resistance problems found in the production stages of the system.