TY - JOUR
T1 - IS26-mediated plasmid reshuffling results in convergence of toxin–antitoxin systems but loss of resistance genes in XDR Klebsiella pneumoniae from a chronic infection
AU - Luo, Ting L.
AU - Corey, Brendan W.
AU - Snesrud, Erik
AU - Iovleva, Alina
AU - McElheny, Christi L.
AU - Preston, Lan N.
AU - Kwak, Yoon I.
AU - Bennett, Jason W.
AU - Doi, Yohei
AU - McGann, Patrick T.
AU - Lebreton, Francois
N1 - Publisher Copyright:
© 2022 The Authors.
PY - 2022
Y1 - 2022
N2 - Carbapenem-resistant Enterobacterales pose an urgent threat to human health worldwide. Klebsiella pneumoniae sequence type (ST) 14, initially identified in the Middle East and South-Asia and co-harbouring the carbapenemase genes blaOXA-232 and blaNDM-1, is now emerging globally. One such strain was detected in the USA in 2013 from a patient initially treated in India that also carried armA, a 16S rRNA methyltransferase that confers resistance to all clinically relevant aminoglyco-sides. Genetic and phenotypic changes were observed in 14 serial isolates collected from this chronically infected patient. The index isolate carried five plasmids, including an IncFIB–IncHI1B (harbouring armA and blaNDM-1 ), an IncFIA (blaCTX-M-15 ) and a ColE-like (blaOXA-232 ), and was extensively resistant to antibiotics. Four years later, a subsequent isolate had accumu-lated 34 variants, including a loss-of-function mutation in romA, resulting in tigecycline non-susceptibility. Importantly, this isolate now only carried two plasmids, including a large mosaic molecule made of fragments, all harbouring distinct toxin–antitoxin systems, from three of the canonical plasmids. Of the original acquired antibiotic resistance genes, this isolate only retained blaCTX-M-15, and as a result susceptibility to the carbapenems and amikacin was restored. Long-read sequencing of a subset of five representative isolates, collected between 2013 and 2017, allowed for the elucidation of the complex plasmid patterns and revealed the role of IS26-mediated plasmid reshuffling in the evolution of this clone. Such investigations of the mechanisms underlying plasmid stability, together with global and local surveillance programmes, are key to a better understanding of plasmid host range and dissemination.
AB - Carbapenem-resistant Enterobacterales pose an urgent threat to human health worldwide. Klebsiella pneumoniae sequence type (ST) 14, initially identified in the Middle East and South-Asia and co-harbouring the carbapenemase genes blaOXA-232 and blaNDM-1, is now emerging globally. One such strain was detected in the USA in 2013 from a patient initially treated in India that also carried armA, a 16S rRNA methyltransferase that confers resistance to all clinically relevant aminoglyco-sides. Genetic and phenotypic changes were observed in 14 serial isolates collected from this chronically infected patient. The index isolate carried five plasmids, including an IncFIB–IncHI1B (harbouring armA and blaNDM-1 ), an IncFIA (blaCTX-M-15 ) and a ColE-like (blaOXA-232 ), and was extensively resistant to antibiotics. Four years later, a subsequent isolate had accumu-lated 34 variants, including a loss-of-function mutation in romA, resulting in tigecycline non-susceptibility. Importantly, this isolate now only carried two plasmids, including a large mosaic molecule made of fragments, all harbouring distinct toxin–antitoxin systems, from three of the canonical plasmids. Of the original acquired antibiotic resistance genes, this isolate only retained blaCTX-M-15, and as a result susceptibility to the carbapenems and amikacin was restored. Long-read sequencing of a subset of five representative isolates, collected between 2013 and 2017, allowed for the elucidation of the complex plasmid patterns and revealed the role of IS26-mediated plasmid reshuffling in the evolution of this clone. Such investigations of the mechanisms underlying plasmid stability, together with global and local surveillance programmes, are key to a better understanding of plasmid host range and dissemination.
KW - CRE
KW - NDM
KW - OXA-232
KW - ST14
KW - mosaic plasmids
KW - within-host evolution
UR - http://www.scopus.com/inward/record.url?scp=85139135234&partnerID=8YFLogxK
U2 - 10.1099/mgen.0.000892
DO - 10.1099/mgen.0.000892
M3 - Article
C2 - 36169644
AN - SCOPUS:85139135234
SN - 2057-5858
VL - 8
JO - Microbial Genomics
JF - Microbial Genomics
IS - 9
M1 - 000892
ER -