A total of 18 Enterobacteriaceae (17 from gulls and 1 from a clinical sample) collected from Australia, carrying IncA/C plasmids with the IMP-encoding In809-like integrons, were studied. Seven plasmids, being representatives of different origins, plasmid sizes, replicon combinations, and resistance genes, were completely sequenced. Plasmid pEc158, identified in a clinical Escherichia coli ST752 isolate, showed extensive similarity to type 2 IncA/C2 plasmids. pEc158 carried none of the blaCMY-2-like region or ARI-B and ARI-A regions, while it contained a hybrid transposon structure. The six remaining plasmids, which were of wildlife origin, were highly similar to each other and probably were fusion derivatives of type 1 and type 2 A/C2 plasmids. The latter plasmids contained an ARI-B region and hybrid transposon structures. In all plasmids, hybrid transposon structures containing In809-like integrons were inserted 3,434 bp downstream of the rhs2 start codon. In all cases, the one outermost 38-bp inverted repeat (IR) of the transposon was associated with the Tn1696 tnp module, while the other outermost 38-bp IR of the transposon was associated with either a Tn6317-like module or a Tn21 mer module. However, the internal structure of the transposon and the resistance genes were different in each plasmid. These findings indicated that, for the specific periods of time and settings, different IncA/C2 plasmid types carrying In809-like elements circulated among isolates of wildlife and clinical origins. Additionally, they provided the basis for speculations regarding the reshuffling of IncA/C2 plasmids with In809-like integrons and confirmed the rapid evolution of IncA/C2 plasmid lineages.

Biomedical Center Faculty of Medicine Charles University Plzen Czech Republic

CEITEC VFU University of Veterinary and Pharmaceutical Sciences Brno Brno Czech Republic

Department of Biology and Wildlife Diseases Faculty of Veterinary Hygiene and Ecology University of Veterinary and Pharmaceutical Sciences Brno Brno Czech Republic

Department of Microbiology Faculty of Medicine and University Hospital in Plzen Charles University Plzen Czech Republic

Veterinary Research Institute Brno Czech Republic

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Carattoli A, Miriagou V, Bertini A, Loli A, Colinon C, Villa L, Whichard JM, Rossolini GM. 2006. Replicon typing of plasmids encoding resistance to newer beta-lactams. Emerg Infect Dis 12:1145–1148. doi:10.3201/eid1207.051555. PubMed DOI PMC

Harmer CJ, Hall RM. 2015. The A to Z of A/C plasmids. Plasmid 80:63–82. doi:10.1016/j.plasmid.2015.04.003. PubMed DOI

Espedido BA, Partridge SR, Iredell JR. 2008. blaIMP-4 in different genetic contexts in Enterobacteriaceae isolates from Australia. Antimicrob Agents Chemother 52:2984–2987. doi:10.1128/AAC.01634-07. PubMed DOI PMC

Peirano G, Lascols C, Hackel M, Hoban DJ, Pitout JD. 2014. Molecular epidemiology of Enterobacteriaceae that produce VIMs and IMPs from the SMART surveillance program. Diagn Microbiol Infect Dis 78:277–281. doi:10.1016/j.diagmicrobio.2013.11.024. PubMed DOI

Papagiannitsis CC, Dolejska M, Izdebski R, Giakkoupi P, Skálová A, Chudějová K, Dobiasova H, Vatopoulos AC, Derde LP, Bonten MJ, Gniadkowski M, Hrabák J. 2016. Characterisation of IncA/C2 plasmids carrying an In416-like integron with the blaVIM-19 gene from Klebsiella pneumoniae ST383 of Greek origin. Int J Antimicrob Agents 47:158–162. doi:10.1016/j.ijantimicag.2015.12.001. PubMed DOI

Dolejska M, Masarikova M, Dobiasova H, Jamborova I, Karpiskova R, Havlicek M, Carlile N, Priddel D, Cizek A, Literak I. 2016. High prevalence of Salmonella and IMP-4-producing Enterobacteriaceae in the silver gull on Five Islands, Australia. J Antimicrob Chemother 71:63–70. doi:10.1093/jac/dkv306. PubMed DOI PMC

Ho PL, Lo WU, Chan J, Cheung YY, Chow KH, Yam WC, Lin CH, Que TL. 2014. pIMP-PH114 carrying blaIMP-4 in a Klebsiella pneumoniae strain is closely related to other multidrug-resistant IncA/C2 plasmids. Curr Microbiol 68:227–232. doi:10.1007/s00284-013-0471-x. PubMed DOI

Hancock SJ, Phan MD, Peters KM, Forde BM, Chong TM, Yin WF, Chan KG, Paterson DL, Walsh TR, Beatson SA, Schembri MA. 2017. Identification of IncA/C plasmid replication and maintenance genes and development of a plasmid multilocus sequence typing scheme. Antimicrob Agents Chemother 61:e01740–e01816. PubMed PMC

Fricke WF, Welch EJ, McDermott PF, Mammel MK, LeClerc JE, White DG, Cebula TA, Ravel J. 2009. Comparative genomics of the IncA/C multidrug resistance plasmid family. J Bacteriol 191:4750–4757. doi:10.1128/JB.00189-09. PubMed DOI PMC

Welch TJ, Fricke WF, McDermott PF, White DG, Rosso ML, Rasko DA, Mammel MK, Eppinger M, Rosovitz MJ, Wagner D, Rahalison L, Leclerc JE, Hinshaw JM, Lindler LE, Cebula TA, Carniel E, Ravel J. 2007. Multiple antimicrobial resistance in plague: an emerging public health risk. PLoS One 2:e309. doi:10.1371/journal.pone.0000309. PubMed DOI PMC

Harmer CJ, Hall RM. 2014. pRMH760, a precursor of A/C2 plasmids carrying blaCMY and blaNDM genes. Microb Drug Resist 20:416–423. doi:10.1089/mdr.2014.0012. PubMed DOI

Miriagou V, Papagiannitsis CC, Kotsakis SD, Loli A, Tzelepi E, Legakis NJ, Tzouvelekis LS. 2010. Sequence of pNL194, a 79.3-kilobase IncN plasmid carrying the blaVIM-1 metallo-β-lactamase gene in Klebsiella pneumoniae. Antimicrob Agents Chemother 54:4497–4502. doi:10.1128/AAC.00665-10. PubMed DOI PMC

Williams LE, Detter C, Barry K, Lapidus A, Summers AO. 2006. Facile recovery of individual high-molecular-weight, low-copy-number natural plasmids for genomic sequencing. Appl Environ Microbiol 72:4899–4906. doi:10.1128/AEM.00354-06. PubMed DOI PMC

Gołebiewski M, Kern-Zdanowicz I, Zienkiewicz M, Adamczyk M, Zylinska J, Baraniak A, Gniadkowski M, Bardowski J, Cegłowski P. 2007. Complete nucleotide sequence of the pCTX-M3 plasmid and its involvement in spread of the extended-spectrum beta-lactamase gene blaCTX-M-3. Antimicrob Agents Chemother 51:3789–3795. doi:10.1128/AAC.00457-07. PubMed DOI PMC

Partridge SR, Hall RM. 2003. The IS1111 family members IS4321 and IS5075 have subterminal inverted repeats of Tn21 family transposons. J Bacteriol 185:6371–6384. doi:10.1128/JB.185.21.6371-6384.2003. PubMed DOI PMC

Wang M, Tran JH, Jacoby GA, Zhang Y, Wang F, Hooper DC. 2003. Plasmid-mediated quinolone resistance in clinical isolates of Escherichia coli from Shanghai, China. Antimicrob Agents Chemother 47:2242–2248. doi:10.1128/AAC.47.7.2242-2248.2003. PubMed DOI PMC

Sun F, Zhou D, Sun Q, Luo W, Tong Y, Zhang D, Wang Q, Feng W, Chen W, Fan Y, Xia P. 2016. Genetic characterization of two fully sequenced multi-drug resistant plasmids pP10164-2 and pP10164-3 from Leclercia adecarboxylata. Sci Rep 6:33982. doi:10.1038/srep33982. PubMed DOI PMC

Liebert CA, Hall RM, Summers AO. 1999. Transposon Tn21, flagship of the floating genome. Microbiol Mol Biol Rev 63:507–522. PubMed PMC

Abraham S, O'Dea M, Trott DJ, Abraham RJ, Hughes D, Pang S, McKew G, Cheong EY, Merlino J, Saputra S, Malik R, Gottlieb T. 2016. Isolation and plasmid characterization of carbapenemase (IMP-4) producing Salmonella enterica Typhimurium from cats. Sci Rep 6:35527. doi:10.1038/srep35527. PubMed DOI PMC

Witzel K, Gwinn-Giglio M, Nadendla S, Shefchek K, Ruppel S. 2012. Genome sequence of Enterobacter radicincitans DSM16656(T), a plant growth-promoting endophyte. J Bacteriol 194:5469. doi:10.1128/JB.01193-12. PubMed DOI PMC

Moura A, Henriques I, Ribeiro R, Correia A. 2007. Prevalence and characterization of integrons from bacteria isolated from a slaughterhouse wastewater treatment plant. J Antimicrob Chemother 60:1243–1250. doi:10.1093/jac/dkm340. PubMed DOI

Wirth T, Falush D, Lan R, Colles F, Mensa P, Wieler LH, Karch H, Reeves PR, Maiden MC, Ochman H, Achtman M. 2006. Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 60:1136–1151. doi:10.1111/j.1365-2958.2006.05172.x. PubMed DOI PMC

Diancourt L, Passet V, Verhoef J, Grimont PA, Brisse S. 2005. Multilocus sequence typing of Klebsiella pneumoniae nosocomial isolates. J Clin Microbiol 43:4178–4182. doi:10.1128/JCM.43.8.4178-4182.2005. PubMed DOI PMC

Bai L, Xia S, Lan R, Liu L, Ye C, Wang Y, Jin D, Cui Z, Jing H, Xiong Y, Bai X, Sun H, Zhang J, Wang L, Xu J. 2012. Isolation and characterization of cytotoxic, aggregative Citrobacter freundii. PLoS One 7:e33054. doi:10.1371/journal.pone.0033054. PubMed DOI PMC

Papagiannitsis CC, Studentova V, Ruzicka F, Tejkalova R, Hrabak J. 2013. Molecular characterization of metallo-β-lactamase-producing Pseudomonas aeruginosa in a Czech hospital (2009-2011). J Med Microbiol 62:945–947. doi:10.1099/jmm.0.056119-0. PubMed DOI

Moura A, Soares M, Pereira C, Leitão N, Henriques I, Correia A. 2009. INTEGRALL: a database and search engine for integrons, integrases and gene cassettes. Bioinformatics 25:1096–1098. doi:10.1093/bioinformatics/btp105. PubMed DOI

Dobiasova H, Dolejska M. 2016. Prevalence and diversity of IncX plasmids carrying fluoroquinolone and β-lactam resistance genes in Escherichia coli originating from diverse sources and geographical areas. J Antimicrob Chemother 71:2118–2124. doi:10.1093/jac/dkw144. PubMed DOI

Barton BM, Harding GP, Zuccarelli AJ. 1995. A general method for detecting and sizing large plasmids. Anal Biochem 226:235–240. doi:10.1006/abio.1995.1220. PubMed DOI

Carattoli A, Bertini A, Villa L, Falbo V, Hopkins KL, Threlfall EJ. 2005. Identification of plasmids by PCR-based replicon typing. J Microbiol Methods 63:219–228. doi:10.1016/j.mimet.2005.03.018. PubMed DOI

Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. doi:10.1093/bioinformatics/btu170. PubMed DOI PMC

Li H. 2013. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv:1303.3997 [q-bio.GN].

Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. 2012. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comp Biol 19:455–477. doi:10.1089/cmb.2012.0021. PubMed DOI PMC

Darling AE, Mau B, Perna NT. 2010. progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5:e11147. doi:10.1371/journal.pone.0011147. PubMed DOI PMC

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