Experimental evidence for IS1294b-mediated transposition of the blaCMY-2 cephalosporinase gene in Enterobacteriaceae

Yassine, Haytham; Bientz, Léa; Cros, Jérôme; Goret, Julien; Bebear, Cécile; Quentin, Claudine; Arpin, Corinne

doi:10.1093/jac/dku472

Cited by 20 publications

(20 citation statements)

References 20 publications

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“…Identification of different genetic environments of bla CMY-2 among IncI1-I␥/ST2, IncI1-I␥/ST12, and IncK plasmids suggested that at least IncI1-I␥/ST2 and IncI1-I␥/ST12 plasmids acquired the resistance gene independently, while the possibility that IncK plasmids acquired the ISEcp1-sugE structure from I1-I␥/ST12 plasmids or vice versa cannot be excluded. The genetic context of bla CMY-2 in IncI1-I␥/ST2 plasmids was nearly identical to previous descriptions (38)(39)(40), except for three gaps and four SNPs that were either synonymous or in intergenic regions. The genetic context of bla CMY-2 in IncI1-I␥/ST12 was highly similar to that of pNF1358 (GenBank accession no.…”

Section: Discussionsupporting

confidence: 76%

Host-Specific Patterns of Genetic Diversity among IncI1-Iγ and IncK Plasmids Encoding CMY-2 β-Lactamase in Escherichia coli Isolates from Humans, Poultry Meat, Poultry, and Dogs in Denmark

Hansen

Bortolaia

Nielsen

et al. 2016

Appl Environ Microbiol

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CMY-2 is the most common plasmid-mediated AmpC ␤-lactamase in Escherichia coli isolates of human and animal origin. The aim of this study was to elucidate the epidemiology of CMY-2-producing E. coli in Denmark. Strain and plasmid relatedness was studied in 93 CMY-2-producing clinical and commensal E. coli isolates collected from 2006 to 2012 from humans, retail poultry meat, broilers, and dogs. Multilocus sequence typing (MLST), antimicrobial susceptibility testing, and conjugation were performed in conjunction with plasmid replicon typing, plasmid multilocus sequence typing (pMLST), restriction fragment length polymorphism (RFLP), and sequencing of selected bla CMY-2 -harboring plasmids. MLST revealed high strain diversity, with few E. coli lineages occurring in multiple host species and sample types. bla CMY-2 was detected on plasmids in 83 (89%) isolates. Most (75%) of the plasmids were conjugative and did not (96%) cotransfer resistance to antimicrobials other than cephalosporins. The main replicon types identified were IncI1-I␥ (55%) and IncK (39%). Isolates from different host species mainly carried distinct plasmid subtypes. Seven of the 18 human isolates harbored IncI1-I␥/sequence type 2 (ST2), IncI1-I␥/ST12, or IncK plasmids highly similar to those found among animal isolates, even though highly related human and animal plasmids differed by nonsynonymous single nucleotide polymorphisms (SNPs) or insertion sequence elements. This study clearly demonstrates that the epidemiology of CMY-2 can be understood only by thorough plasmid characterization. To date, the spread of this ␤-lactam resistance determinant in Denmark is mainly associated with IncK and IncI1-I␥ plasmids that are generally distributed according to host-specific patterns. These baseline data will be useful to assess the consequences of the increasing human exposure to CMY-2-producing E. coli via animal sources. IMPORTANCECMY-2 is the most common plasmid-mediated AmpC ␤-lactamase in Escherichia coli. This ␤-lactamase is poorly inhibited by clavulanic acid and confers resistance to cephamycins, third-generation cephalosporins, and aztreonam. Furthermore, resistance to carbapenems has been reported in E. coli as a result of production of plasmid-encoded CMY-2 ␤-lactamase in combination with decreased outer membrane permeability. The gene encoding CMY-2 generally resides on transferable plasmids belonging to different incompatibility groups. The prevalence of CMY-2-mediated cephalosporin resistance in E. coli varies significantly depending on the geographical region and host. This study demonstrates that the epidemiology of CMY-2 can be understood only by thorough plasmid characterization. To date, the spread of this ␤-lactam resistance determinant in Denmark is mainly associated with IncK and IncI1-I␥ plasmids, which are generally distributed according to host-specific patterns. These data will be useful to assess the consequences of the increasing human exposure to CMY-2-producing E. coli via animal sources. C MY-2 is the most common p...

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Section: Discussionsupporting

confidence: 76%

Host-Specific Patterns of Genetic Diversity among IncI1-Iγ and IncK Plasmids Encoding CMY-2 β-Lactamase in Escherichia coli Isolates from Humans, Poultry Meat, Poultry, and Dogs in Denmark

Hansen

Bortolaia

Nielsen

et al. 2016

Appl Environ Microbiol

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“…A similar genetic context surrounding the bla CMY -2 gene was identified in an IncI1 plasmid p2735 (KP017243; Yassine et al, 2014 ) isolated from Klebsiella pneumoniae as well as six IncI1 plasmids isolated from E. coli including two completely sequenced plasmids pJIE512b (HG970648; Tagg et al, 2014 ), and pR7AC (KF434766; Minoia et al, 2012 ), and four partially sequenced plasmids pTN38148 (FM246883), pTN10, pTN13, and pTN386 ( Verdet et al, 2009 ) ( Figure 4 ). Compared to pS10584, the bla CMY -2 insertion was within the yagA gene 16-bp from the 5′ end, removing the rest of the yagA gene, as well as a large part of the cia gene, leaving the same part of the cia gene in the 3′ end followed by the same 159-bp IncA/C backbone ending in GTTC in pJIE512b.…”

Section: Resultsmentioning

confidence: 67%

IncHI2 Plasmids Are Predominant in Antibiotic-Resistant Salmonella Isolates

et al. 2016

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The wide usage of antibiotics contributes to the increase in the prevalence of antibiotic-resistant Salmonella. Plasmids play a critical role in horizontal transfer of antibiotic resistance markers in Salmonella. This study aimed to screen and characterize plasmid profiles responsible for antibiotic resistance in Salmonella and ultimately to clarify the molecular mechanism of transferable plasmid-mediated antibiotic resistance. A total of 226 Salmonella isolates were examined for antimicrobial susceptibility by a disk diffusion method. Thirty-two isolates (14.2%) were resistant to at least one antibiotic. The presence of plasmid-mediated quinolone resistance (PMQR) genes and β-lactamase genes were established by PCR amplification. PCR-based replicon typing revealed that these 32 isolates represented seven plasmid incompatibility groups (IncP, HI2, A/C, FIIs, FIA, FIB, and I1), and the IncHI2 (59.4%) was predominant. Antibiotic resistance markers located on plasmids were identified through plasmid curing. Fifteen phenotypic variants were obtained with the curing efficiency of 46.9% (15/32). The cured plasmids mainly belong to the HI2 incompatibility group. The elimination of IncHI2 plasmids correlated with the loss of β-lactamase genes (blaOXA-1 and blaTEM-1) and PMQR genes (qnrA and aac(6′)-Ib-cr). Both IncHI2 and IncI1 plasmids in a S. enterica serovar Indiana isolate SJTUF 10584 were lost by curing. The blaCMY -2-carrying plasmid pS10584 from SJTUF 10584 was fully sequenced. Sequence analysis revealed that it possessed a plasmid scaffold typical for IncI1 plasmids with the unique genetic arrangement of IS1294-ΔISEcp1-blaCMY -2-blc-sugE-ΔecnR inserted into the colicin gene cia. These data suggested that IncHI2 was the major plasmid lineage contributing to the dissemination of antibiotic resistance in Salmonella and the activity of multiple mobile genetic elements may contribute to antibiotic resistance evolution and dissemination between different plasmid replicons.

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“…IS91 and IS801 do not seem to have been involved in movement of known resistance genes, but IS1294 ( Fig. 2F) and the variant IS1294b have transferred bla CMY-2 -like genes originally associated with ISEcp1 between different plasmid types (55,56).…”

Section: Is91-like and Iscr Elementsmentioning

confidence: 99%

Mobile Genetic Elements Associated with Antimicrobial Resistance

et al. 2018

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SUMMARYStrains of bacteria resistant to antibiotics, particularly those that are multiresistant, are an increasing major health care problem around the world. It is now abundantly clear that both Gram-negative and Gram-positive bacteria are able to meet the evolutionary challenge of combating antimicrobial chemotherapy, often by acquiring preexisting resistance determinants from the bacterial gene pool. This is achieved through the concerted activities of mobile genetic elements able to move within or between DNA molecules, which include insertion sequences, transposons, and gene cassettes/integrons, and those that are able to transfer between bacterial cells, such as plasmids and integrative conjugative elements. Together these elements play a central role in facilitating horizontal genetic exchange and therefore promote the acquisition and spread of resistance genes. This review aims to outline the characteristics of the major types of mobile genetic elements involved in acquisition and spread of antibiotic resistance in both Gram-negative and Gram-positive bacteria, focusing on the so-called ESKAPEE group of organisms (, ,, ,, spp., and), which have become the most problematic hospital pathogens.

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Experimental evidence for IS1294b-mediated transposition of the blaCMY-2 cephalosporinase gene in Enterobacteriaceae

Abstract: Our experimental data demonstrate for the first time, to our knowledge, the mobilization of a β-lactamase gene mediated by a member of the IS91 family and highlight the important role of this mobile genetic element in the spread of antibiotic resistance genes.

Cited by 20 publications

References 20 publications

Host-Specific Patterns of Genetic Diversity among IncI1-Iγ and IncK Plasmids Encoding CMY-2 β-Lactamase in Escherichia coli Isolates from Humans, Poultry Meat, Poultry, and Dogs in Denmark

Host-Specific Patterns of Genetic Diversity among IncI1-Iγ and IncK Plasmids Encoding CMY-2 β-Lactamase in Escherichia coli Isolates from Humans, Poultry Meat, Poultry, and Dogs in Denmark

IncHI2 Plasmids Are Predominant in Antibiotic-Resistant Salmonella Isolates

Mobile Genetic Elements Associated with Antimicrobial Resistance

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