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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Diversity and Global Distribution of IncL/M Plasmids Enabling Horizontal Dissemination of <italic>β</italic>-Lactam Resistance Genes among the Enterobacteriaceae</title><author><name sortKey="Adamczuk, Marcin" sort="Adamczuk, Marcin" uniqKey="Adamczuk M" first="Marcin" last="Adamczuk">Marcin Adamczuk</name><affiliation><nlm:aff id="I1">Department of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland</nlm:aff></affiliation></author><author><name sortKey="Zaleski, Piotr" sort="Zaleski, Piotr" uniqKey="Zaleski P" first="Piotr" last="Zaleski">Piotr Zaleski</name><affiliation><nlm:aff id="I2">Institute of Biotechnology and Antibiotics, Staroscinska 5, 02-516 Warsaw, Poland</nlm:aff></affiliation></author><author><name sortKey="Dziewit, Lukasz" sort="Dziewit, Lukasz" uniqKey="Dziewit L" first="Lukasz" last="Dziewit">Lukasz Dziewit</name><affiliation><nlm:aff id="I1">Department of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland</nlm:aff></affiliation></author><author><name sortKey="Wolinowska, Renata" sort="Wolinowska, Renata" uniqKey="Wolinowska R" first="Renata" last="Wolinowska">Renata Wolinowska</name><affiliation><nlm:aff id="I3">Department of Pharmaceutical Microbiology, Medical University of Warsaw, Oczki 3, 02-007 Warsaw, Poland</nlm:aff></affiliation></author><author><name sortKey="Nieckarz, Marta" sort="Nieckarz, Marta" uniqKey="Nieckarz M" first="Marta" last="Nieckarz">Marta Nieckarz</name><affiliation><nlm:aff id="I1">Department of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland</nlm:aff></affiliation></author><author><name sortKey="Wawrzyniak, Pawel" sort="Wawrzyniak, Pawel" uniqKey="Wawrzyniak P" first="Pawel" last="Wawrzyniak">Pawel Wawrzyniak</name><affiliation><nlm:aff id="I1">Department of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland</nlm:aff></affiliation><affiliation><nlm:aff id="I2">Institute of Biotechnology and Antibiotics, Staroscinska 5, 02-516 Warsaw, Poland</nlm:aff></affiliation></author><author><name sortKey="Kieryl, Piotr" sort="Kieryl, Piotr" uniqKey="Kieryl P" first="Piotr" last="Kieryl">Piotr Kieryl</name><affiliation><nlm:aff id="I2">Institute of Biotechnology and Antibiotics, Staroscinska 5, 02-516 Warsaw, Poland</nlm:aff></affiliation></author><author><name sortKey="Plucienniczak, Andrzej" sort="Plucienniczak, Andrzej" uniqKey="Plucienniczak A" first="Andrzej" last="Plucienniczak">Andrzej Plucienniczak</name><affiliation><nlm:aff id="I2">Institute of Biotechnology and Antibiotics, Staroscinska 5, 02-516 Warsaw, Poland</nlm:aff></affiliation></author><author><name sortKey="Bartosik, Dariusz" sort="Bartosik, Dariusz" uniqKey="Bartosik D" first="Dariusz" last="Bartosik">Dariusz Bartosik</name><affiliation><nlm:aff id="I1">Department of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26236726</idno><idno type="pmc">4510254</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4510254</idno><idno type="RBID">PMC:4510254</idno><idno type="doi">10.1155/2015/414681</idno><date when="2015">2015</date><idno type="wicri:Area/Pmc/Corpus">000010</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000010</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Diversity and Global Distribution of IncL/M Plasmids Enabling Horizontal Dissemination of <italic>β</italic>-Lactam Resistance Genes among the Enterobacteriaceae</title><author><name sortKey="Adamczuk, Marcin" sort="Adamczuk, Marcin" uniqKey="Adamczuk M" first="Marcin" last="Adamczuk">Marcin Adamczuk</name><affiliation><nlm:aff id="I1">Department of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland</nlm:aff></affiliation></author><author><name sortKey="Zaleski, Piotr" sort="Zaleski, Piotr" uniqKey="Zaleski P" first="Piotr" last="Zaleski">Piotr Zaleski</name><affiliation><nlm:aff id="I2">Institute of Biotechnology and Antibiotics, Staroscinska 5, 02-516 Warsaw, Poland</nlm:aff></affiliation></author><author><name sortKey="Dziewit, Lukasz" sort="Dziewit, Lukasz" uniqKey="Dziewit L" first="Lukasz" last="Dziewit">Lukasz Dziewit</name><affiliation><nlm:aff id="I1">Department of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland</nlm:aff></affiliation></author><author><name sortKey="Wolinowska, Renata" sort="Wolinowska, Renata" uniqKey="Wolinowska R" first="Renata" last="Wolinowska">Renata Wolinowska</name><affiliation><nlm:aff id="I3">Department of Pharmaceutical Microbiology, Medical University of Warsaw, Oczki 3, 02-007 Warsaw, Poland</nlm:aff></affiliation></author><author><name sortKey="Nieckarz, Marta" sort="Nieckarz, Marta" uniqKey="Nieckarz M" first="Marta" last="Nieckarz">Marta Nieckarz</name><affiliation><nlm:aff id="I1">Department of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland</nlm:aff></affiliation></author><author><name sortKey="Wawrzyniak, Pawel" sort="Wawrzyniak, Pawel" uniqKey="Wawrzyniak P" first="Pawel" last="Wawrzyniak">Pawel Wawrzyniak</name><affiliation><nlm:aff id="I1">Department of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland</nlm:aff></affiliation><affiliation><nlm:aff id="I2">Institute of Biotechnology and Antibiotics, Staroscinska 5, 02-516 Warsaw, Poland</nlm:aff></affiliation></author><author><name sortKey="Kieryl, Piotr" sort="Kieryl, Piotr" uniqKey="Kieryl P" first="Piotr" last="Kieryl">Piotr Kieryl</name><affiliation><nlm:aff id="I2">Institute of Biotechnology and Antibiotics, Staroscinska 5, 02-516 Warsaw, Poland</nlm:aff></affiliation></author><author><name sortKey="Plucienniczak, Andrzej" sort="Plucienniczak, Andrzej" uniqKey="Plucienniczak A" first="Andrzej" last="Plucienniczak">Andrzej Plucienniczak</name><affiliation><nlm:aff id="I2">Institute of Biotechnology and Antibiotics, Staroscinska 5, 02-516 Warsaw, Poland</nlm:aff></affiliation></author><author><name sortKey="Bartosik, Dariusz" sort="Bartosik, Dariusz" uniqKey="Bartosik D" first="Dariusz" last="Bartosik">Dariusz Bartosik</name><affiliation><nlm:aff id="I1">Department of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland</nlm:aff></affiliation></author></analytic><series><title level="j">BioMed Research International</title><idno type="ISSN">2314-6133</idno><idno type="eISSN">2314-6141</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Antibiotic resistance determinants are frequently associated with plasmids and other mobile genetic elements, which simplifies their horizontal transmission. Several groups of plasmids (including replicons of the IncL/M incompatibility group) were found to play an important role in the dissemination of resistance genes encoding <italic>β</italic>-lactamases. The IncL/M plasmids are large, broad host range, and self-transmissible replicons. We have identified and characterized two novel members of this group: pARM26 (isolated from bacteria inhabiting activated sludge from a wastewater treatment plant) and pIGT15 (originating from a clinical strain of <italic>Escherichia coli</italic>). This instigated a detailed comparative analysis of all available sequences of IncL/M plasmids encoding <italic>β</italic>-lactamases. The core genome of these plasmids is comprised of 20 genes with conserved synteny. Phylogenetic analyses of these core genes allowed clustering of the plasmids into four separate groups, which reflect their antibiotic resistance profiles. Examination of the biogeography of the IncL/M plasmids revealed that they are most frequently found in bacteria of the family Enterobacteriaceae originating from the Mediterranean region and Western Europe and that they are able to persist in various ecological niches even in the absence of direct antibiotic selection pressure.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Bush, K" uniqKey="Bush K">K. Bush</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Drawz, S M" uniqKey="Drawz S">S. M. Drawz</name></author><author><name sortKey="Bonomo, R A" uniqKey="Bonomo R">R. A. Bonomo</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Bush, K" uniqKey="Bush K">K. Bush</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Poirel, L" uniqKey="Poirel L">L. Poirel</name></author><author><name sortKey="Heritier, C" uniqKey="Heritier C">C. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Biomed Res Int</journal-id><journal-id journal-id-type="iso-abbrev">Biomed Res Int</journal-id><journal-id journal-id-type="publisher-id">BMRI</journal-id><journal-title-group><journal-title>BioMed Research International</journal-title></journal-title-group><issn pub-type="ppub">2314-6133</issn><issn pub-type="epub">2314-6141</issn><publisher><publisher-name>Hindawi Publishing Corporation</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26236726</article-id><article-id pub-id-type="pmc">4510254</article-id><article-id pub-id-type="doi">10.1155/2015/414681</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group></article-categories><title-group><article-title>Diversity and Global Distribution of IncL/M Plasmids Enabling Horizontal Dissemination of <italic>β</italic>-Lactam Resistance Genes among the Enterobacteriaceae</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Adamczuk</surname><given-names>Marcin</given-names></name><xref ref-type="aff" rid="I1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Zaleski</surname><given-names>Piotr</given-names></name><xref ref-type="aff" rid="I2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Dziewit</surname><given-names>Lukasz</given-names></name><xref ref-type="aff" rid="I1"><sup>1</sup></xref><xref ref-type="corresp" rid="cor1"><sup>*</sup></xref></contrib><contrib contrib-type="author"><name><surname>Wolinowska</surname><given-names>Renata</given-names></name><xref ref-type="aff" rid="I3"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Nieckarz</surname><given-names>Marta</given-names></name><xref ref-type="aff" rid="I1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Wawrzyniak</surname><given-names>Pawel</given-names></name><xref ref-type="aff" rid="I1"><sup>1</sup></xref><xref ref-type="aff" rid="I2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Kieryl</surname><given-names>Piotr</given-names></name><xref ref-type="aff" rid="I2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Plucienniczak</surname><given-names>Andrzej</given-names></name><xref ref-type="aff" rid="I2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Bartosik</surname><given-names>Dariusz</given-names></name><xref ref-type="aff" rid="I1"><sup>1</sup></xref><xref ref-type="corresp" rid="cor2"><sup>*</sup></xref></contrib></contrib-group><aff id="I1"><sup>1</sup>Department of Bacterial Genetics, Institute of Microbiology, Faculty of Biology, University of Warsaw, Miecznikowa 1, 02-096 Warsaw, Poland</aff><aff id="I2"><sup>2</sup>Institute of Biotechnology and Antibiotics, Staroscinska 5, 02-516 Warsaw, Poland</aff><aff id="I3"><sup>3</sup>Department of Pharmaceutical Microbiology, Medical University of Warsaw, Oczki 3, 02-007 Warsaw, Poland</aff><author-notes><corresp id="cor1">*Lukasz Dziewit: <email>ldziewit@biol.uw.edu.pl</email> and </corresp><corresp id="cor2">*Dariusz Bartosik: <email>bartosik@biol.uw.edu.pl</email></corresp><fn fn-type="other"><p>Academic Editor: Jorge F. Quarleri</p></fn></author-notes><pub-date pub-type="ppub"><year>2015</year></pub-date><pub-date pub-type="epub"><day>8</day><month>7</month><year>2015</year></pub-date><volume>2015</volume><elocation-id>414681</elocation-id><history><date date-type="received"><day>23</day><month>12</month><year>2014</year></date><date date-type="accepted"><day>22</day><month>6</month><year>2015</year></date></history><permissions><copyright-statement>Copyright © 2015 Marcin Adamczuk et al.</copyright-statement><copyright-year>2015</copyright-year><license license-type="open-access"><license-p>This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p></license></permissions><abstract><p>Antibiotic resistance determinants are frequently associated with plasmids and other mobile genetic elements, which simplifies their horizontal transmission. Several groups of plasmids (including replicons of the IncL/M incompatibility group) were found to play an important role in the dissemination of resistance genes encoding <italic>β</italic>-lactamases. The IncL/M plasmids are large, broad host range, and self-transmissible replicons. We have identified and characterized two novel members of this group: pARM26 (isolated from bacteria inhabiting activated sludge from a wastewater treatment plant) and pIGT15 (originating from a clinical strain of <italic>Escherichia coli</italic>). This instigated a detailed comparative analysis of all available sequences of IncL/M plasmids encoding <italic>β</italic>-lactamases. The core genome of these plasmids is comprised of 20 genes with conserved synteny. Phylogenetic analyses of these core genes allowed clustering of the plasmids into four separate groups, which reflect their antibiotic resistance profiles. Examination of the biogeography of the IncL/M plasmids revealed that they are most frequently found in bacteria of the family Enterobacteriaceae originating from the Mediterranean region and Western Europe and that they are able to persist in various ecological niches even in the absence of direct antibiotic selection pressure.</p></abstract></article-meta></front><body><sec id="sec1"><title>1. Introduction</title><p>The discovery of antibiotics initiated a new era in medicine. However, in recent years, the rapidly growing antibiotic resistance of pathogenic bacterial strains has greatly hindered the fight against infectious diseases. This problem is particularly serious in relation to the use of <italic>β</italic>-lactam antibiotics due to the profusion and diversity of <italic>β</italic>-lactamases. The production of these enzymes by Gram-negative bacteria is the most important factor undermining the efficacy of treatment using this group of antibiotics [<xref rid="B1" ref-type="bibr">1</xref>].</p><p>Two major schemes are used to classify <italic>β</italic>-lactamases: molecular discrimination (proposed by Ambler) based on amino acid sequences and functional discrimination (proposed by Bush-Jacoby-Medeiros) dividing enzymes according to their substrate and inhibitor specificities [<xref rid="B2" ref-type="bibr">2</xref>]. The Ambler classification is more commonly used, with each <italic>β</italic>-lactamase class grouping proteins according to discernible features such as molecular weight or conserved amino acid motifs [<xref rid="B3" ref-type="bibr">3</xref>].</p><p>Ambler classes A, C, and D <italic>β</italic>-lactamases contain a serine residue in their active site, whereas class B includes metalloenzymes (MBLs: metallo-<italic>β</italic>-lactamases) that require zinc ions for substrate hydrolysis. Attempts have been made to assign specific substrates to <italic>β</italic>-lactamases of particular classes (e.g., class A as penicillinases), but this division has proven to be inaccurate as novel enzymes with modified activity profiles are discovered following the introduction of newly developed drugs into clinical practice. For example, a single amino acid alteration in the narrow-spectrum <italic>β</italic>-lactamase SHV-1 may lead to the emergence of enzymes that can hydrolyze extended-spectrum cephalosporins or even carbapenems [<xref rid="B4" ref-type="bibr">4</xref>].</p><p>The dissemination of <italic>β</italic>-lactamase genes and other antibiotic resistance determinants is a consequence of inter- and intraspecies DNA exchange, occurring mainly due to the transfer of bacterial plasmids. Plasmids are extrachromosomal DNA molecules capable of autonomous replication, which are the major players in horizontal gene transfer and are responsible for shaping bacterial resistomes. A harmless environmental strain may be transformed into a pathogen by the acquisition of a multiresistance plasmid [<xref rid="B5" ref-type="bibr">5</xref>].</p><p>Plasmids promote the horizontal transfer of antibiotic resistance genes among bacteria belonging to various species or genera. The spread of these genes depends on the host range and conjugative properties of plasmids. Thus, conjugative, broad host range replicons have the greatest impact on overall antibiotic resistance transmission [<xref rid="B6" ref-type="bibr">6</xref>, <xref rid="B7" ref-type="bibr">7</xref>].</p><p>Amongst broad host range conjugative plasmids, special attention has been paid to IncL/M replicons, one of the six major resistance plasmid groups identified in clinically relevant Enterobacteriaceae [<xref rid="B8" ref-type="bibr">8</xref>, <xref rid="B9" ref-type="bibr">9</xref>]. Plasmids representing this incompatibility group have been identified as carriers of various <italic>β</italic>-lactam resistance genes encoding extended-spectrum <italic>β</italic>-lactamases (ESBL), classes A, B, and D carbapenemases, and AmpC <italic>β</italic>-lactamases [<xref rid="B10" ref-type="bibr">10</xref>–<xref rid="B21" ref-type="bibr">21</xref>]. Plasmid pEL60 of<italic> Erwinia amylovora</italic> was recognized as an archetype for the IncL/M group. It lacks mobile elements and drug resistance genes, typical for other multiresistant IncL/M plasmids [<xref rid="B22" ref-type="bibr">22</xref>]. However, a detailed genomic analysis revealed the presence of backbone genes typical for all IncL/M replicons, including replication and stabilization modules, a conjugative transfer system and a<italic> mucAB</italic>-like mutagenic DNA repair system, which is closely related to the<italic> rulAB</italic> operon conferring tolerance to UV radiation [<xref rid="B22" ref-type="bibr">22</xref>].</p><p>This study comprises an analysis of the complete nucleotide sequences of two SHV-5 <italic>β</italic>-lactamase-encoding plasmids (pARM26 and pIGT15) isolated from environmental and clinical samples, plus a detailed meta-analysis of available sequence data describing IncL/M replicons carrying <italic>β</italic>-lactamase genes.</p></sec><sec id="sec2"><title>2. Materials and Methods</title><sec id="sec2.1"><title>2.1. Bacterial Strains and Culture Conditions</title><p><italic>Escherichia coli</italic> strains DH5<italic>α</italic> [<xref rid="B23" ref-type="bibr">23</xref>] and CZD1527 [<xref rid="B24" ref-type="bibr">24</xref>] were grown in lysogeny broth (LB) medium [<xref rid="B25" ref-type="bibr">25</xref>] at 30°C or 37°C. Plates of solidified LB medium were prepared by the addition of 1.5% agar. Where necessary, the medium was supplemented with ampicillin (100 <italic>μ</italic>g/mL) and/or tetracycline (20 <italic>μ</italic>g/mL).</p></sec><sec id="sec2.2"><title>2.2. Isolation of Plasmids</title><p>Plasmid pARM26 was isolated exogenously in 2011. A flask containing 19 mL of LB medium supplemented with ampicillin (100 <italic>μ</italic>g/mL) was inoculated with 1 mL of return activated sludge from the “Czajka” wastewater treatment plant (Warsaw, Poland) and incubated overnight at 30°C with aeration. The bacterial growth was pelleted by centrifugation and plasmid DNA isolated by alkaline lysis.<italic> E. coli</italic> DH5<italic>α</italic> was transformed with the purified DNA, selecting on LB agar plates supplemented with ampicillin (100 <italic>μ</italic>g/mL) and tetracycline (20 <italic>μ</italic>g/mL).</p><p>Plasmid pIGT15 was isolated in 2005 from the multiresistant and multireplicon<italic> E. coli</italic> strain CZD1527 obtained from a child hospitalized in The Children's Memorial Health Institute in Warsaw (Poland) during the course of standard microbiological diagnostic testing.</p></sec><sec id="sec2.3"><title>2.3. DNA Sequencing</title><p>The complete nucleotide sequences of plasmids pARM26 and pIGT15 were determined using MiSeq sequencers (Illumina Inc.) in the DNA Sequencing and Oligonucleotide Synthesis Laboratory (oligo.pl) at the Institute of Biochemistry and Biophysics, Polish Academy of Sciences (Warsaw, Poland) and StarSEQ (Mainz, Germany), respectively. After quality filtering, the sequence data were assembled into contigs and scaffolds using Newbler De Novo Assembler v3.0 (Roche). Gaps were closed by the PCR amplification of DNA fragments, followed by Sanger sequencing with an ABI3730xl Genetic Analyzer (Life Technologies) using BigDye Terminator Mix v. 3.1 chemistry (Life Technologies).</p></sec><sec id="sec2.4"><title>2.4. DNA Manipulations and the Transformation of Bacterial Cells with Plasmids</title><p>The isolation of plasmids and common DNA manipulation methods were carried out as described previously [<xref rid="B25" ref-type="bibr">25</xref>]. PCR was performed in a Mastercycler (Eppendorf) using Taq DNA polymerase (Qiagen; with the supplied buffer), dNTP mixture, and appropriate primer pairs. Transformation of<italic> E. coli</italic> strains was performed according to the method of Kushner [<xref rid="B26" ref-type="bibr">28</xref>].</p></sec><sec id="sec2.5"><title>2.5. Bioinformatics</title><p>The plasmid nucleotide sequences were analyzed using Clone Manager (Sci-Ed8) and Artemis [<xref rid="B27" ref-type="bibr">29</xref>]. Similarity searches were performed using the BLAST programs [<xref rid="B28" ref-type="bibr">30</xref>]. Identified insertion sequences were compared with the ISfinder database [<xref rid="B29" ref-type="bibr">31</xref>]. For comparative analyses of plasmid sequences, the Easyfig program was used [<xref rid="B30" ref-type="bibr">32</xref>]. Phylogenetic analysis of the IncL/M plasmids was performed using the EDGAR tool [<xref rid="B31" ref-type="bibr">33</xref>]. To construct the phylogenetic tree, 20 core genes from the 20 IncL/M plasmid genomes were compared. Multiple alignments were created using MUSCLE software [<xref rid="B32" ref-type="bibr">34</xref>] and the highly variable regions of these alignments were removed using Gblocks [<xref rid="B33" ref-type="bibr">35</xref>]. The remaining sections of the alignments were concatenated into one multiple alignment and used in the construction of a phylogenetic tree with PHYLIP software [<xref rid="B34" ref-type="bibr">36</xref>]. The tree was visualized using TreeView version 1.6.6. [<xref rid="B35" ref-type="bibr">37</xref>]. Singletons and the core genes, initially defined using the EDGAR tool, were manually verified with BLASTn.</p></sec><sec id="sec2.6"><title>2.6. Nucleotide Sequence Accession Numbers</title><p>The sequences of plasmids pARM26 and pIGT15 determined in this study have been deposited in GenBank (NCBI) with the accession numbers KP294350 and KP294351, respectively.</p></sec></sec><sec id="sec3"><title>3. Results and Discussion</title><sec id="sec3.1"><title>3.1. The Structure of Plasmids pARM26 and pIGT15</title><p>Two novel antibiotic resistance plasmids belonging to the IncL/M incompatibility group were isolated: pARM26 from bacteria inhabiting activated sludge and pIGT15 from a clinical<italic> E. coli</italic> isolate. DNA sequencing demonstrated that both pARM26 (86,948 bp) and pIGT15 (74,839 bp) are circular plasmids with mean GC contents of 54.4% and 54.7%, respectively.<italic> In silico</italic> sequence analyses revealed that the plasmids carry 107 (pARM26) and 88 (pIGT15) putative genes. A summary of these genes, including their position, transcriptional orientation, the size of the encoded proteins, and their closest known homologs, is presented in Table S1 (Supplementary Materials, available online at <ext-link ext-link-type="uri" xlink:href="http://dx.doi.org/10.1155/2015/414681">http://dx.doi.org/10.1155/2015/414681</ext-link>).</p><p>Comparative analyses of the plasmid genomes revealed high levels of synteny and sequence identity. Homologs of all the pIGT15 genes are also present in the pARM26 genome and the aligned nucleotide sequences show 99% identity. Plasmid pARM26 is approximately 12 kb larger than pIGT15 because it possesses two additional DNA regions named region I and region II (<xref ref-type="fig" rid="fig1">Figure 1</xref>). Region I (nucleotide position 18,704–20,614) contains genes encoding (i) a conserved membrane protein (pIGT15 carries a truncated homologous gene encoding only the N-terminal part of this protein), (ii) a putative L-fuculose-phosphate aldolase (EC 4.1.2.17; which can also function as a D-ribulose-phosphate aldolase) involved in the utilization of L-fucose and D-arabinose [<xref rid="B36" ref-type="bibr">38</xref>], and (iii) a hydroxypyruvate isomerase (EC 5.3.1.22, which catalyzes the reversible isomerization of hydroxypyruvate and tartronate semialdehyde [<xref rid="B37" ref-type="bibr">39</xref>]). The region II (nucleotide position 53,618–63,898) carries 17 genes encoding (i) a DNA repair protein RadC, (ii) a HTH_XRE transcriptional regulator, (iii) gene expression modulator RmoA, (iv) antirestriction protein KlcA, (v) a mobilization protein C, and (vi) 12 hypothetical proteins of unknown function.</p><p>Comparison with the GenBank database revealed that pARM26 and pIGT15 are most closely related to plasmid pACM1 of<italic> Klebsiella oxytoca</italic> [<xref rid="B10" ref-type="bibr">10</xref>]. As shown in <xref ref-type="fig" rid="fig1">Figure 1</xref>, the three plasmids share gene synteny and show high levels of sequence conservation. Plasmid pACM1, the largest of the replicons, has an additional unique DNA region containing a class I integron carrying two antibiotic resistance gene cassettes (<xref ref-type="fig" rid="fig1">Figure 1</xref>). Each of the plasmids also contains several transposable elements (TEs), including (i) the insertion sequences IS<italic>26</italic> (2 copies; some in different genomic locations) and IS<italic>6100</italic> (1 copy), both classified within the IS<italic>6</italic> family [<xref rid="B29" ref-type="bibr">31</xref>] and (ii) a large Tn<italic>1721</italic>-like noncomposite Tn<italic>3</italic> family transposon (of 28,815 bp in pARM26, 26,985 bp in pIGT15, and 31,842 bp in pACM1), which is absent in other members of the IncL/M group. These three closely related plasmids are self-transmissible replicons conferring resistance to multiple antibiotics, including aminoglycosides (<italic>aacA4</italic>,<italic> aacC1</italic>, and<italic> aadA1</italic>), trimethoprim (<italic>dfrA1</italic>, only in pACM1), sulfonamides (<italic>sul1</italic>), and tetracycline (<italic>tetA</italic>). They also encode an extended-spectrum <italic>β</italic>-lactamase (ESBL) belonging to the SHV family, SHV-5 (<xref ref-type="fig" rid="fig1">Figure 1</xref>). Interestingly, all of the resistance determinants are embedded within the aforementioned Tn<italic>3</italic> family transposon (<xref ref-type="fig" rid="fig1">Figure 1</xref>).</p><p>It is important to mention that the bacterial host strains carrying these plasmids originated from different environments (i.e., nosocomial and nonnosocomial) and were isolated at different times. The plasmid pACM1 was isolated in 1993 from a cephalosporin-resistant<italic> K. oxytoca</italic> strain from the USA [<xref rid="B38" ref-type="bibr">40</xref>], pIGT15 in 2005 from a Polish clinical strain of<italic> E. coli</italic>, and pARM26 in 2011 from bacteria inhabiting a wastewater treatment plant, also in Poland. Comparative genomic analyses of other IncL/M replicons may shed light on the phylogeny and evolution of this group of antibiotic resistance plasmids, which play an important role in the dissemination of <italic>β</italic>-lactamase genes among members of the family Enterobacteriaceae.</p></sec><sec id="sec3.2"><title>3.2. Diversity and Comparative Genomics of the IncL/M Plasmids</title><p>To our knowledge, until now (December 2014), only eighteen complete nucleotide sequences of IncL/M plasmids have been deposited in public databases (<xref ref-type="table" rid="tab1">Table 1</xref>). With the addition of the two replicons described in this study (pARM26 and pIGT15) the sequences of 20 plasmids from this group were available for comparative genomic analyses.</p><p>Comparative analyses revealed that the pan-genome of the IncL/M plasmids consists of 248 genes. This is a relatively small number considering the fact that each of these large plasmids (of 60–90 kb in size; <xref ref-type="table" rid="tab1">Table 1</xref>) carries about 100 genes. This finding indicates that the IncL/M plasmids are highly conserved, sharing the majority of their genes. It is also in accordance with the small number of unique genes (56) identified in the plasmid genomes. Only half of the analyzed IncL/M plasmids contain singletons (<xref ref-type="table" rid="tab2">Table 2</xref>) and their number ranges from 0 to 15 per replicon. The highest number of singleton genes was found in plasmid R830b of<italic> Serratia marcescens</italic>, which does not carry any AR determinants. Several of these genes may play an important role in adaptation of the host strain to changing environmental conditions. Some appear to confer resistance to toxic heavy metals (mercury, cobalt, zinc, and cadmium), while others are probably engaged in formaldehyde detoxification (<xref ref-type="table" rid="tab2">Table 2</xref>). Heavy metal resistance genes (an arsenic resistance gene cluster) were also identified in pKOI-34, another member of the IncL/M group (<xref ref-type="table" rid="tab2">Table 2</xref>). The pool of singletons also includes 11 (19.6%) antibiotic resistance genes (<italic>aadA2</italic>, <italic>bla</italic><sub>CTX-M-14</sub>, <italic>bla</italic><sub>FOX-7</sub>, <italic>bla</italic><sub>IMP-4</sub>, <italic>bla</italic><sub>IMP-34</sub>, <italic>bla</italic><sub>KPC-4</sub>,<italic> dfrA1</italic>,<italic> dfrA12</italic>,<italic> mphA</italic>,<italic> strA</italic>, and<italic> strB</italic>), frequently associated with transposable elements (<xref ref-type="table" rid="tab2">Table 2</xref>). This finding is in agreement with previous observations suggesting that the majority of AR genes of the IncL/M plasmids have been acquired within TEs (or mobile integron gene cassettes) inserted at “hotspot” sites in the highly conserved plasmid backbone [<xref rid="B10" ref-type="bibr">10</xref>].</p><p>The core genome of the IncL/M plasmids consists of 20 genes, conserved in all the analyzed replicons. Functional classification of these genes revealed that they encode proteins involved in plasmid replication (<italic>repA, repC</italic>), stable plasmid maintenance (<italic>resD</italic>,<italic> parA</italic>), conjugal transfer (<italic>trbA</italic>,<italic> trbB</italic>,<italic> trbC</italic>,<italic> nikA</italic>,<italic> mobA</italic>,<italic> traH</italic>,<italic> traI</italic>,<italic> traJ</italic>,<italic> traM</italic>,<italic> traN</italic>,<italic> traO</italic>,<italic> traQ</italic>,<italic> traU</italic>,<italic> traW</italic>, and<italic> traY</italic>), and UV resistance (<italic>mucA</italic>). In an effort to understand the evolution of these plasmids, a phylogenetic analysis was performed based on the amino acid sequences of the proteins encoded by the core genes (<xref ref-type="fig" rid="fig2">Figure 2</xref>). Within the constructed phylogenetic tree, four main clusters are evident, grouping closely related replicons.</p><p>The first cluster (cluster I) is comprised of the plasmids pARM26 and pIGT15, identified in this work, and also the closely related pACM1. All three are multiresistance replicons carrying 7 (or 8 in the case of pACM1 [<xref rid="B10" ref-type="bibr">10</xref>]) AR genes, including a<italic> tetA</italic> gene conferring resistance to tetracycline, which is not present in other IncL/M plasmids (<xref ref-type="fig" rid="fig2">Figure 2</xref>). The second cluster (cluster II) contains two multiresistance replicons (pFOX-7a, pNE1280) [<xref rid="B15" ref-type="bibr">15</xref>, <xref rid="B20" ref-type="bibr">20</xref>] and plasmid pEL60 of the plant pathogen<italic> E. amylovora</italic>, which does not contain any AR genes [<xref rid="B22" ref-type="bibr">22</xref>] (<xref ref-type="fig" rid="fig2">Figure 2</xref>). The third and largest cluster (cluster III) is divided into two subclusters. The IIIA branch groups closely related plasmids pKPN-068, pENT-e56, and pENT-d0d, carrying five common, identical AR genes (<italic>bla</italic><sub>TEM-1</sub>, <italic>bla</italic><sub>SHV-12</sub>,<italic> aadB</italic>,<italic> qnrB19</italic>, and<italic> cat</italic>) [<xref rid="B39" ref-type="bibr">26</xref>], as well as the R830b replicon (containing no AR genes), which forms an outgroup within this subcluster (<xref ref-type="fig" rid="fig2">Figure 2</xref>). The IIIB branch gathers four similar plasmids (pOXA-48a, pJEG011, pKPoxa-48N1, and pE71T) with an embedded <italic>bla</italic><sub>OXA-48</sub> gene [<xref rid="B13" ref-type="bibr">13</xref>, <xref rid="B16" ref-type="bibr">16</xref>, <xref rid="B17" ref-type="bibr">17</xref>, <xref rid="B21" ref-type="bibr">21</xref>]. Interestingly, within this subcluster there is only one multiresistance plasmid, pJEG011 [<xref rid="B16" ref-type="bibr">16</xref>] (<xref ref-type="fig" rid="fig2">Figure 2</xref>). The fourth cluster (cluster IV) is also divided into two smaller subclusters: IVA, consisting of two plasmids, pNDM-HK and pNDM-OM, with a high level of genetic synteny [<xref rid="B18" ref-type="bibr">18</xref>, <xref rid="B19" ref-type="bibr">19</xref>], and IVB, grouping closely related plasmids pCTX-M3, pCTX-M360, and pEl1573 [<xref rid="B11" ref-type="bibr">11</xref>, <xref rid="B12" ref-type="bibr">12</xref>, <xref rid="B14" ref-type="bibr">14</xref>] (<xref ref-type="fig" rid="fig2">Figure 2</xref>).</p><p>The results of this phylogenetic analysis confirmed previous assumptions that there were probably several lineages of the IncL/M plasmids before they began acquiring diverse exogenous segments of DNA [<xref rid="B10" ref-type="bibr">10</xref>]. A more detailed comparative analysis showed that the insertions occurred within several “hotspots,” which are usually located between conserved core genes in the plasmid backbone. Insertions at other locations were observed in only a few cases, for example, in the plasmids pOXA-48a, pJEG011, pE71T, and pKPoxa-48N1 (all grouped in the subcluster IIIB), in which the acquired DNA interrupted the<italic> tir</italic> gene encoding a transfer inhibition protein.</p></sec><sec id="sec3.3"><title>3.3. IncL/M Plasmids: A Reservoir of <italic>β</italic>-Lactamase Genes</title><p>Among the 20 completely sequenced IncL/M plasmids, 18 encode at least one <italic>β</italic>-lactam resistance gene. In total, these plasmids carry 28 genes encoding 8 families of <italic>β</italic>-lactam hydrolyzing enzymes, representing all of the classes distinguished by Ambler: TEM, CTX-M, SHV, and KPC of Ambler class A; IMP and NDM of class B; FOX of class C; and OXA of class D [<xref rid="B40" ref-type="bibr">41</xref>, <xref rid="B41" ref-type="bibr">42</xref>].</p><p>The most common is the <italic>bla</italic><sub>TEM-1</sub> gene (encoding the TEM-1 type enzyme), which is present in 9 plasmids: (i–iv) pFOX-7a, pKPN-068, pENT-e56, and pENT-d0d, representing clusters II and III in the phylogenetic tree (<xref ref-type="fig" rid="fig2">Figure 2</xref>), and (v–ix) pNDM-OM, pNDM-HK, pCTX-M3, pCTX-M360, and pEl1573, all belonging to cluster IV (<xref ref-type="fig" rid="fig2">Figure 2</xref>). Interestingly, all of the aforementioned plasmids also encode another <italic>β</italic>-lactamase inactivating a wider range of <italic>β</italic>-lactams. The presence of this second <italic>β</italic>-lactamase gene reflects the relatively narrow substrate specificity of the TEM-1 type enzyme, which is capable of hydrolyzing only penicillins and narrow-spectrum cephalosporins (such as cephalothin or cefazolin), but not more recently developed higher-generation cephalosporins with an oxyimino side chain (oxyimino-cephalosporins) [<xref rid="B2" ref-type="bibr">2</xref>]. Thus, the resistance conferred by the TEM-1 enzyme (probably the most common among enteric bacteria [<xref rid="B42" ref-type="bibr">43</xref>]) is in fact currently ineffective and has been “bolstered” by the acquisition of other genes encoding <italic>β</italic>-lactamases with a broader specificity in the course of IncL/M plasmid evolution.</p><p>The IncL/M plasmids also frequently encode <italic>β</italic>-lactam hydrolyzing enzymes of the SHV family, which gathers more than 160 <italic>β</italic>-lactamases [<xref rid="B43" ref-type="bibr">44</xref>], including the common enzymes SHV-5 and SHV-12 [<xref rid="B44" ref-type="bibr">45</xref>]. The <italic>bla</italic><sub>SHV-5</sub> genes are carried by three closely related plasmids, pARM26, pIGT15, and pACM1 (cluster I in the phylogenetic tree), while <italic>bla</italic><sub>SHV-12</sub> genes are present within plasmids pKPN-068, pENT-e56, and pENT-d0d of the subcluster IIIA (<xref ref-type="fig" rid="fig2">Figure 2</xref>).</p><p>The IncL/M plasmids also encode enzymes representing the CTX-M family of ESBLs. These enzymes are less closely related to TEM or SHV <italic>β</italic>-lactamases but show high similarity to the <italic>β</italic>-lactamases of various<italic> Kluyvera</italic> species [<xref rid="B45" ref-type="bibr">46</xref>]. Three of the IncL/M plasmids encode the CTX-M family <italic>β</italic>-lactamases: (i-ii) pCTX-M3 and pCTX-M360 (<italic>bla</italic><sub>CTX-M3</sub>) and (iii) pJEG011 (<italic>bla</italic><sub>CTX-M14</sub>) (<xref ref-type="fig" rid="fig2">Figure 2</xref>).</p><p>Another class of <italic>β</italic>-lactamases encoded by the IncL/M plasmids is represented by KPC-4, a carbapenemase of the KPC family. The gene encoding this enzyme is located within the transposon Tn<italic>4401f</italic> embedded in the plasmid pNE1280 [<xref rid="B20" ref-type="bibr">20</xref>].</p><p>Several IncL/M plasmids also encode metallo-<italic>β</italic>-lactamases (MBL) of Ambler class B, that is, enzymes that require metal ions as cofactors for their activity [<xref rid="B46" ref-type="bibr">47</xref>]. MBLs are the most clinically important carbapenemases due to their ability to hydrolyze almost all <italic>β</italic>-lactams, except monobactams. Moreover, they are not susceptible to therapeutic <italic>β</italic>-lactam inhibitors, for example, clavulanate [<xref rid="B47" ref-type="bibr">48</xref>]. MBL genes were found within (i) pEl1573 (<italic>bla</italic><sub>IMP-4</sub> gene), (ii) pKOI-34 (<italic>bla</italic><sub>IMP-34</sub>), and (iii-iv) two nearly identical plasmids of the subcluster IVA, pNDM-HK and pNDM-OM (<italic>bla</italic><sub>NDM-1</sub>) (<xref ref-type="fig" rid="fig2">Figure 2</xref>). It is important to note that the <italic>bla</italic><sub>IMP-4</sub> and <italic>bla</italic><sub>IMP-34</sub> genes of pEl1573 and pKOI-34 are in fact class 1 integron gene cassettes, which is typical for most, if not all, genes encoding IMP-, VIM-, and GIM-type MBLs [<xref rid="B46" ref-type="bibr">47</xref>].</p><p>An Ambler class C <italic>β</italic>-lactamase (AmpC-type, CBL) is encoded by only one IncL/M plasmid, pFOX-7a, which was isolated from strains of<italic> Klebsiella pneumoniae</italic> associated with an outbreak in a neonatal intensive care unit in central Italy [<xref rid="B15" ref-type="bibr">15</xref>]. The FOX-7 enzyme can hydrolyze extended-spectrum cephalosporins (e.g., cephamycins) and is resistant to various combinations of <italic>β</italic>-lactamase inhibitors [<xref rid="B15" ref-type="bibr">15</xref>]. The <italic>bla</italic><sub>FOX-7</sub> gene is unique in the current pan-genome of the IncL/M plasmids (<xref ref-type="fig" rid="fig2">Figure 2</xref>, <xref ref-type="table" rid="tab2">Table 2</xref>).</p><p>Four of the IncL/M plasmids (pOXA-48, pJEG011, pKPoxa-48N1, and pE71T) (subcluster IIIB; <xref ref-type="fig" rid="fig2">Figure 2</xref>) carry the <italic>bla</italic><sub>OXA-48</sub> gene encoding a <italic>β</italic>-lactamase of Ambler class D. This enzyme is an OXA-family carbapenemase, which can hydrolyze penicillins and carbapenems but not extended-spectrum cephalosporins [<xref rid="B21" ref-type="bibr">21</xref>].</p><p>Epidemiological surveys have revealed that IncL/M plasmids play an important role in the global dissemination of <italic>β</italic>-lactam resistance genes (e.g., [<xref rid="B48" ref-type="bibr">49</xref>]). These replicons are not simply carriers of these resistance genes; they may also be considered “donors” of<italic> bla </italic>genes to other replicons coresiding in a particular host.</p><p>Close inspection of the IncL/M plasmid genomes revealed that the majority of their <italic>β</italic>-lactamase genes are associated with transposable elements (e.g., (i) <italic>bla</italic><sub>TEM-1</sub> is present within Tn<italic>2</italic> of pCTX-M360, pCTX-M3, pNDM-HK, pNDM-OM, and pEl1573, (ii) <italic>bla</italic><sub>CTX-M3</sub> was mobilized by IS<italic>Ecp1</italic> into pCTX-M3 and pCTX-M360, and (iii) <italic>bla</italic><sub>OXA-48</sub> occurs in Tn<italic>1999</italic> of pOXA-48a) or they persist in the form of integron gene cassettes (<italic>bla</italic><sub>IMP-4</sub> of pEl1573 and <italic>bla</italic><sub>IMP-34</sub> of pKOI-34). This localization significantly enhances the “mobility” of the resistance genes, which can be readily transferred from the IncL/M plasmids into bacterial chromosomes, as shown for the <italic>bla</italic><sub>OXA-48</sub> gene associated with the IS<italic>1R</italic>-based composite transposon Tn<italic>6237</italic> [<xref rid="B49" ref-type="bibr">50</xref>]. However, an even greater epidemiological threat is posed by the transfer of<italic> bla</italic> genes into other plasmids coresiding in a bacterial cell. This may result in the generation of novel resistance plasmids with a host range that is different from that of the parental IncL/M plasmids. Therefore, plasmid-mediated gene transfer can play a fundamental role in the crossing of taxonomic boundaries and may significantly influence the prevalence of <italic>β</italic>-lactam resistance.</p><p>It is notable that 13 of the analyzed IncL/M plasmids also contain other AR genes, which confer resistance to antibiotics representing 8 drug classes: aminoglycosides, macrolides, quinolones, trimethoprim, sulfonamides, bleomycin, chloramphenicol, and tetracycline (<xref ref-type="fig" rid="fig2">Figure 2</xref>). Interestingly, this phenomenon of multiresistance has also been observed in several other types of plasmids encoding extended-spectrum <italic>β</italic>-lactamases (e.g., [<xref rid="B50" ref-type="bibr">51</xref>]). In consequence, the choice of appropriate antibiotics to eliminate <italic>β</italic>-lactamase-producing pathogenic bacterial strains is becoming more and more limited [<xref rid="B51" ref-type="bibr">52</xref>].</p></sec><sec id="sec3.4"><title>3.4. Biogeography of the IncL/M Plasmids</title><p>Although IncL/M broad host range, self-transferable plasmids play an important role in the horizontal transmission of multiresistance phenotypes among Enterobacteriaceae, still very little is known about the diversity and distribution of these replicons in different environments. As mentioned above, the genetic structure of only 20 replicons of this group has been revealed to date. However, database searches (performed at the NCBI website) produced some information about four other members of the IncL/M group that have been partially sequenced and subjected to molecular analyses. These are R446b of<italic> Morganella morganii</italic> [<xref rid="B52" ref-type="bibr">53</xref>], R471a of<italic> Serratia marcescens</italic> [<xref rid="B53" ref-type="bibr">54</xref>], pMU407.1 of<italic> Klebsiella pneumoniae</italic> [<xref rid="B54" ref-type="bibr">55</xref>], and p61/9 of<italic> Salmonella enterica</italic> serovar Typhimurium [<xref rid="B55" ref-type="bibr">56</xref>]. Moreover, in depth analysis of sequence accessions in the NCBI database yielded further information concerning IncL/M plasmids (usually identified by PCR-based replicon typing) in samples originating from various environments. Most of the detected IncL/M plasmids were carried by pathogenic strains of Enterobacteriaceae isolated from hospitalized patients. These strains originated from 27 countries: Albania [<xref rid="B56" ref-type="bibr">57</xref>], Algeria [<xref rid="B57" ref-type="bibr">58</xref>], Argentina [<xref rid="B58" ref-type="bibr">59</xref>], Australia [<xref rid="B59" ref-type="bibr">60</xref>], Belgium [<xref rid="B60" ref-type="bibr">61</xref>], Brazil [<xref rid="B61" ref-type="bibr">62</xref>], Bulgaria [<xref rid="B62" ref-type="bibr">63</xref>], Canada [<xref rid="B63" ref-type="bibr">64</xref>], China [<xref rid="B64" ref-type="bibr">65</xref>], Croatia [<xref rid="B65" ref-type="bibr">66</xref>], Denmark [<xref rid="B66" ref-type="bibr">67</xref>], Egypt [<xref rid="B21" ref-type="bibr">21</xref>], France [<xref rid="B67" ref-type="bibr">68</xref>], Greece [<xref rid="B68" ref-type="bibr">69</xref>], Kenya [<xref rid="B69" ref-type="bibr">70</xref>], Korea [<xref rid="B70" ref-type="bibr">71</xref>], Lebanon [<xref rid="B21" ref-type="bibr">21</xref>], Libya [<xref rid="B71" ref-type="bibr">72</xref>], Morocco [<xref rid="B21" ref-type="bibr">21</xref>], Philippines [<xref rid="B68" ref-type="bibr">69</xref>], Portugal [<xref rid="B72" ref-type="bibr">73</xref>], Russia [<xref rid="B73" ref-type="bibr">74</xref>], Spain [<xref rid="B74" ref-type="bibr">75</xref>], Switzerland [<xref rid="B75" ref-type="bibr">76</xref>], Tunisia [<xref rid="B76" ref-type="bibr">77</xref>], Turkey [<xref rid="B21" ref-type="bibr">21</xref>], and USA [<xref rid="B77" ref-type="bibr">78</xref>]. IncL/M plasmids were also found in enterobacteria isolated from companion animals in Italy [<xref rid="B78" ref-type="bibr">79</xref>] and from an urban wastewater treatment plant in Algeria [<xref rid="B79" ref-type="bibr">80</xref>]. Thus, IncL/M plasmids have so far been identified in 31 countries on 6 continents, which points to their global distribution (<xref ref-type="fig" rid="fig3">Figure 3</xref>). Notably, the majority of strains carrying the IncL/M plasmids were identified in countries located near the Mediterranean Sea and in Western Europe (<xref ref-type="fig" rid="fig3">Figure 3</xref>).</p><p>Majority of the IncL/M plasmids were isolated from pathogenic strains of Enterobacteriaceae in the course of epidemiological studies. The unique genes found within these plasmids are usually involved in antibiotic resistance (<xref ref-type="table" rid="tab2">Table 2</xref>) and may be linked with the specific medical treatment in the particular health care unit. This exemplifies the role of mobile genetic elements in transfer of genes, enabling bacteria to improve their fitness under local stress conditions [<xref rid="B80" ref-type="bibr">81</xref>]. Such phenomenon is common for environmental bacterial strains, which are able to survive under various harsh conditions (e.g., [<xref rid="B81" ref-type="bibr">82</xref>–<xref rid="B83" ref-type="bibr">84</xref>]). This study illustrates that the IncL/M plasmids are not exclusively associated with pathogenic enterobacteria but are also found in nonnosocomial environments, including communal wastes. Wide dissemination of these multiresistance plasmids and their possible transfer into pathogenic bacteria make them an important and considerable epidemiological threat.</p></sec></sec><sec id="sec4"><title>4. Conclusions</title><p>The plasmids of the IncL/M incompatibility group are broad host range, multiresistance, self-transmissible replicons, which actively participate in the horizontal transfer of antibiotic resistance genes. These replicons have been associated with several outbreaks of disease caused by pathogenic strains of Enterobacteriaceae all over the world. They are also involved in the dissemination of <italic>β</italic>-lactam resistance, since they carry genes encoding enzymes representing all four Ambler classes of <italic>β</italic>-lactamases: Class A: TEM-1, SHV-5, SHV-12, CTX-M3, CTX-M14, and KPC-4; Class B: IMP-4, IMP-34, and NDM-1; Class C: FOX-7; and Class D: OXA-48.</p><p>Detailed analysis of the IncL/M plasmid genomes revealed that they have highly conserved backbones and share significant gene synteny. Moreover, phylogenetic analysis showed that these replicons may be grouped into four clusters, which also reflect the distribution of the antibiotic resistance determinants.</p><p>This study is the first to present available data indicating the global dissemination of bacteria carrying IncL/M plasmids. These multiresistance replicons not only are maintained by pathogenic strains of Enterobacteriaceae but also have been detected in bacteria inhabiting different nonnosocomial environments. A good example is the <italic>β</italic>-lactamase-encoding plasmid pARM26 characterized in this study, which was isolated from a wastewater treatment plant in Poland. Its identification strongly suggests that IncL/M plasmids have the ability to persist in various ecological niches even in the absence of direct antibiotic selection. Therefore, these plasmids constitute a rich reservoir of AR genes that may be disseminated among diverse bacteria (including pathogenic strains) in the natural environment.</p></sec><sec sec-type="supplementary-material" id="supplementary-material-sec"><title>Supplementary Material</title><supplementary-material content-type="local-data" id="f1"><caption><p>Table S1. Genes located within plasmids pARM26 and pIGT15.</p></caption><media xlink:href="414681.f1.pdf" mimetype="application" mime-subtype="pdf" orientation="portrait" id="d35e1274" position="anchor"></media></supplementary-material></sec></body><back><ack><title>Acknowledgments</title><p>This work was supported by the National Science Centre, Poland (Grant 2012/05/N/NZ9/01262) and the Ministry of Science and Higher Education, Poland (Grant DPN/N58/COST/2010).</p></ack><sec sec-type="conflict"><title>Conflict of Interests</title><p>The authors declare that there is no conflict of interests regarding the publication of this paper.</p></sec><ref-list><ref id="B1"><label>1</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Bush</surname><given-names>K.</given-names></name></person-group><article-title>Bench-to-bedside review: the role of <italic>β</italic>-lactamases in antibiotic-resistant Gram-negative infections</article-title><source><italic>Critical Care</italic></source><year>2010</year><volume>14</volume><issue>3, article 224</issue><pub-id pub-id-type="doi">10.1186/cc8892</pub-id><pub-id pub-id-type="other">2-s2.0-79952111025</pub-id></element-citation></ref><ref id="B2"><label>2</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Drawz</surname><given-names>S. 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The gray-shaded area connects DNA regions of different plasmids with at least 99% nucleotide sequence identity. Yellow frames indicate DNA regions (I and II) of pARM26 not present within pIGT15. REP: replication system; TRA: conjugal transfer system; PAR: partitioning system; InA and InB: class 1 integrons.</p></caption><graphic xlink:href="BMRI2015-414681.001"></graphic></fig><fig id="fig2" orientation="portrait" position="float"><label>Figure 2</label><caption><p>Comparative analyses of IncL/M plasmids. (a) Phylogenetic tree based on the 20 core genes of the IncL/M plasmids. (b) Comparative genomic analysis of the IncL/M plasmids (sequence annotations of several plasmids have been manually corrected; the distinguished genes are shown by arrows on the linear maps: red:<italic> bla</italic> genes; yellow: other AR genes). The gray-shaded areas connect DNA regions of different plasmids with at least 68% nucleotide sequence identity. (c–k) Comparison of the antibiotic resistance gene contents of the IncL/M plasmids: (c) <italic>β</italic>-lactam resistance genes; (d) aminoglycoside resistance genes; (e) macrolide resistance genes; (f) quinolone resistance genes; (g) trimethoprim resistance genes; (h) sulfonamide resistance genes; (i) bleomycin resistance genes; (j) chloramphenicol resistance genes; (k) tetracycline resistance genes.</p></caption><graphic xlink:href="BMRI2015-414681.002"></graphic></fig><fig id="fig3" orientation="portrait" position="float"><label>Figure 3</label><caption><p>Geographical distribution of IncL/M plasmids.</p></caption><graphic xlink:href="BMRI2015-414681.003"></graphic></fig><table-wrap id="tab1" orientation="portrait" position="float"><label>Table 1</label><caption><p>IncL/M plasmid sequences deposited in the GenBank database.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left" rowspan="1" colspan="1">Plasmid name</th><th align="left" rowspan="1" colspan="1">Host strain</th><th align="left" rowspan="1" colspan="1">Strain origin</th><th align="center" rowspan="1" colspan="1">Size <break></break>(bp)</th><th align="center" rowspan="1" colspan="1">% <break></break>GC </th><th align="left" rowspan="1" colspan="1">Reference/GenBank accession number</th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">pACM1</td><td align="left" rowspan="1" colspan="1"><italic>Klebsiella oxytoca </italic></td><td align="left" rowspan="1" colspan="1">New York, USA; hospital patient</td><td align="center" rowspan="1" colspan="1">89,977</td><td align="center" rowspan="1" colspan="1">54.4</td><td align="left" rowspan="1" colspan="1">[<xref rid="B10" ref-type="bibr">10</xref>]/NC_024997</td></tr><tr><td align="left" rowspan="1" colspan="1">pARM26</td><td align="left" rowspan="1" colspan="1">unknown bacterium</td><td align="left" rowspan="1" colspan="1">Warsaw, Poland; wastewater treatment plant</td><td align="center" rowspan="1" colspan="1">86,948</td><td align="center" rowspan="1" colspan="1">54.4</td><td align="left" rowspan="1" colspan="1">this work/KP294350</td></tr><tr><td align="left" rowspan="1" colspan="1">pCTX-M3</td><td align="left" rowspan="1" colspan="1"><italic>Citrobacter freundii </italic>2526</td><td align="left" rowspan="1" colspan="1">Warsaw, Poland; hospital patient</td><td align="center" rowspan="1" colspan="1">89,468</td><td align="center" rowspan="1" colspan="1">51.0</td><td align="left" rowspan="1" colspan="1">[<xref rid="B11" ref-type="bibr">11</xref>]/NC_004464</td></tr><tr><td align="left" rowspan="1" colspan="1">pCTX-M360</td><td align="left" rowspan="1" colspan="1"><italic>Klebsiella pneumoniae</italic> 0773</td><td align="left" rowspan="1" colspan="1">Guangzhou, China; hospital patient</td><td align="center" rowspan="1" colspan="1">68,018</td><td align="center" rowspan="1" colspan="1">51.4</td><td align="left" rowspan="1" colspan="1">[<xref rid="B12" ref-type="bibr">12</xref>]/NC_011641</td></tr><tr><td align="left" rowspan="1" colspan="1">pE71T</td><td align="left" rowspan="1" colspan="1"><italic>Klebsiella pneumoniae</italic> E71T</td><td align="left" rowspan="1" colspan="1">Ireland; hospital patient</td><td align="center" rowspan="1" colspan="1">63,578</td><td align="center" rowspan="1" colspan="1">51.2</td><td align="left" rowspan="1" colspan="1">[<xref rid="B13" ref-type="bibr">13</xref>]/NC_023027</td></tr><tr><td align="left" rowspan="1" colspan="1">pEl1573</td><td align="left" rowspan="1" colspan="1"><italic>Enterobacter cloacae</italic> El1573</td><td align="left" rowspan="1" colspan="1">Sydney, Australia; hospital patient</td><td align="center" rowspan="1" colspan="1">87,731</td><td align="center" rowspan="1" colspan="1">52.8</td><td align="left" rowspan="1" colspan="1">[<xref rid="B14" ref-type="bibr">14</xref>]/NC_019368</td></tr><tr><td align="left" rowspan="1" colspan="1">pEL60</td><td align="left" rowspan="1" colspan="1"><italic>Erwinia amylovora</italic> LebB66</td><td align="left" rowspan="1" colspan="1">Lebanon; fruits</td><td align="center" rowspan="1" colspan="1">60,145</td><td align="center" rowspan="1" colspan="1">51.5</td><td align="left" rowspan="1" colspan="1">[<xref rid="B22" ref-type="bibr">22</xref>]/NC_005246</td></tr><tr><td align="left" rowspan="1" colspan="1">pENT-d0d</td><td align="left" rowspan="1" colspan="1"><italic>Enterobacter cloacae</italic> ECNIH5</td><td align="left" rowspan="1" colspan="1">Bethesda, USA; hospital sink drain</td><td align="center" rowspan="1" colspan="1">77,575</td><td align="center" rowspan="1" colspan="1">50.7</td><td align="left" rowspan="1" colspan="1">[<xref rid="B39" ref-type="bibr">26</xref>]/CP009857</td></tr><tr><td align="left" rowspan="1" colspan="1">pENT-e56</td><td align="left" rowspan="1" colspan="1"><italic>Enterobacter cloacae</italic> ECNIH4</td><td align="left" rowspan="1" colspan="1">Bethesda, USA; hospital sink drain</td><td align="center" rowspan="1" colspan="1">77,248</td><td align="center" rowspan="1" colspan="1">51.5</td><td align="left" rowspan="1" colspan="1">[<xref rid="B39" ref-type="bibr">26</xref>]/CP009852</td></tr><tr><td align="left" rowspan="1" colspan="1">pFOX-7a</td><td align="left" rowspan="1" colspan="1"><italic>Klebsiella pneumonia</italic>e 45A03</td><td align="left" rowspan="1" colspan="1">Siena, Italy; hospital patient</td><td align="center" rowspan="1" colspan="1">90,439</td><td align="center" rowspan="1" colspan="1">53.4</td><td align="left" rowspan="1" colspan="1">[<xref rid="B15" ref-type="bibr">15</xref>]/NC_025134</td></tr><tr><td align="left" rowspan="1" colspan="1">pIGT15</td><td align="left" rowspan="1" colspan="1"><italic>Escherichia coli</italic> CZD1527</td><td align="left" rowspan="1" colspan="1">Warsaw, Poland; hospital patient</td><td align="center" rowspan="1" colspan="1">74,839</td><td align="center" rowspan="1" colspan="1">54.7</td><td align="left" rowspan="1" colspan="1">this work/KP294351</td></tr><tr><td align="left" rowspan="1" colspan="1">pJEG011</td><td align="left" rowspan="1" colspan="1"><italic>Klebsiella pneumoniae</italic> Kp002</td><td align="left" rowspan="1" colspan="1">Sydney, Australia; hospital patient</td><td align="center" rowspan="1" colspan="1">71,446</td><td align="center" rowspan="1" colspan="1">50.6</td><td align="left" rowspan="1" colspan="1">[<xref rid="B16" ref-type="bibr">16</xref>]/NC_021078</td></tr><tr><td align="left" rowspan="1" colspan="1">pKOI-34</td><td align="left" rowspan="1" colspan="1"><italic>Klebsiella oxytoca</italic> MS5279</td><td align="left" rowspan="1" colspan="1">Japan; hospital patient</td><td align="center" rowspan="1" colspan="1">87,343</td><td align="center" rowspan="1" colspan="1">53.3</td><td align="left" rowspan="1" colspan="1">[<xref rid="B84" ref-type="bibr">27</xref>]/AB715422</td></tr><tr><td align="left" rowspan="1" colspan="1">pKPN-068</td><td align="left" rowspan="1" colspan="1"><italic>Klebsiella pneumoniae </italic>KPNIH27</td><td align="left" rowspan="1" colspan="1">USA; hospital patient</td><td align="center" rowspan="1" colspan="1">80,411</td><td align="center" rowspan="1" colspan="1">51.3</td><td align="left" rowspan="1" colspan="1">—/CP007733</td></tr><tr><td align="left" rowspan="1" colspan="1">pKPoxa-48N1</td><td align="left" rowspan="1" colspan="1"><italic>Klebsiella pneumoniae </italic>KP1a</td><td align="left" rowspan="1" colspan="1">Nancy, France; hospital patient</td><td align="center" rowspan="1" colspan="1">62,592</td><td align="center" rowspan="1" colspan="1">51.1</td><td align="left" rowspan="1" colspan="1">[<xref rid="B17" ref-type="bibr">17</xref>]/NC_021488</td></tr><tr><td align="left" rowspan="1" colspan="1">pNDM-HK</td><td align="left" rowspan="1" colspan="1"><italic>Escherichia coli</italic> HK-01</td><td align="left" rowspan="1" colspan="1">Hong Kong, China; hospital patient</td><td align="center" rowspan="1" colspan="1">88,803</td><td align="center" rowspan="1" colspan="1">51.5</td><td align="left" rowspan="1" colspan="1">[<xref rid="B18" ref-type="bibr">18</xref>]/NC_019063</td></tr><tr><td align="left" rowspan="1" colspan="1">pNDM-OM</td><td align="left" rowspan="1" colspan="1"><italic>Klebsiella pneumoniae</italic> 601</td><td align="left" rowspan="1" colspan="1">Oman; hospital patient</td><td align="center" rowspan="1" colspan="1">87,185</td><td align="center" rowspan="1" colspan="1">51.5</td><td align="left" rowspan="1" colspan="1">[<xref rid="B19" ref-type="bibr">19</xref>]/NC_019889</td></tr><tr><td align="left" rowspan="1" colspan="1">pNE1280</td><td align="left" rowspan="1" colspan="1"><italic>Enterobacter cloacae</italic> 1623</td><td align="left" rowspan="1" colspan="1">Omaha, USA; hospital patient</td><td align="center" rowspan="1" colspan="1">66,531</td><td align="center" rowspan="1" colspan="1">52.3</td><td align="left" rowspan="1" colspan="1">[<xref rid="B20" ref-type="bibr">20</xref>]/NC_019346</td></tr><tr><td align="left" rowspan="1" colspan="1">pOXA-48a</td><td align="left" rowspan="1" colspan="1"><italic>Klebsiella pneumoniae </italic>Kp11978</td><td align="left" rowspan="1" colspan="1">Turkey; hospital patient</td><td align="center" rowspan="1" colspan="1">61,881</td><td align="center" rowspan="1" colspan="1">51.1</td><td align="left" rowspan="1" colspan="1">[<xref rid="B21" ref-type="bibr">21</xref>]/NC_019154</td></tr><tr><td align="left" rowspan="1" colspan="1">R830b</td><td align="left" rowspan="1" colspan="1"><italic>Serratia marcescens </italic></td><td align="left" rowspan="1" colspan="1">USA</td><td align="center" rowspan="1" colspan="1">81,793</td><td align="center" rowspan="1" colspan="1">53.2</td><td align="left" rowspan="1" colspan="1">—/NC_019344</td></tr></tbody></table></table-wrap><table-wrap id="tab2" orientation="portrait" position="float"><label>Table 2</label><caption><p>Unique genes identified within IncL/M plasmids.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left" rowspan="1" colspan="1">Plasmid name</th><th align="center" rowspan="1" colspan="1">Number of singletons</th><th align="left" rowspan="1" colspan="1">Singleton gene/locus tag [possible function]</th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">pACM1</td><td align="center" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1"><italic>dfrA1</italic>/D733_p1025 [dihydrofolate reductase]</td></tr><tr><td align="center" colspan="3" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1">pARM26</td><td align="center" rowspan="1" colspan="1">0</td><td align="left" rowspan="1" colspan="1">—</td></tr><tr><td align="center" colspan="3" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1">pCTX-M3</td><td align="center" rowspan="1" colspan="1">3</td><td align="left" rowspan="1" colspan="1"><italic>dfrA12</italic>/pCTX-M3_084 [dihydrofolate reductase]; <italic>orfF</italic>/pCTX-M3_085 [integron gene cassette, hypothetical protein]; <italic>aadA2</italic>/pCTX-M3_086 [streptomycin 3′-adenyltransferase]</td></tr><tr><td align="center" colspan="3" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1">pCTX-M360</td><td align="center" rowspan="1" colspan="1">0</td><td align="left" rowspan="1" colspan="1">—</td></tr><tr><td align="center" colspan="3" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1">pE71T</td><td align="center" rowspan="1" colspan="1">0</td><td align="left" rowspan="1" colspan="1">—</td></tr><tr><td align="center" colspan="3" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1">pEl1573</td><td align="center" rowspan="1" colspan="1">5</td><td align="left" rowspan="1" colspan="1"><italic>mphA</italic>/D727_p1024 [macrolide phosphorylase]; <italic>mrx</italic>/D727_p1026 [protein of unknown function, required for MphA expression]; <italic>mphR(A)</italic>/D727_p1027 [transcriptional regulator for macrolide phosphorylase gene <italic>mph(A</italic>)]; <italic>catB3</italic>/D727_p1035 [chloramphenicol acetyltransferase]; <italic>bla</italic><sub>IMP-4</sub>/D727_p1038 [IMP-4 metallo-<italic>β</italic>-lactamase]</td></tr><tr><td align="center" colspan="3" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1">pEL60</td><td align="center" rowspan="1" colspan="1">2</td><td align="left" rowspan="1" colspan="1"><italic>orf8</italic>/pEL60p08 [hypothetical protein]; <italic>kfrA</italic>/pEL60p09 [plasmid maintenance protein KfrA]</td></tr><tr><td align="center" colspan="3" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1">pENT-d0d</td><td align="center" rowspan="1" colspan="1">0</td><td align="left" rowspan="1" colspan="1">—</td></tr><tr><td align="center" colspan="3" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1">pENT-e56</td><td align="center" rowspan="1" colspan="1">0</td><td align="left" rowspan="1" colspan="1">—</td></tr><tr><td align="center" colspan="3" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1">pFOX-7a</td><td align="center" rowspan="1" colspan="1">9</td><td align="left" rowspan="1" colspan="1">bla<sub>FOX-7</sub>/D647_p51042 [FOX-7 <italic>β</italic>-lactamase]; <italic>mdrL</italic>/D647_p51043 [major facilitator transporter]; <italic>lysR</italic>/D647_p51044 [LysR family transcriptional regulator];<italic> tnpA</italic>/D647_p51045 [transposase of IS<italic>1634</italic>-family insertion sequence]; tnpA/D647_p51046 [transposase of IS<italic>Apu1</italic> (IS<italic>4</italic> family/IS<italic>H8</italic> group)]; D647_p51047 [hypothetical protein]; <italic>tnpA</italic>/D647_p51048 [transposase of IS<italic>Apu2</italic> (IS<italic>4</italic> family/IS<italic>H8</italic> group)]; <italic>istA</italic>/D647_p51052 [IstA protein of IS<italic>1326</italic> (IS<italic>21</italic> family)]; <italic>istB</italic>/D647_p51053 [IstB protein of IS<italic>1326</italic> (IS<italic>21</italic> family)]</td></tr><tr><td align="center" colspan="3" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1">pIGT15</td><td align="center" rowspan="1" colspan="1">0</td><td align="left" rowspan="1" colspan="1">—</td></tr><tr><td align="center" colspan="3" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1">pJEG011</td><td align="center" rowspan="1" colspan="1">5</td><td align="left" rowspan="1" colspan="1"><italic>strA</italic>/D647_p23045 [streptomycin phosphotransferase A]; <italic>strB</italic>/D647_p23040 [streptomycin phosphotransferase B]; <italic>aphA6</italic>/D647_p23043 [aminoglycoside 3′-phosphotransferase]; tnpA/D647_p23042 [transposase of IS<italic>1</italic>-family insertion sequence]; <italic>bla</italic><sub>CTX-M-14</sub>/D647_p23049 [extended-spectrum <italic>β</italic>-lactamase]</td></tr><tr><td align="center" colspan="3" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1">pKOI-34</td><td align="center" rowspan="1" colspan="1">7</td><td align="left" rowspan="1" colspan="1"><italic>arsR</italic> [arsenical resistance operon repressor]; arsD [arsenical resistance operon transacting repressor]; <italic>arsA</italic> [arsenical pump-driving ATPase]; <italic>arsB</italic> [arsenic efflux pump protein]; <italic>arsC</italic> [arsenate reductase]; <italic>ycgA</italic> [arsenical pump-driving ATPase]; <italic>bla</italic><sub>IMP-34</sub> [IMP-34 metallo-<italic>β</italic>-lactamase]</td></tr><tr><td align="center" colspan="3" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1">pKPN-068</td><td align="center" rowspan="1" colspan="1">0</td><td align="left" rowspan="1" colspan="1">—</td></tr><tr><td align="center" colspan="3" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1">pKPoxa-48N1</td><td align="center" rowspan="1" colspan="1">0</td><td align="left" rowspan="1" colspan="1">—</td></tr><tr><td align="center" colspan="3" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1">pNDM-HK</td><td align="center" rowspan="1" colspan="1">1</td><td align="left" rowspan="1" colspan="1"><italic>insL</italic>/D616_p59011 [transposase of IS<italic>4</italic> family/IS<italic>231</italic> group insertion sequence]</td></tr><tr><td align="center" colspan="3" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1">pNDM-OM</td><td align="center" rowspan="1" colspan="1">0</td><td align="left" rowspan="1" colspan="1">—</td></tr><tr><td align="center" colspan="3" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1">pNE1280</td><td align="center" rowspan="1" colspan="1">8</td><td align="left" rowspan="1" colspan="1"><italic>istB</italic>/KPC4_0043 [IstB protein of IS<italic>21</italic>-family insertion sequence]; <italic>bla</italic><sub>KPC-4</sub>/KPC4_0045 [<italic>β</italic>-lactamase]; <italic>tnpA</italic>/KPC4_0047 [transposase]; KPC4_0049 [hypothetical protein]; KPC4_0051 [hypothetical protein]; KPC4_0053 [hypothetical protein]; <italic>rom</italic>/KPC4_0055 [Rop family protein]; <italic>exc1</italic>/KPC4_0057 [exclusion protein 1]</td></tr><tr><td align="center" colspan="3" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1">pOXA-48a</td><td align="center" rowspan="1" colspan="1">0</td><td align="left" rowspan="1" colspan="1">—</td></tr><tr><td align="center" colspan="3" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1">R830b</td><td align="center" rowspan="1" colspan="1">15</td><td align="left" rowspan="1" colspan="1"><italic>tniQ</italic>/D739_p1005 [transposase helper protein TniQ]; D739_p1006 [resolvase/integrase]; D739_p1010 [organomercurial lyase]; D739_p1020 [putative reverse transcriptase]; D739_p1024 [hypothetical protein]; D739_p1025 [Il-IS_2, transposase]; D739_p1026 [lipoprotein signal peptidase]; D739_p1027 [cobalt-zinc-cadmium resistance protein CzcD]; D739_p1028 [Cd(II)/Pb(II)-responsive transcriptional regulator]; D739_p1029 [hypothetical protein]; D739_p1107 [resolvase]; D739_p1108 [S-formylglutathione hydrolase]; D739_p1109 [glyoxalase]; D739_p1110 [S-(hydroxymethyl)glutathione dehydrogenase]; D739_p1111 [uncharacterized protein YaiN in formaldehyde detoxification operon]</td></tr></tbody></table></table-wrap></floats-group></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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