Natural Transformation Facilitates Transfer of Transposons, Integrons and Gene Cassettes between Bacterial Species
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{"title"=>"Natural Transformation Facilitates Transfer of Transposons, Integrons and Gene Cassettes between Bacterial Species", "type"=>"journal", "authors"=>[{"first_name"=>"Sara", "last_name"=>"Domingues", "scopus_author_id"=>"55110692600"}, {"first_name"=>"Klaus", "last_name"=>"Harms", "scopus_author_id"=>"57104663800"}, {"first_name"=>"W. Florian", "last_name"=>"Fricke", "scopus_author_id"=>"34568855100"}, {"first_name"=>"Pål J.", "last_name"=>"Johnsen", "scopus_author_id"=>"7004281191"}, {"first_name"=>"Gabriela J.", "last_name"=>"da Silva", "scopus_author_id"=>"7004554469"}, {"first_name"=>"Kaare Magne", "last_name"=>"Nielsen", "scopus_author_id"=>"7401572752"}], "year"=>2012, "source"=>"PLoS Pathogens", "identifiers"=>{"pui"=>"365631414", "sgr"=>"84866172604", "issn"=>"15537366", "pmid"=>"22876180", "scopus"=>"2-s2.0-84866172604", "doi"=>"10.1371/journal.ppat.1002837", "isbn"=>"1553-7374 (Electronic)\\n1553-7366 (Linking)"}, "id"=>"9edf2f43-a96d-3a61-8421-8e113d9e5b4b", "abstract"=>"We have investigated to what extent natural transformation acting on free DNA substrates can facilitate transfer of mobile elements including transposons, integrons and/or gene cassettes between bacterial species. Naturally transformable cells of Acinetobacter baylyi were exposed to DNA from integron-carrying strains of the genera Acinetobacter, Citrobacter, Enterobacter, Escherichia, Pseudomonas, and Salmonella to determine the nature and frequency of transfer. Exposure to the various DNA sources resulted in acquisition of antibiotic resistance traits as well as entire integrons and transposons, over a 24 h exposure period. DNA incorporation was not solely dependent on integrase functions or the genetic relatedness between species. DNA sequence analyses revealed that several mechanisms facilitated stable integration in the recipient genome depending on the nature of the donor DNA; homologous or heterologous recombination and various types of transposition (Tn21-like and IS26-like). Both donor strains and transformed isolates were extensively characterized by antimicrobial susceptibility testing, integron- and cassette-specific PCRs, DNA sequencing, pulsed field gel electrophoreses (PFGE), Southern blot hybridizations, and by re-transformation assays. Two transformant strains were also genome-sequenced. Our data demonstrate that natural transformation facilitates interspecies transfer of genetic elements, suggesting that the transient presence of DNA in the cytoplasm may be sufficient for genomic integration to occur. Our study provides a plausible explanation for why sequence-conserved transposons, IS elements and integrons can be found disseminated among bacterial species. Moreover, natural transformation of integron harboring populations of competent bacteria revealed that interspecies exchange of gene cassettes can be highly efficient, and independent on genetic relatedness between donor and recipient. In conclusion, natural transformation provides a much broader capacity for horizontal acquisitions of genetic elements and hence, resistance traits from divergent species than previously assumed.", "link"=>"http://www.mendeley.com/research/natural-transformation-facilitates-transfer-transposons-integrons-gene-cassettes-between-bacterial-s", "reader_count"=>138, "reader_count_by_academic_status"=>{"Unspecified"=>4, "Professor > Associate Professor"=>9, "Researcher"=>21, "Student > Doctoral Student"=>10, "Student > Ph. D. Student"=>36, "Student > Postgraduate"=>6, "Student > Master"=>25, "Other"=>4, "Student > Bachelor"=>12, "Lecturer"=>4, "Professor"=>7}, "reader_count_by_user_role"=>{"Unspecified"=>4, "Professor > Associate Professor"=>9, "Researcher"=>21, "Student > Doctoral Student"=>10, "Student > Ph. D. 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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/598445"], "description"=>"a)<p>Natural transformation assays were performed with purified DNA as donor source, except in the experiments with the various donor species and <i>A. baylyi</i> BD413 recipient bacteria, where supernatants of heat-treated cell suspensions were used as the sole source of DNA.</p>b)<p>The transformation frequency obtained with DNA from positive control source (<i>A. baylyi</i> KTG with the <i>ntpII</i> gene) was 4.7×10<sup>−4</sup>. Negative control experiments, consisting of the same experimental conditions, with the exception of that no DNA was added, were included in each transformation assay.</p>c)<p>The transformation frequency is, when calculated as the frequency per exposed unit of DNA: 1.3×10<sup>−8</sup> transformants per genome equivalent and 7.5×10<sup>−8</sup> transformants per genome equivalent for <i>A. baumannii</i> 064 and <i>S. enterica</i> serovar Typhimurium 490, respectively. The genome equivalent size is based on the average size calculated from published genomes of the 2 species, as available in GenBank (Apr. 2012); 3.95 Mb and 4.99 Mb, respectively).</p>", "links"=>[], "tags"=>["genomic", "dna"], "article_id"=>268928, "categories"=>["Genetics", "Microbiology"], "users"=>["Sara Domingues", "Klaus Harms", "W. Florian Fricke", "Pål J. Johnsen", "Gabriela J. da Silva", "Kaare Magne Nielsen"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002837.t002", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Natural_transformation_of_A_baylyi_with_genomic_DNA_from_different_sources_/268928", "title"=>"Natural transformation of <i>A. baylyi</i> with genomic DNA from different sources.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-08-02 02:28:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/313159", "https://ndownloader.figshare.com/files/313181", "https://ndownloader.figshare.com/files/313200", "https://ndownloader.figshare.com/files/313242", "https://ndownloader.figshare.com/files/313249"], "description"=>"<div><p>We have investigated to what extent natural transformation acting on free DNA substrates can facilitate transfer of mobile elements including transposons, integrons and/or gene cassettes between bacterial species. Naturally transformable cells of <em>Acinetobacter baylyi</em> were exposed to DNA from integron-carrying strains of the genera <em>Acinetobacter</em>, <em>Citrobacter</em>, <em>Enterobacter</em>, <em>Escherichia</em>, <em>Pseudomonas</em>, and<em> Salmonella</em> to determine the nature and frequency of transfer. Exposure to the various DNA sources resulted in acquisition of antibiotic resistance traits as well as entire integrons and transposons, over a 24 h exposure period. DNA incorporation was not solely dependent on integrase functions or the genetic relatedness between species. DNA sequence analyses revealed that several mechanisms facilitated stable integration in the recipient genome depending on the nature of the donor DNA; homologous or heterologous recombination and various types of transposition (Tn<em>21</em>-like and IS<em>26</em>-like). Both donor strains and transformed isolates were extensively characterized by antimicrobial susceptibility testing, integron- and cassette-specific PCRs, DNA sequencing, pulsed field gel electrophoreses (PFGE), Southern blot hybridizations, and by re-transformation assays. Two transformant strains were also genome-sequenced. Our data demonstrate that natural transformation facilitates interspecies transfer of genetic elements, suggesting that the transient presence of DNA in the cytoplasm may be sufficient for genomic integration to occur. Our study provides a plausible explanation for why sequence-conserved transposons, IS elements and integrons can be found disseminated among bacterial species. Moreover, natural transformation of integron harboring populations of competent bacteria revealed that interspecies exchange of gene cassettes can be highly efficient, and independent on genetic relatedness between donor and recipient. In conclusion, natural transformation provides a much broader capacity for horizontal acquisitions of genetic elements and hence, resistance traits from divergent species than previously assumed.</p> </div>", "links"=>[], "tags"=>["facilitates", "integrons", "cassettes", "bacterial"], "article_id"=>121766, "categories"=>["Genetics", "Microbiology"], "users"=>["Sara Domingues", "Klaus Harms", "W. Florian Fricke", "Pål J. Johnsen", "Gabriela J. da Silva", "Kaare Magne Nielsen"], "doi"=>["https://dx.doi.org/10.1371/journal.ppat.1002837.s001", "https://dx.doi.org/10.1371/journal.ppat.1002837.s002", "https://dx.doi.org/10.1371/journal.ppat.1002837.s003", "https://dx.doi.org/10.1371/journal.ppat.1002837.s004", "https://dx.doi.org/10.1371/journal.ppat.1002837.s005"], "stats"=>{"downloads"=>10, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Natural_Transformation_Facilitates_Transfer_of_Transposons_Integrons_and_Gene_Cassettes_between_Bacterial_Species/121766", "title"=>"Natural Transformation Facilitates Transfer of Transposons, Integrons and Gene Cassettes between Bacterial Species", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-08-02 00:29:26"}
  • {"files"=>["https://ndownloader.figshare.com/files/598354"], "description"=>"<p>A) Transformant (St)1 obtained after exposure to DNA of <i>S. enterica</i> serovar Typhimurium 490. B) Transformants SD1, (SD1)1, (SD1)2 and (SD1)3 obtained after exposure to DNA of <i>S. enterica</i> serovar Typhimurium 490. C) Transformants SD2, (SD2)1, (SD2)2 and (SD2)3 obtained after exposure of DNA of <i>A. baumannii</i> 064, D) transformants (AbII)3 obtained after exposure to DNA of <i>A. baumannii</i> 064, E) transformant (St)3 obtained after exposure to DNA of <i>S. enterica</i> serovar Typhimurium 490; Gene 1 – gene coding for a bacterial regulatory, tetR family protein; Gene 2 – gene coding for a flavodoxin-like fold family protein. Class 1 integron includes the <i>intI1</i>, gene cassettes, <i>qacΔE</i>, <i>sulI1</i> and <i>orf5</i> genes.</p>", "links"=>[], "tags"=>["fragments", "acquired"], "article_id"=>268830, "categories"=>["Genetics", "Microbiology"], "users"=>["Sara Domingues", "Klaus Harms", "W. Florian Fricke", "Pål J. Johnsen", "Gabriela J. da Silva", "Kaare Magne Nielsen"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002837.g001", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_DNA_fragments_acquired_from_S_enterica_and_A_baumannii_by_the_A_baylyi_transformants_/268830", "title"=>"DNA fragments acquired from <i>S. enterica</i> and <i>A. baumannii</i> by the <i>A. baylyi</i> transformants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-08-02 02:27:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/598489"], "description"=>"a<p>Obtained with 5′-CS and 3′-CS primers <a href=\"http://www.plospathogens.org/article/info:doi/10.1371/journal.ppat.1002837#ppat.1002837-Levesque1\" target=\"_blank\">[24]</a>.</p>b<p>The resistance trait was used for selection in the natural transformation assays.</p>c<p>Transformants obtained after exposure to these sources of DNA were only tested at the phenotypic level.</p>d<p>Obtained by natural transformation of <i>A. baylyi</i> BD413 with purified DNA from <i>A. baumannii</i> 064. Integron acquisition was shown first by PCR, which explains the antimicrobial susceptibility profile of the tested antibiotics. The PFGE profile obtained with restriction digestion using the enzyme I-<i>Ceu</i>I revealed unexpected bands that co-hybridized with the probe for <i>intI</i>1 gene in Southern blot.</p>e<p>Obtained by natural transformation of <i>A. baylyi</i> BD413 with purified DNA from <i>S. enterica</i> serovar Thypimurium 490. Integron acquisition was shown first by PCR, which explains the antimicrobial susceptibility profile of the tested antibiotics. Initial sequencing of the integron flanking regions, by primer walking, showed that the acquired fragment was large; suggestive of the possible acquisition of a plasmid (excluded after sequencing).</p>R<p>resistance; CN – gentamicin, CTX – cefotaxime, K – kanamycin, R – rifampicin, SC – spectinomycin, W – trimethoprim.</p><p>n.d.- not determined.</p>", "links"=>[], "tags"=>["strains"], "article_id"=>268978, "categories"=>["Genetics", "Microbiology"], "users"=>["Sara Domingues", "Klaus Harms", "W. Florian Fricke", "Pål J. Johnsen", "Gabriela J. da Silva", "Kaare Magne Nielsen"], "doi"=>"https://dx.doi.org/10.1371/journal.ppat.1002837.t001", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_the_strains_used_in_this_study_/268978", "title"=>"Summary of the strains used in this study.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-08-02 02:29:38"}

PMC Usage Stats | Further Information

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Relative Metric

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