Natural transformation facilitates transfer of transposons, integrons and gene cassettes between bacterial species.
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 integro...
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oai:doaj.org-article:92dcdc30f0994e77a5a1be035e52a2442021-11-18T06:04:08ZNatural transformation facilitates transfer of transposons, integrons and gene cassettes between bacterial species.1553-73661553-737410.1371/journal.ppat.1002837https://doaj.org/article/92dcdc30f0994e77a5a1be035e52a2442012-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22876180/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374We 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.Sara DominguesKlaus HarmsW Florian FrickePål J JohnsenGabriela J da SilvaKaare Magne NielsenPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 8, Iss 8, p e1002837 (2012) |
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Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 |
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Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 Sara Domingues Klaus Harms W Florian Fricke Pål J Johnsen Gabriela J da Silva Kaare Magne Nielsen Natural transformation facilitates transfer of transposons, integrons and gene cassettes between bacterial species. |
description |
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. |
format |
article |
author |
Sara Domingues Klaus Harms W Florian Fricke Pål J Johnsen Gabriela J da Silva Kaare Magne Nielsen |
author_facet |
Sara Domingues Klaus Harms W Florian Fricke Pål J Johnsen Gabriela J da Silva Kaare Magne Nielsen |
author_sort |
Sara Domingues |
title |
Natural transformation facilitates transfer of transposons, integrons and gene cassettes between bacterial species. |
title_short |
Natural transformation facilitates transfer of transposons, integrons and gene cassettes between bacterial species. |
title_full |
Natural transformation facilitates transfer of transposons, integrons and gene cassettes between bacterial species. |
title_fullStr |
Natural transformation facilitates transfer of transposons, integrons and gene cassettes between bacterial species. |
title_full_unstemmed |
Natural transformation facilitates transfer of transposons, integrons and gene cassettes between bacterial species. |
title_sort |
natural transformation facilitates transfer of transposons, integrons and gene cassettes between bacterial species. |
publisher |
Public Library of Science (PLoS) |
publishDate |
2012 |
url |
https://doaj.org/article/92dcdc30f0994e77a5a1be035e52a244 |
work_keys_str_mv |
AT saradomingues naturaltransformationfacilitatestransferoftransposonsintegronsandgenecassettesbetweenbacterialspecies AT klausharms naturaltransformationfacilitatestransferoftransposonsintegronsandgenecassettesbetweenbacterialspecies AT wflorianfricke naturaltransformationfacilitatestransferoftransposonsintegronsandgenecassettesbetweenbacterialspecies AT paljjohnsen naturaltransformationfacilitatestransferoftransposonsintegronsandgenecassettesbetweenbacterialspecies AT gabrielajdasilva naturaltransformationfacilitatestransferoftransposonsintegronsandgenecassettesbetweenbacterialspecies AT kaaremagnenielsen naturaltransformationfacilitatestransferoftransposonsintegronsandgenecassettesbetweenbacterialspecies |
_version_ |
1718424617969778688 |