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...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Sara Domingues, Klaus Harms, W Florian Fricke, Pål J Johnsen, Gabriela J da Silva, Kaare Magne Nielsen
Formato: article
Lenguaje:EN
Publicado: Public Library of Science (PLoS) 2012
Materias:
Acceso en línea:https://doaj.org/article/92dcdc30f0994e77a5a1be035e52a244
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:92dcdc30f0994e77a5a1be035e52a244
record_format dspace
spelling 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)
institution DOAJ
collection DOAJ
language EN
topic Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
spellingShingle 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