Genotoxic stress stimulates eDNA release via explosive cell lysis and thereby promotes streamer formation of Burkholderia cenocepacia H111 cultured in a microfluidic device
Abstract DNA is a component of biofilms, but the triggers of DNA release during biofilm formation and how DNA contributes to biofilm development are poorly investigated. One key mechanism involved in DNA release is explosive cell lysis, which is a consequence of prophage induction. In this article,...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2023-12-01
|
| Series: | npj Biofilms and Microbiomes |
| Online Access: | https://doi.org/10.1038/s41522-023-00464-7 |
| _version_ | 1797398140163194880 |
|---|---|
| author | Zaira Heredia-Ponce Eleonora Secchi Masanori Toyofuku Gabriela Marinova Giovanni Savorana Leo Eberl |
| author_facet | Zaira Heredia-Ponce Eleonora Secchi Masanori Toyofuku Gabriela Marinova Giovanni Savorana Leo Eberl |
| author_sort | Zaira Heredia-Ponce |
| collection | DOAJ |
| description | Abstract DNA is a component of biofilms, but the triggers of DNA release during biofilm formation and how DNA contributes to biofilm development are poorly investigated. One key mechanism involved in DNA release is explosive cell lysis, which is a consequence of prophage induction. In this article, the role of explosive cell lysis in biofilm formation was investigated in the opportunistic human pathogen Burkholderia cenocepacia H111 (H111). Biofilm streamers, flow-suspended biofilm filaments, were used as a biofilm model in this study, as DNA is an essential component of their matrix. H111 contains three prophages on chromosome 1 of its genome, and the involvement of each prophage in causing explosive cell lysis of the host and subsequent DNA and membrane vesicle (MV) release, as well as their contribution to streamer formation, were studied in the presence and absence of genotoxic stress. The results show that two of the three prophages of H111 encode functional lytic prophages that can be induced by genotoxic stress and their activation causes DNA and MVs release by explosive cell lysis. Furthermore, it is shown that the released DNA enables the strain to develop biofilm streamers, and streamer formation can be enhanced by genotoxic stress. Overall, this study demonstrates the involvement of prophages in streamer formation and uncovers an often-overlooked problem with the use of antibiotics that trigger the bacterial SOS response for the treatment of bacterial infections. |
| first_indexed | 2024-03-09T01:20:26Z |
| format | Article |
| id | doaj.art-5c13ebbdbfad44f4b553431390f27760 |
| institution | Directory Open Access Journal |
| issn | 2055-5008 |
| language | English |
| last_indexed | 2024-03-09T01:20:26Z |
| publishDate | 2023-12-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | npj Biofilms and Microbiomes |
| spelling | doaj.art-5c13ebbdbfad44f4b553431390f277602023-12-10T12:09:25ZengNature Portfolionpj Biofilms and Microbiomes2055-50082023-12-019111010.1038/s41522-023-00464-7Genotoxic stress stimulates eDNA release via explosive cell lysis and thereby promotes streamer formation of Burkholderia cenocepacia H111 cultured in a microfluidic deviceZaira Heredia-Ponce0Eleonora Secchi1Masanori Toyofuku2Gabriela Marinova3Giovanni Savorana4Leo Eberl5Department of Plant and Microbial Biology, University of ZürichInstitute of Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH ZürichFaculty of Life and Environmental Sciences, Microbiology Research Center for Sustainability (MiCS), University of TsukubaDepartment of Plant and Microbial Biology, University of ZürichInstitute of Environmental Engineering, Department of Civil, Environmental and Geomatic Engineering, ETH ZürichDepartment of Plant and Microbial Biology, University of ZürichAbstract DNA is a component of biofilms, but the triggers of DNA release during biofilm formation and how DNA contributes to biofilm development are poorly investigated. One key mechanism involved in DNA release is explosive cell lysis, which is a consequence of prophage induction. In this article, the role of explosive cell lysis in biofilm formation was investigated in the opportunistic human pathogen Burkholderia cenocepacia H111 (H111). Biofilm streamers, flow-suspended biofilm filaments, were used as a biofilm model in this study, as DNA is an essential component of their matrix. H111 contains three prophages on chromosome 1 of its genome, and the involvement of each prophage in causing explosive cell lysis of the host and subsequent DNA and membrane vesicle (MV) release, as well as their contribution to streamer formation, were studied in the presence and absence of genotoxic stress. The results show that two of the three prophages of H111 encode functional lytic prophages that can be induced by genotoxic stress and their activation causes DNA and MVs release by explosive cell lysis. Furthermore, it is shown that the released DNA enables the strain to develop biofilm streamers, and streamer formation can be enhanced by genotoxic stress. Overall, this study demonstrates the involvement of prophages in streamer formation and uncovers an often-overlooked problem with the use of antibiotics that trigger the bacterial SOS response for the treatment of bacterial infections.https://doi.org/10.1038/s41522-023-00464-7 |
| spellingShingle | Zaira Heredia-Ponce Eleonora Secchi Masanori Toyofuku Gabriela Marinova Giovanni Savorana Leo Eberl Genotoxic stress stimulates eDNA release via explosive cell lysis and thereby promotes streamer formation of Burkholderia cenocepacia H111 cultured in a microfluidic device npj Biofilms and Microbiomes |
| title | Genotoxic stress stimulates eDNA release via explosive cell lysis and thereby promotes streamer formation of Burkholderia cenocepacia H111 cultured in a microfluidic device |
| title_full | Genotoxic stress stimulates eDNA release via explosive cell lysis and thereby promotes streamer formation of Burkholderia cenocepacia H111 cultured in a microfluidic device |
| title_fullStr | Genotoxic stress stimulates eDNA release via explosive cell lysis and thereby promotes streamer formation of Burkholderia cenocepacia H111 cultured in a microfluidic device |
| title_full_unstemmed | Genotoxic stress stimulates eDNA release via explosive cell lysis and thereby promotes streamer formation of Burkholderia cenocepacia H111 cultured in a microfluidic device |
| title_short | Genotoxic stress stimulates eDNA release via explosive cell lysis and thereby promotes streamer formation of Burkholderia cenocepacia H111 cultured in a microfluidic device |
| title_sort | genotoxic stress stimulates edna release via explosive cell lysis and thereby promotes streamer formation of burkholderia cenocepacia h111 cultured in a microfluidic device |
| url | https://doi.org/10.1038/s41522-023-00464-7 |
| work_keys_str_mv | AT zairaherediaponce genotoxicstressstimulatesednareleaseviaexplosivecelllysisandtherebypromotesstreamerformationofburkholderiacenocepaciah111culturedinamicrofluidicdevice AT eleonorasecchi genotoxicstressstimulatesednareleaseviaexplosivecelllysisandtherebypromotesstreamerformationofburkholderiacenocepaciah111culturedinamicrofluidicdevice AT masanoritoyofuku genotoxicstressstimulatesednareleaseviaexplosivecelllysisandtherebypromotesstreamerformationofburkholderiacenocepaciah111culturedinamicrofluidicdevice AT gabrielamarinova genotoxicstressstimulatesednareleaseviaexplosivecelllysisandtherebypromotesstreamerformationofburkholderiacenocepaciah111culturedinamicrofluidicdevice AT giovannisavorana genotoxicstressstimulatesednareleaseviaexplosivecelllysisandtherebypromotesstreamerformationofburkholderiacenocepaciah111culturedinamicrofluidicdevice AT leoeberl genotoxicstressstimulatesednareleaseviaexplosivecelllysisandtherebypromotesstreamerformationofburkholderiacenocepaciah111culturedinamicrofluidicdevice |