Environmental Burkholderia cenocepacia Strain Enhances Fitness by Serial Passages during Long-Term Chronic Airways Infection in Mice
Burkholderia cenocepacia is an important opportunistic pathogen in cystic fibrosis (CF) patients, and has also been isolated from natural environments. In previous work, we explored the virulence and pathogenic potential of environmental B. cenocepacia strains and demonstrated that they do not diffe...
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| Format: | Article |
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MDPI AG
2017-11-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/18/11/2417 |
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| author | Alessandra Bragonzi Moira Paroni Luisa Pirone Ivan Coladarci Fiorentina Ascenzioni Annamaria Bevivino |
| author_facet | Alessandra Bragonzi Moira Paroni Luisa Pirone Ivan Coladarci Fiorentina Ascenzioni Annamaria Bevivino |
| author_sort | Alessandra Bragonzi |
| collection | DOAJ |
| description | Burkholderia cenocepacia is an important opportunistic pathogen in cystic fibrosis (CF) patients, and has also been isolated from natural environments. In previous work, we explored the virulence and pathogenic potential of environmental B. cenocepacia strains and demonstrated that they do not differ from clinical strains in some pathogenic traits. Here, we investigated the ability of the environmental B. cenocepacia Mex1 strain, isolated from the maize rhizosphere, to persist and increase its virulence after serial passages in a mouse model of chronic infection. B. cenocepacia Mex1 strain, belonging to the recA lineage IIIA, was embedded in agar beads and challenged into the lung of C57Bl/6 mice. The mice were sacrificed after 28 days from infection and their lungs were tested for bacterial loads. Agar beads containing the pool of B. cenocepacia colonies from the four sequential passages were used to infect the mice. The environmental B. cenocepacia strain showed a low incidence of chronic infection after the first passage; after the second, third and fourth passages in mice, its ability to establish chronic infection increased significantly and progressively up to 100%. Colonial morphology analysis and genetic profiling of the Mex1-derived clones recovered after the fourth passage from infected mice revealed that they were indistinguishable from the challenged strain both at phenotypic and genetic level. By testing the virulence of single clones in the Galleria mellonella infection model, we found that two Mex1-derived clones significantly increased their pathogenicity compared to the parental Mex1 strain and behaved similarly to the clinical and epidemic B. cenocepacia LMG16656T. Our findings suggest that serial passages of the environmental B. cenocepacia Mex1 strain in mice resulted in an increased ability to determine chronic lung infection and the appearance of clonal variants with increased virulence in non-vertebrate hosts. |
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| issn | 1422-0067 |
| language | English |
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| spelling | doaj.art-4b6d946c7fa44b158d31c63b38b827ad2022-12-22T02:36:42ZengMDPI AGInternational Journal of Molecular Sciences1422-00672017-11-011811241710.3390/ijms18112417ijms18112417Environmental Burkholderia cenocepacia Strain Enhances Fitness by Serial Passages during Long-Term Chronic Airways Infection in MiceAlessandra Bragonzi0Moira Paroni1Luisa Pirone2Ivan Coladarci3Fiorentina Ascenzioni4Annamaria Bevivino5Infections and Cystic Fibrosis Unit, IRCCS San Raffaele Scientific Institute, 20132 Milan, ItalyInfections and Cystic Fibrosis Unit, IRCCS San Raffaele Scientific Institute, 20132 Milan, ItalyTerritorial and Production Systems Sustainability Department, ENEA, Italian National Agency for New Technologies, Energy and Sustainable Economic Development, Casaccia Research Center, 00123 Rome, ItalyBiology and Biotechnology Department “Charles Darwin”, Sapienza University of Rome, 00185 Rome, ItalyBiology and Biotechnology Department “Charles Darwin”, Sapienza University of Rome, 00185 Rome, ItalyTerritorial and Production Systems Sustainability Department, ENEA, Italian National Agency for New Technologies, Energy and Sustainable Economic Development, Casaccia Research Center, 00123 Rome, ItalyBurkholderia cenocepacia is an important opportunistic pathogen in cystic fibrosis (CF) patients, and has also been isolated from natural environments. In previous work, we explored the virulence and pathogenic potential of environmental B. cenocepacia strains and demonstrated that they do not differ from clinical strains in some pathogenic traits. Here, we investigated the ability of the environmental B. cenocepacia Mex1 strain, isolated from the maize rhizosphere, to persist and increase its virulence after serial passages in a mouse model of chronic infection. B. cenocepacia Mex1 strain, belonging to the recA lineage IIIA, was embedded in agar beads and challenged into the lung of C57Bl/6 mice. The mice were sacrificed after 28 days from infection and their lungs were tested for bacterial loads. Agar beads containing the pool of B. cenocepacia colonies from the four sequential passages were used to infect the mice. The environmental B. cenocepacia strain showed a low incidence of chronic infection after the first passage; after the second, third and fourth passages in mice, its ability to establish chronic infection increased significantly and progressively up to 100%. Colonial morphology analysis and genetic profiling of the Mex1-derived clones recovered after the fourth passage from infected mice revealed that they were indistinguishable from the challenged strain both at phenotypic and genetic level. By testing the virulence of single clones in the Galleria mellonella infection model, we found that two Mex1-derived clones significantly increased their pathogenicity compared to the parental Mex1 strain and behaved similarly to the clinical and epidemic B. cenocepacia LMG16656T. Our findings suggest that serial passages of the environmental B. cenocepacia Mex1 strain in mice resulted in an increased ability to determine chronic lung infection and the appearance of clonal variants with increased virulence in non-vertebrate hosts.https://www.mdpi.com/1422-0067/18/11/2417Burkholderia cenocepaciamiceenvironmentalchronic infectionadaptationlung tissuesGalleria mellonella |
| spellingShingle | Alessandra Bragonzi Moira Paroni Luisa Pirone Ivan Coladarci Fiorentina Ascenzioni Annamaria Bevivino Environmental Burkholderia cenocepacia Strain Enhances Fitness by Serial Passages during Long-Term Chronic Airways Infection in Mice International Journal of Molecular Sciences Burkholderia cenocepacia mice environmental chronic infection adaptation lung tissues Galleria mellonella |
| title | Environmental Burkholderia cenocepacia Strain Enhances Fitness by Serial Passages during Long-Term Chronic Airways Infection in Mice |
| title_full | Environmental Burkholderia cenocepacia Strain Enhances Fitness by Serial Passages during Long-Term Chronic Airways Infection in Mice |
| title_fullStr | Environmental Burkholderia cenocepacia Strain Enhances Fitness by Serial Passages during Long-Term Chronic Airways Infection in Mice |
| title_full_unstemmed | Environmental Burkholderia cenocepacia Strain Enhances Fitness by Serial Passages during Long-Term Chronic Airways Infection in Mice |
| title_short | Environmental Burkholderia cenocepacia Strain Enhances Fitness by Serial Passages during Long-Term Chronic Airways Infection in Mice |
| title_sort | environmental burkholderia cenocepacia strain enhances fitness by serial passages during long term chronic airways infection in mice |
| topic | Burkholderia cenocepacia mice environmental chronic infection adaptation lung tissues Galleria mellonella |
| url | https://www.mdpi.com/1422-0067/18/11/2417 |
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