Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Bragonzi, Alessandra, Paroni, Moira, Pirone, Luisa, Coladarci, Ivan, Ascenzioni, Fiorentina, Bevivino, Annamaria
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5713385/
https://www.ncbi.nlm.nih.gov/pubmed/29135920
http://dx.doi.org/10.3390/ijms18112417
_version_ 1783283412848607232
author Bragonzi, Alessandra
Paroni, Moira
Pirone, Luisa
Coladarci, Ivan
Ascenzioni, Fiorentina
Bevivino, Annamaria
author_facet Bragonzi, Alessandra
Paroni, Moira
Pirone, Luisa
Coladarci, Ivan
Ascenzioni, Fiorentina
Bevivino, Annamaria
author_sort Bragonzi, Alessandra
collection PubMed
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 LMG16656(T). 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.
format Online
Article
Text
id pubmed-5713385
institution National Center for Biotechnology Information
language English
publishDate 2017
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-57133852017-12-07 Environmental Burkholderia cenocepacia Strain Enhances Fitness by Serial Passages during Long-Term Chronic Airways Infection in Mice Bragonzi, Alessandra Paroni, Moira Pirone, Luisa Coladarci, Ivan Ascenzioni, Fiorentina Bevivino, Annamaria Int J Mol Sci Article 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 LMG16656(T). 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. MDPI 2017-11-14 /pmc/articles/PMC5713385/ /pubmed/29135920 http://dx.doi.org/10.3390/ijms18112417 Text en © 2017 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Bragonzi, Alessandra
Paroni, Moira
Pirone, Luisa
Coladarci, Ivan
Ascenzioni, Fiorentina
Bevivino, Annamaria
Environmental Burkholderia cenocepacia Strain Enhances Fitness by Serial Passages during Long-Term Chronic Airways Infection in Mice
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 Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5713385/
https://www.ncbi.nlm.nih.gov/pubmed/29135920
http://dx.doi.org/10.3390/ijms18112417
work_keys_str_mv AT bragonzialessandra environmentalburkholderiacenocepaciastrainenhancesfitnessbyserialpassagesduringlongtermchronicairwaysinfectioninmice
AT paronimoira environmentalburkholderiacenocepaciastrainenhancesfitnessbyserialpassagesduringlongtermchronicairwaysinfectioninmice
AT pironeluisa environmentalburkholderiacenocepaciastrainenhancesfitnessbyserialpassagesduringlongtermchronicairwaysinfectioninmice
AT coladarciivan environmentalburkholderiacenocepaciastrainenhancesfitnessbyserialpassagesduringlongtermchronicairwaysinfectioninmice
AT ascenzionifiorentina environmentalburkholderiacenocepaciastrainenhancesfitnessbyserialpassagesduringlongtermchronicairwaysinfectioninmice
AT bevivinoannamaria environmentalburkholderiacenocepaciastrainenhancesfitnessbyserialpassagesduringlongtermchronicairwaysinfectioninmice