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Gene and Protein Expression in Response to Different Growth Temperatures and Oxygen Availability in Burkholderia thailandensis

Burkholderia thailandensis, although normally avirulent for mammals, can infect macrophages in vitro and has occasionally been reported to cause pneumonia in humans. It is therefore used as a model organism for the human pathogen B. pseudomallei, to which it is closely related phylogenetically. We c...

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Autores principales: Peano, Clelia, Chiaramonte, Fabrizio, Motta, Sara, Pietrelli, Alessandro, Jaillon, Sebastien, Rossi, Elio, Consolandi, Clarissa, Champion, Olivia L., Michell, Stephen L., Freddi, Luca, Falciola, Luigi, Basilico, Fabrizio, Garlanda, Cecilia, Mauri, Pierluigi, De Bellis, Gianluca, Landini, Paolo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3966863/
https://www.ncbi.nlm.nih.gov/pubmed/24671187
http://dx.doi.org/10.1371/journal.pone.0093009
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author Peano, Clelia
Chiaramonte, Fabrizio
Motta, Sara
Pietrelli, Alessandro
Jaillon, Sebastien
Rossi, Elio
Consolandi, Clarissa
Champion, Olivia L.
Michell, Stephen L.
Freddi, Luca
Falciola, Luigi
Basilico, Fabrizio
Garlanda, Cecilia
Mauri, Pierluigi
De Bellis, Gianluca
Landini, Paolo
author_facet Peano, Clelia
Chiaramonte, Fabrizio
Motta, Sara
Pietrelli, Alessandro
Jaillon, Sebastien
Rossi, Elio
Consolandi, Clarissa
Champion, Olivia L.
Michell, Stephen L.
Freddi, Luca
Falciola, Luigi
Basilico, Fabrizio
Garlanda, Cecilia
Mauri, Pierluigi
De Bellis, Gianluca
Landini, Paolo
author_sort Peano, Clelia
collection PubMed
description Burkholderia thailandensis, although normally avirulent for mammals, can infect macrophages in vitro and has occasionally been reported to cause pneumonia in humans. It is therefore used as a model organism for the human pathogen B. pseudomallei, to which it is closely related phylogenetically. We characterized the B. thailandensis clinical isolate CDC2721121 (BtCDC272) at the genome level and studied its response to environmental cues associated with human host colonization, namely, temperature and oxygen limitation. Effects of the different growth conditions on BtCDC272 were studied through whole genome transcription studies and analysis of proteins associated with the bacterial cell surface. We found that growth at 37°C, compared to 28°C, negatively affected cell motility and flagella production through a mechanism involving regulation of the flagellin-encoding fliC gene at the mRNA stability level. Growth in oxygen-limiting conditions, in contrast, stimulated various processes linked to virulence, such as lipopolysaccharide production and expression of genes encoding protein secretion systems. Consistent with these observations, BtCDC272 grown in oxygen limitation was more resistant to phagocytosis and strongly induced the production of inflammatory cytokines from murine macrophages. Our results suggest that, while temperature sensing is important for regulation of B. thailandensis cell motility, oxygen limitation has a deeper impact on its physiology and constitutes a crucial environmental signal for the production of virulence factors.
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spelling pubmed-39668632014-03-31 Gene and Protein Expression in Response to Different Growth Temperatures and Oxygen Availability in Burkholderia thailandensis Peano, Clelia Chiaramonte, Fabrizio Motta, Sara Pietrelli, Alessandro Jaillon, Sebastien Rossi, Elio Consolandi, Clarissa Champion, Olivia L. Michell, Stephen L. Freddi, Luca Falciola, Luigi Basilico, Fabrizio Garlanda, Cecilia Mauri, Pierluigi De Bellis, Gianluca Landini, Paolo PLoS One Research Article Burkholderia thailandensis, although normally avirulent for mammals, can infect macrophages in vitro and has occasionally been reported to cause pneumonia in humans. It is therefore used as a model organism for the human pathogen B. pseudomallei, to which it is closely related phylogenetically. We characterized the B. thailandensis clinical isolate CDC2721121 (BtCDC272) at the genome level and studied its response to environmental cues associated with human host colonization, namely, temperature and oxygen limitation. Effects of the different growth conditions on BtCDC272 were studied through whole genome transcription studies and analysis of proteins associated with the bacterial cell surface. We found that growth at 37°C, compared to 28°C, negatively affected cell motility and flagella production through a mechanism involving regulation of the flagellin-encoding fliC gene at the mRNA stability level. Growth in oxygen-limiting conditions, in contrast, stimulated various processes linked to virulence, such as lipopolysaccharide production and expression of genes encoding protein secretion systems. Consistent with these observations, BtCDC272 grown in oxygen limitation was more resistant to phagocytosis and strongly induced the production of inflammatory cytokines from murine macrophages. Our results suggest that, while temperature sensing is important for regulation of B. thailandensis cell motility, oxygen limitation has a deeper impact on its physiology and constitutes a crucial environmental signal for the production of virulence factors. Public Library of Science 2014-03-26 /pmc/articles/PMC3966863/ /pubmed/24671187 http://dx.doi.org/10.1371/journal.pone.0093009 Text en © 2014 Peano et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Peano, Clelia
Chiaramonte, Fabrizio
Motta, Sara
Pietrelli, Alessandro
Jaillon, Sebastien
Rossi, Elio
Consolandi, Clarissa
Champion, Olivia L.
Michell, Stephen L.
Freddi, Luca
Falciola, Luigi
Basilico, Fabrizio
Garlanda, Cecilia
Mauri, Pierluigi
De Bellis, Gianluca
Landini, Paolo
Gene and Protein Expression in Response to Different Growth Temperatures and Oxygen Availability in Burkholderia thailandensis
title Gene and Protein Expression in Response to Different Growth Temperatures and Oxygen Availability in Burkholderia thailandensis
title_full Gene and Protein Expression in Response to Different Growth Temperatures and Oxygen Availability in Burkholderia thailandensis
title_fullStr Gene and Protein Expression in Response to Different Growth Temperatures and Oxygen Availability in Burkholderia thailandensis
title_full_unstemmed Gene and Protein Expression in Response to Different Growth Temperatures and Oxygen Availability in Burkholderia thailandensis
title_short Gene and Protein Expression in Response to Different Growth Temperatures and Oxygen Availability in Burkholderia thailandensis
title_sort gene and protein expression in response to different growth temperatures and oxygen availability in burkholderia thailandensis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3966863/
https://www.ncbi.nlm.nih.gov/pubmed/24671187
http://dx.doi.org/10.1371/journal.pone.0093009
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