Insights into the diverse roles of the terminal oxidases in Burkholderia cenocepacia H111

Abstract Burkholderia cenocepacia H111 is an obligate aerobic bacterium which has been isolated from a cystic fibrosis (CF) patient. In CF lungs the environment is considered micro-oxic or even oxygen-depleted due to bacterial activities and limited oxygen diffusion in the mucus layer. To adapt to l...

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Main Authors: Sarah Paszti, Olivier Biner, Yilei Liu, Kim Bolli, Sarah Dorothy Jeggli, Gabriella Pessi, Leo Eberl
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-025-86211-8
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author Sarah Paszti
Olivier Biner
Yilei Liu
Kim Bolli
Sarah Dorothy Jeggli
Gabriella Pessi
Leo Eberl
author_facet Sarah Paszti
Olivier Biner
Yilei Liu
Kim Bolli
Sarah Dorothy Jeggli
Gabriella Pessi
Leo Eberl
author_sort Sarah Paszti
collection DOAJ
description Abstract Burkholderia cenocepacia H111 is an obligate aerobic bacterium which has been isolated from a cystic fibrosis (CF) patient. In CF lungs the environment is considered micro-oxic or even oxygen-depleted due to bacterial activities and limited oxygen diffusion in the mucus layer. To adapt to low oxygen concentrations, bacteria possess multiple terminal oxidases. In this study, we identified six terminal oxidases of B. cenocepacia H111 and constructed reporter strains to monitor their expression in different environments. While the heme-copper oxidase aa 3 (cta) was constitutively expressed, the bd-1 oxidase (cyd) was induced under oxygen-limited growth conditions. The cyanide-insensitive bd-type terminal oxidase (cio-1) was mainly expressed in cells grown on the surface of solid medium or in liquid cultures in presence of cyanide, which is known to be produced in the CF lung by the often co-residing CF pathogen Pseudomonas aeruginosa. Indeed, a cio-1 insertional mutant was not able to grow in the presence of cyanide confirming the important role of Cio-1 in cyanide resistance. The caa 3 oxidase (caa), was only expressed under nutrient limitation when cells were grown on the surface of solid medium. We also investigated the involvement of two regulatory systems, Anr and RoxS/RoxR, in the expression of cio-1 and cyd. Our data suggest, that, given that Cio-1 is only present in prokaryotes and plays an important role in the defense against cyanide-producing P. aeruginosa, it may be a valuable drug target for treatment of polymicrobial infections in CF patients.
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spelling doaj-art-04eddf5a7c904c2f8811ac02dfba25f92025-01-19T12:18:51ZengNature PortfolioScientific Reports2045-23222025-01-0115111210.1038/s41598-025-86211-8Insights into the diverse roles of the terminal oxidases in Burkholderia cenocepacia H111Sarah Paszti0Olivier Biner1Yilei Liu2Kim Bolli3Sarah Dorothy Jeggli4Gabriella Pessi5Leo Eberl6Department of Plant and Microbial Biology, University of ZurichDepartment of Plant and Microbial Biology, University of ZurichDepartment of Plant and Microbial Biology, University of ZurichDepartment of Plant and Microbial Biology, University of ZurichDepartment of Plant and Microbial Biology, University of ZurichDepartment of Plant and Microbial Biology, University of ZurichDepartment of Plant and Microbial Biology, University of ZurichAbstract Burkholderia cenocepacia H111 is an obligate aerobic bacterium which has been isolated from a cystic fibrosis (CF) patient. In CF lungs the environment is considered micro-oxic or even oxygen-depleted due to bacterial activities and limited oxygen diffusion in the mucus layer. To adapt to low oxygen concentrations, bacteria possess multiple terminal oxidases. In this study, we identified six terminal oxidases of B. cenocepacia H111 and constructed reporter strains to monitor their expression in different environments. While the heme-copper oxidase aa 3 (cta) was constitutively expressed, the bd-1 oxidase (cyd) was induced under oxygen-limited growth conditions. The cyanide-insensitive bd-type terminal oxidase (cio-1) was mainly expressed in cells grown on the surface of solid medium or in liquid cultures in presence of cyanide, which is known to be produced in the CF lung by the often co-residing CF pathogen Pseudomonas aeruginosa. Indeed, a cio-1 insertional mutant was not able to grow in the presence of cyanide confirming the important role of Cio-1 in cyanide resistance. The caa 3 oxidase (caa), was only expressed under nutrient limitation when cells were grown on the surface of solid medium. We also investigated the involvement of two regulatory systems, Anr and RoxS/RoxR, in the expression of cio-1 and cyd. Our data suggest, that, given that Cio-1 is only present in prokaryotes and plays an important role in the defense against cyanide-producing P. aeruginosa, it may be a valuable drug target for treatment of polymicrobial infections in CF patients.https://doi.org/10.1038/s41598-025-86211-8
spellingShingle Sarah Paszti
Olivier Biner
Yilei Liu
Kim Bolli
Sarah Dorothy Jeggli
Gabriella Pessi
Leo Eberl
Insights into the diverse roles of the terminal oxidases in Burkholderia cenocepacia H111
Scientific Reports
title Insights into the diverse roles of the terminal oxidases in Burkholderia cenocepacia H111
title_full Insights into the diverse roles of the terminal oxidases in Burkholderia cenocepacia H111
title_fullStr Insights into the diverse roles of the terminal oxidases in Burkholderia cenocepacia H111
title_full_unstemmed Insights into the diverse roles of the terminal oxidases in Burkholderia cenocepacia H111
title_short Insights into the diverse roles of the terminal oxidases in Burkholderia cenocepacia H111
title_sort insights into the diverse roles of the terminal oxidases in burkholderia cenocepacia h111
url https://doi.org/10.1038/s41598-025-86211-8
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