CzcR-dependent reduction of catalase gene expression and induction of catalase activity in Pseudomonas aeruginosa during zinc excess

Abstract Background Pseudomonas aeruginosa is able to survive, grow, and cause severe infections at different sites throughout the human body owing to its ability to sense diverse signals and precisely modulate target gene expression using its abundant signaling systems. Release of zinc (Zn) and hyd...

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Main Authors: Ting Li, Zhifeng Mo, Yuying Zhao, Huiluo Cao, Shuo Sheng, Zeling Xu
Format: Article
Language:English
Published: BMC 2024-11-01
Series:BMC Microbiology
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Online Access:https://doi.org/10.1186/s12866-024-03671-0
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author Ting Li
Zhifeng Mo
Yuying Zhao
Huiluo Cao
Shuo Sheng
Zeling Xu
author_facet Ting Li
Zhifeng Mo
Yuying Zhao
Huiluo Cao
Shuo Sheng
Zeling Xu
author_sort Ting Li
collection DOAJ
description Abstract Background Pseudomonas aeruginosa is able to survive, grow, and cause severe infections at different sites throughout the human body owing to its ability to sense diverse signals and precisely modulate target gene expression using its abundant signaling systems. Release of zinc (Zn) and hydrogen peroxide (H2O2) within the phagocyte are two major host strategies to defend against bacterial infections. It was previously shown that the response regulator CzcR controls global gene expression including catalase genes during Zn excess, but regulatory mechanisms of catalase gene expression and the role of CzcR in H2O2 tolerance remain unclear. Results In the study, comparative transcriptome analysis comprehensively described the CzcR-dependent and -independent gene regulatory pattern in P. aeruginosa during Zn excess, which revealed the counteractive co-regulation of two key H2O2-detoxifying catalase genes katA and katB through CzcR-dependent and -independent pathways in response to Zn excess. Protein-DNA interaction assay demonstrated that CzcR negatively regulates the expression of catalase genes katA and katB by directly binding to their promoters. While interestingly, we further showed that CzcR positively regulates H2O2 tolerance by inducing the catalase activity during Zn excess. Conclusion This study reported the opposite functions of CzcR in negatively regulating the expression of catalase genes katA and katB but in positively regulating the activity of catalase and H2O2 tolerance during Zn excess in P. aeruginosa.
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spelling doaj-art-8b0d0c2a7d2f49b2a8652363c13ac10f2024-12-01T12:12:38ZengBMCBMC Microbiology1471-21802024-11-0124111110.1186/s12866-024-03671-0CzcR-dependent reduction of catalase gene expression and induction of catalase activity in Pseudomonas aeruginosa during zinc excessTing Li0Zhifeng Mo1Yuying Zhao2Huiluo Cao3Shuo Sheng4Zeling Xu5Guangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural UniversityGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural UniversityGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural UniversityDepartment of Microbiology, Li Ka Shing Faculty of Medicine, The University of Hong KongKey Laboratory of Basic Pharmacology of the Ministry of Education, Joint International Research Laboratory of Ethnomedicine of the Ministry of Education and Key Laboratory of Basic Pharmacology of Guizhou Province, Zunyi Medical UniversityGuangdong Province Key Laboratory of Microbial Signals and Disease Control, Integrative Microbiology Research Centre, South China Agricultural UniversityAbstract Background Pseudomonas aeruginosa is able to survive, grow, and cause severe infections at different sites throughout the human body owing to its ability to sense diverse signals and precisely modulate target gene expression using its abundant signaling systems. Release of zinc (Zn) and hydrogen peroxide (H2O2) within the phagocyte are two major host strategies to defend against bacterial infections. It was previously shown that the response regulator CzcR controls global gene expression including catalase genes during Zn excess, but regulatory mechanisms of catalase gene expression and the role of CzcR in H2O2 tolerance remain unclear. Results In the study, comparative transcriptome analysis comprehensively described the CzcR-dependent and -independent gene regulatory pattern in P. aeruginosa during Zn excess, which revealed the counteractive co-regulation of two key H2O2-detoxifying catalase genes katA and katB through CzcR-dependent and -independent pathways in response to Zn excess. Protein-DNA interaction assay demonstrated that CzcR negatively regulates the expression of catalase genes katA and katB by directly binding to their promoters. While interestingly, we further showed that CzcR positively regulates H2O2 tolerance by inducing the catalase activity during Zn excess. Conclusion This study reported the opposite functions of CzcR in negatively regulating the expression of catalase genes katA and katB but in positively regulating the activity of catalase and H2O2 tolerance during Zn excess in P. aeruginosa.https://doi.org/10.1186/s12866-024-03671-0P. aeruginosaTwo-component systemCzcS/CzcRCatalaseOxidative tolerance
spellingShingle Ting Li
Zhifeng Mo
Yuying Zhao
Huiluo Cao
Shuo Sheng
Zeling Xu
CzcR-dependent reduction of catalase gene expression and induction of catalase activity in Pseudomonas aeruginosa during zinc excess
BMC Microbiology
P. aeruginosa
Two-component system
CzcS/CzcR
Catalase
Oxidative tolerance
title CzcR-dependent reduction of catalase gene expression and induction of catalase activity in Pseudomonas aeruginosa during zinc excess
title_full CzcR-dependent reduction of catalase gene expression and induction of catalase activity in Pseudomonas aeruginosa during zinc excess
title_fullStr CzcR-dependent reduction of catalase gene expression and induction of catalase activity in Pseudomonas aeruginosa during zinc excess
title_full_unstemmed CzcR-dependent reduction of catalase gene expression and induction of catalase activity in Pseudomonas aeruginosa during zinc excess
title_short CzcR-dependent reduction of catalase gene expression and induction of catalase activity in Pseudomonas aeruginosa during zinc excess
title_sort czcr dependent reduction of catalase gene expression and induction of catalase activity in pseudomonas aeruginosa during zinc excess
topic P. aeruginosa
Two-component system
CzcS/CzcR
Catalase
Oxidative tolerance
url https://doi.org/10.1186/s12866-024-03671-0
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