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The transcriptome response of Neisseria gonorrhoeae to hydrogen peroxide reveals genes with previously uncharacterized roles in oxidative damage protection.

ABSTRACT: Symptomatic gonococcal infection, caused by the pathogen Neisseria gonorrhoeae (Gc), is characterized by the influx of polymorphonuclear leukocytes (PMNs) to the site of infection. Although PMNs possess several mechanisms of oxidative killing, intact Gc can be found associated with PMNs, suggesting that gonococcal defences against oxidative stress are crucial for its ability to evade killing by PMNs. We used microarrays to identify genes that were differentially expressed after transient exposure of Gc to hydrogen peroxide (H2O2). Of the 75 genes found to be upregulated after H2O2 treatment, over one-quarter, including two of the most highly upregulated genes (NGO1686 and NGO554), were predicted to encode proteins with unknown functions. Further characterization of a subset of these upregulated genes demonstrated that NGO1686, a putative zinc metalloprotease, protects against oxidative damage caused by both H2O2 and cumene hydroperoxide, and that NGO554, a Gc-specific protein, acts to protect against damage caused by high levels of H2O2. Our current study also ascribes a role in H2O2 damage protection to recN, a gene previously characterized for its role in DNA repair. A PMN survival assay demonstrated that the recN and NGO1686 mutants were more susceptible to killing than the parent strain FA1090. These results define for the first time the robust transcriptional response to H2O2 by this strict human pathogen and underscore the importance of this system for survival to host defences.

SUBMITTER: Stohl EA

PROVIDER: S-EPMC2612779 | biostudies-literature | 2005 Oct

REPOSITORIES: biostudies-literature

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The transcriptome response of Neisseria gonorrhoeae to hydrogen peroxide reveals genes with previously uncharacterized roles in oxidative damage protection.

Stohl Elizabeth A EA Criss Alison K AK Seifert H Steven HS

Molecular microbiology 20051001 2

Symptomatic gonococcal infection, caused by the pathogen Neisseria gonorrhoeae (Gc), is characterized by the influx of polymorphonuclear leukocytes (PMNs) to the site of infection. Although PMNs possess several mechanisms of oxidative killing, intact Gc can be found associated with PMNs, suggesting that gonococcal defences against oxidative stress are crucial for its ability to evade killing by PMNs. We used microarrays to identify genes that were differentially expressed after transient exposur ...[more]

PMID: 16194237

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Project description:Carbon catabolite repression (CCR) is a gene regulation process that allows bacteria to use carbon-energy sources in a hierarchical manner. Thus, the presence of a preferred sugar, usually D-glucose, results in downregulation of genes participating in the transport and catabolic pathways of secondary carbon sources. Further, CCR controls the expression of global regulators that control expression of many genes involved in multiple aspects of bacterial physiology such as stress response proteins and virulence factors. The human-restricted pathogen Neisseria gonorrhoeae can rely upon a limited number of carbon-energy sources, including glucose and lactate and both are available within its infection niches. We recently reported that expression of the L-lactate permease-encoding gene lctP is subjected to glucose repression within physiological concentrations. However, the transducing mechanism or the gene that connect glucose with lctP promoter repression remained unknown. To address this issue, we performed an RNA-Seq analysis to determine the transcriptional landscape of gonococci due to changes in glucose or lactate concentrations in the growth media. Glucose was found to regulate 144 genes (5.5% of total genes in the genome) while lactate influenced the expression of 434 (16.5%) genes with an overlap of 97 genes between the two sugars. Both, glucose and lactate were found to upregulate genes involved in protein translation, a high energy consumption cellular function. Individually, glucose enhanced genes participating in glycolysis and repressed genes in the tricarboxylic acid (TCA) cycle, while lactate enhanced genes encoding respiratory enzymes and ATP synthase. Interestingly, lactate was found to repress expression of several genes encoding known gonococcal virulence factors such as tbpAB encoding the transferrin-binding proteins; the tonB and exbBD genes encoding the membrane energy transfer complex TonB-ExbB-ExbD required for many outer membrane transport systems; katA encoding an important H2O2-inducible catalase and to upregulate mtrR encoding the master repressor of the mtrCDE antimicrobial efflux pump genes. Moreover, glucose repressed mntC encoding a Zn/Mn ABC transporter and lctP, both required for resistance to killing by H2O2. These results set the framework to determine important gonococci virulent factor genes whose expression can be modulated by CCR as well as to discover the corresponding CCR regulators that control such genes.

Dataset Information

The transcriptome response of Neisseria gonorrhoeae to hydrogen peroxide reveals genes with previously uncharacterized roles in oxidative damage protection.

Publications

The transcriptome response of Neisseria gonorrhoeae to hydrogen peroxide reveals genes with previously uncharacterized roles in oxidative damage protection.

Similar Datasets

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