Ahp deficiency-induced redox imbalance leads to metabolic alterations in E. coli
Alkyl hydroperoxide reductase (Ahp) is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli (E. coli). Ahp-deficient strains have been found to have high reactive oxygen species (ROS) levels, sufficient to cause cell damage. However, the exact role and underlying mechanisms of A...
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| Format: | Article |
| Language: | English |
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Elsevier
2023-11-01
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| Series: | Redox Biology |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2213231723002896 |
| _version_ | 1797647928124243968 |
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| author | Feng Liu Penggang Han Nuomin Li Yongqian Zhang |
| author_facet | Feng Liu Penggang Han Nuomin Li Yongqian Zhang |
| author_sort | Feng Liu |
| collection | DOAJ |
| description | Alkyl hydroperoxide reductase (Ahp) is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli (E. coli). Ahp-deficient strains have been found to have high reactive oxygen species (ROS) levels, sufficient to cause cell damage. However, the exact role and underlying mechanisms of Ahp deficiency-induced cell damage remain largely unknown. Here, the E. coli MG1655 ΔAhp mutant strain was constructed as a model of deficiency to assess its role. The cells of the ΔAhp strain were found to be significantly longer than those of the wild strain, with elevated ROS and hydrogen peroxide (H2O2) levels. Proteome, redox proteome and metabolome analyses were performed to systematically present a global and quantitative profile and delineate the redox signaling and metabolic alterations at the proteome, metabolome, and cysteine oxidation site levels. The multiomics data revealed that Ahp deficiency disrupted the redox balance, activated the OxyR system, upregulated oxidative defense proteins and inhibited the TCA cycle to some extent. Surprisingly, the mutant strain shifted from aerobic respiration to anaerobic respiration and fermentation during the logarithmic phase in the presence of sufficient O2. The acid resistance system was activated to mitigate the effect of excessive acid produced by fermentation. Taken together, the results of this study demonstrated that Ahp deficiency triggered cellular redox imbalance and regulated metabolic pathways to confer resistance to submicromolar intracellular H2O2 levels in E. coli. |
| first_indexed | 2024-03-11T15:24:44Z |
| format | Article |
| id | doaj.art-f2e13288e6dc4e88b722c3b0c42254ac |
| institution | Directory Open Access Journal |
| issn | 2213-2317 |
| language | English |
| last_indexed | 2024-03-11T15:24:44Z |
| publishDate | 2023-11-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Redox Biology |
| spelling | doaj.art-f2e13288e6dc4e88b722c3b0c42254ac2023-10-28T05:07:11ZengElsevierRedox Biology2213-23172023-11-0167102888Ahp deficiency-induced redox imbalance leads to metabolic alterations in E. coliFeng Liu0Penggang Han1Nuomin Li2Yongqian Zhang3School of Medical Technology, Beijing Institute of Technology, Beijing, 100081, ChinaState Key Laboratory of NBC Protection for Civilian, Beijing, ChinaSchool of Medical Technology, Beijing Institute of Technology, Beijing, 100081, ChinaSchool of Medical Technology, Beijing Institute of Technology, Beijing, 100081, China; Corresponding author.Alkyl hydroperoxide reductase (Ahp) is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli (E. coli). Ahp-deficient strains have been found to have high reactive oxygen species (ROS) levels, sufficient to cause cell damage. However, the exact role and underlying mechanisms of Ahp deficiency-induced cell damage remain largely unknown. Here, the E. coli MG1655 ΔAhp mutant strain was constructed as a model of deficiency to assess its role. The cells of the ΔAhp strain were found to be significantly longer than those of the wild strain, with elevated ROS and hydrogen peroxide (H2O2) levels. Proteome, redox proteome and metabolome analyses were performed to systematically present a global and quantitative profile and delineate the redox signaling and metabolic alterations at the proteome, metabolome, and cysteine oxidation site levels. The multiomics data revealed that Ahp deficiency disrupted the redox balance, activated the OxyR system, upregulated oxidative defense proteins and inhibited the TCA cycle to some extent. Surprisingly, the mutant strain shifted from aerobic respiration to anaerobic respiration and fermentation during the logarithmic phase in the presence of sufficient O2. The acid resistance system was activated to mitigate the effect of excessive acid produced by fermentation. Taken together, the results of this study demonstrated that Ahp deficiency triggered cellular redox imbalance and regulated metabolic pathways to confer resistance to submicromolar intracellular H2O2 levels in E. coli.http://www.sciencedirect.com/science/article/pii/S2213231723002896Alkyl hydroperoxide reductaseLabel-free proteomicsMetabolic alterationsRedox proteomicsMetabolomics |
| spellingShingle | Feng Liu Penggang Han Nuomin Li Yongqian Zhang Ahp deficiency-induced redox imbalance leads to metabolic alterations in E. coli Redox Biology Alkyl hydroperoxide reductase Label-free proteomics Metabolic alterations Redox proteomics Metabolomics |
| title | Ahp deficiency-induced redox imbalance leads to metabolic alterations in E. coli |
| title_full | Ahp deficiency-induced redox imbalance leads to metabolic alterations in E. coli |
| title_fullStr | Ahp deficiency-induced redox imbalance leads to metabolic alterations in E. coli |
| title_full_unstemmed | Ahp deficiency-induced redox imbalance leads to metabolic alterations in E. coli |
| title_short | Ahp deficiency-induced redox imbalance leads to metabolic alterations in E. coli |
| title_sort | ahp deficiency induced redox imbalance leads to metabolic alterations in e coli |
| topic | Alkyl hydroperoxide reductase Label-free proteomics Metabolic alterations Redox proteomics Metabolomics |
| url | http://www.sciencedirect.com/science/article/pii/S2213231723002896 |
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