Distinct Roles of Shewanella oneidensis Thioredoxin in Regulation of Cellular Responses to Hydrogen and Organic Peroxides

Xue, Feng; Sun, Weining; Kong, Linggen; Gao, Haichun

doi:10.1128/aem.01700-19

Cited by 15 publications

(12 citation statements)

References 52 publications

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“…This was largely achieved in the dsbD-negative background. In S. oneidensis, DsbD is the only thiol:disulfide interchange protein that passes electrons from cytoplasmic Trx1 to CCM for the reduction of oxidized apocyts c (56). In the absence of DsbD, maturation can occur only on apocyts c with free thiol groups resulting from the depletion of DsbA proteins, eliminating the interference from those that are oxidized independently of DsbA proteins.…”

Section: Discussionmentioning

confidence: 99%

Complex Oxidation of Apocytochromes c during Bacterial Cytochrome c Maturation

Guo

Wang

et al. 2019

Appl Environ Microbiol

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c-Type cytochromes (cyts c) are proteins that contain covalently bound heme and that thus require posttranslational modification for activity, a process carried out by the cytochrome c (cyt c) maturation system (referred to as the Ccm system) in many Gram-negative bacteria. It has been established that during cyt c maturation (CCM), two cysteine thiols of the heme binding motif (CXXCH) within apocytochromes c (apocyts c) are first oxidized largely by DsbA to form a disulfide bond, which is later reduced through a thio-reductive pathway involving DsbD. However, the physiological impacts of DsbA proteins on CCM in fact vary significantly among bacteria. In this work, we used the cyt c-rich Gram-negative bacterium Shewanella oneidensis as the research model to clarify the roles of DsbA proteins in CCM. We show that in terms of the oxidation of apocyts c, DsbA proteins are an important but not critical factor, and, strikingly, oxygen is not either. By exploiting the DsbD-independent pathway, we identify DsbA1, DsbA2, and DsbA3 as oxidants contributing to the oxidation of apocyts c and reductants, such as cysteine, to be an effective antagonist against DsbA-independent oxidation. We further show that DsbB proteins are partially responsible for the reoxidization of reduced DsbA proteins. Overall, our results indicate that the DsbA-DsbB redox pair has a limited role in CCM, challenging the established notion that it is the main oxidant for apocyts c. IMPORTANCE DsbA is a powerful oxidase that functions in the bacterial periplasm to introduce disulfide bonds in many proteins, including apocytochromes c. It has been well established that although DsbA is not essential, it plays a primary role in cytochrome c maturation, based on studies in bacteria hosting several cyts c. Here, with cyt c-rich S. oneidensis as a research model, we show that this is not always the case. Moreover, we demonstrate that DsbB is also not essential for cytochrome c maturation. These results underscore the need to identify oxidants other than DsbA/DsbB that are crucial in the oxidation of apocyts c in bacteria.

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Section: Discussionmentioning

confidence: 99%

Complex Oxidation of Apocytochromes c during Bacterial Cytochrome c Maturation

Guo

Wang

et al. 2019

Appl Environ Microbiol

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“…Intracellular sulfur homeostasis should be carefully maintained because H 2 S and cysteine in vast excess promote oxidative damages by inhibiting catalases (Park and Imlay, 2003;Wu et al, 2015). Consistently, all components of thiol-based antioxidant systems of YPIII are most highly induced upon exposure to H 2 O 2 , conceivably requiring an active metabolism and fast shuttling of sulfur species (Feng et al, 2019). In parallel, genes for iron/manganese transport system are highly induced by exogenous H 2 O 2 .…”

Section: Discussionmentioning

confidence: 98%

“…Other putative OxyR regulon members that were induced but not among the top 10 included katG, trxB, ahpC, and sufABC (Fe-S cluster assembly proteins; Table 2). Intriguingly, the entire thioredoxin and glutathione antioxidant systems, which play a supporting role in combating oxidative stress in many bacteria (Feng et al, 2019), were found to be highly induced by H 2 O 2 (for instance, YPK_RS20590 was induced 689-fold), implying that these systems may have more significant contribution in protecting YPIII cells from oxidative damage. It is also worth mentioning that the oxyR gene was transcribed at substantially elevated levels (4.5-fold) upon H 2 O 2 stress (Table 2), suggesting that the regulator per se is also subjected to quantity control, in addition to activity transformation upon oxidation.…”

Section: Transcriptomics Analysis Of Ypiii In Response To H 2 O 2 Stressmentioning

confidence: 99%

Distinct H2O2-Scavenging System in Yersinia pseudotuberculosis: KatG and AhpC Act Together to Scavenge Endogenous Hydrogen Peroxide

et al. 2021

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To colonize in the digestive tract of animals and humans, Yersinia pseudotuberculosis has to deal with reactive oxygen species (ROS) produced by host cells and microbiota. However, an understanding of the ROS-scavenging systems and their regulation in this bacterium remains largely elusive. In this study, we identified OxyR as the master transcriptional regulator mediating cellular responses to hydrogen peroxide (H2O2) in Y. pseudotuberculosis through genomics and transcriptomics analyses. OxyR activates transcription of diverse genes, especially the core members of its regulon, including those encoding catalases, peroxidases, and thiol reductases. The data also suggest that sulfur species and manganese may play a particular role in the oxidative stress response of Y. pseudotuberculosis. Among the three H2O2-scavenging systems in Y. pseudotuberculosis, catalase/peroxidase KatE functions as the primary scavenger for high levels of H2O2; NADH peroxidase alkyl hydroperoxide reductase (AhpR) and catalase KatG together are responsible for removing low levels of H2O2. The simultaneous loss of both AhpC (the peroxidatic component of AhpR) and KatG results in activation of OxyR. Moreover, we found that AhpC, unlike its well-characterized Escherichia coli counterpart, has little effect on protecting cells against toxicity of organic peroxides. These findings provide not only novel insights into the structural and functional diversity of bacterial H2O2-scavenging systems but also a basic understanding of how Y. pseudotuberculosis copes with oxidative stress.

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“…strain CF-1 confer more protection to E. coli when exposed to oxidative conditions with ferric iron than does the endogenous gene trxA. As mentioned above, the TrxA protein from E. coli is a thioredoxin directly related to oxidative protection [7,57].…”

Section: The Expression Of Tfp Genes From Leptospirillum Sp Cf-1 Is mentioning

confidence: 97%

“…In addition to reducing cytoplasmic proteins, thioredoxins are indirectly involved in reducing endogenously-or exogenously-produced inorganic and organic peroxides. In this way, they provide reducing equivalents to thiol-based peroxiredoxins that are responsible for peroxide scavenging activity [6,7].…”

Section: Introductionmentioning

confidence: 99%

Deciphering the Role of Multiple Thioredoxin Fold Proteins of Leptospirillum sp. in Oxidative Stress Tolerance

González

Álamos

Rivero

et al. 2020

IJMS

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Thioredoxin fold proteins (TFPs) form a family of diverse proteins involved in thiol/disulfide exchange in cells from all domains of life. Leptospirillum spp. are bioleaching bacteria naturally exposed to extreme conditions like acidic pH and high concentrations of metals that can contribute to the generation of reactive oxygen species (ROS) and consequently the induction of thiol oxidative damage. Bioinformatic studies have predicted 13 genes that encode for TFP proteins in Leptospirillum spp. We analyzed the participation of individual tfp genes from Leptospirillum sp. CF-1 in the response to oxidative conditions. Genomic context analysis predicted the involvement of these genes in the general thiol-reducing system, cofactor biosynthesis, carbon fixation, cytochrome c biogenesis, signal transduction, and pilus and fimbria assembly. All tfp genes identified were transcriptionally active, although they responded differentially to ferric sulfate and diamide stress. Some of these genes confer oxidative protection to a thioredoxin-deficient Escherichia coli strain by restoring the wild-type phenotype under oxidative stress conditions. These findings contribute to our understanding of the diversity and complexity of thiol/disulfide systems, and of adaptations that emerge in acidophilic microorganisms that allow them to thrive in highly oxidative environments. These findings also give new insights into the physiology of these microorganisms during industrial bioleaching operations.

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Distinct Roles of Shewanella oneidensis Thioredoxin in Regulation of Cellular Responses to Hydrogen and Organic Peroxides

Cited by 15 publications

References 52 publications

Complex Oxidation of Apocytochromes c during Bacterial Cytochrome c Maturation

Complex Oxidation of Apocytochromes c during Bacterial Cytochrome c Maturation

Distinct H2O2-Scavenging System in Yersinia pseudotuberculosis: KatG and AhpC Act Together to Scavenge Endogenous Hydrogen Peroxide

Deciphering the Role of Multiple Thioredoxin Fold Proteins of Leptospirillum sp. in Oxidative Stress Tolerance

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