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

Abstract

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.

Culturomics of Bacteria from Radon-Saturated Water of the World’s Oldest Radium Mine

“…Similarly, antioxidant genes such as those encoding catalase-peroxidase ( P ≤ 0.05) and the superoxide dismutase-Cu-Zn family ( P ≤ 0.001) were also positively correlated with tolerance of menadione. The presence of diverse catalases, peroxidases, superoxide dismutases, and glutathione peroxidases has been extensively reported to reduce the deleterious impact of oxidative stress on macromolecules ( 102 – 107 ). Additionally, a positive correlation between hydrogen peroxide or menadione tolerance and the presence of genes encoding MutL, MutS (DNA mismatch repair protein) ( P ≤ 0.05 and P ≤ 0.001, respectively) emphasize the role of DNA repair in the adaption to this stress ( 95 ).…”

Loss of 2‐Cys‐Prx affects cellular ultrastructure, disturbs redox poise and impairs photosynthesis in cyanobacteria

“…In E. coli and Yersinia pseudotuberculosis, in the absence of catalase activity, the AhpC protein (homologous to Alr4641) scavenges the endogenously generated H 2 O 2 produced during aerobic growth, but when catalases are present, the ahpC mutant shows no obvious phenotype (Seaver & Imlay, 2001;Wan et al, 2021).…”

“…In E. coli and Yersinia pseudotuberculosis , in the absence of catalase activity, the AhpC protein (homologous to Alr4641) scavenges the endogenously generated H 2 O 2 produced during aerobic growth, but when catalases are present, the ahpC mutant shows no obvious phenotype (Seaver & Imlay, 2001; Wan et al, 2021). In Synechococcus PCC 7942 too, due to the presence of active catalase (KatG), the 2‐Cys‐Prx mutant (tplAΩ) did not show any obvious phenotype during conditions of normal growth or when subjected to treatment with H 2 O 2 (Perelman et al, 2003).…”

Bacterioferritin: a key iron storage modulator that affects strain growth and butenyl-spinosyn biosynthesis in Saccharopolyspora pogona

“…TrxB can form an antioxidant system with Txr/NADPH to eliminate superoxide [ 38 ]. SOD is a kind of antioxidant metal enzymes, which can catalyze the disproportionation of superoxide anion radicals to generate O 2 and H 2 O 2 , while KatG can decompose H 2 O 2 to relieve the threat of oxidative damage to cells [ 39 , 49 ]. The catalytic activity of these enzymes, such as ferredoxin and SOD, often requires the participation of iron [ 40 ].…”