Mutations of ferric uptake regulator (fur) impair iron homeostasis, growth, oxidative stress survival, and virulence of Xanthomonas campestris pv. campestris

Jittawuttipoka, Thichakorn; Sallabhan, Ratiboot; Vattanaviboon, Paiboon; Fuangthong, Mayuree; Mongkolsuk, Skorn

doi:10.1007/s00203-010-0558-8

Cited by 42 publications

(42 citation statements)

References 54 publications

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“…Previous reports revealed that Fur is a critical cytoplasmic regulator of iron homeostasis in X . campestris as in other bacteria [16, 27]. Our study revealed that in X .…”

Section: Discussionsupporting

confidence: 59%

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Two-Component Signaling System VgrRS Directly Senses Extracytoplasmic and Intracellular Iron to Control Bacterial Adaptation under Iron Depleted Stress

et al. 2016

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Both iron starvation and excess are detrimental to cellular life, especially for animal and plant pathogens since they always live in iron-limited environments produced by host immune responses. However, how organisms sense and respond to iron is incompletely understood. Herein, we reveal that in the phytopathogenic bacterium Xanthomonas campestris pv. campestris, VgrS (also named ColS) is a membrane-bound receptor histidine kinase that senses extracytoplasmic iron limitation in the periplasm, while its cognate response regulator, VgrR (ColR), detects intracellular iron excess. Under iron-depleted conditions, dissociation of Fe3+ from the periplasmic sensor region of VgrS activates the VgrS autophosphorylation and subsequent phosphotransfer to VgrR, an OmpR-family transcription factor that regulates bacterial responses to take up iron. VgrR-VgrS regulon and the consensus DNA binding motif of the transcription factor VgrR were dissected by comparative proteomic and ChIP-seq analyses, which revealed that in reacting to iron-depleted environments, VgrR directly or indirectly controls the expressions of hundreds of genes that are involved in various physiological cascades, especially those associated with iron-uptake. Among them, we demonstrated that the phosphorylated VgrR tightly represses the transcription of a special TonB-dependent receptor gene, tdvA. This regulation is a critical prerequisite for efficient iron uptake and bacterial virulence since activation of tdvA transcription is detrimental to these processes. When the intracellular iron accumulates, the VgrR-Fe2+ interaction dissociates not only the binding between VgrR and the tdvA promoter, but also the interaction between VgrR and VgrS. This relieves the repression in tdvA transcription to impede continuous iron uptake and avoids possible toxic effects of excessive iron accumulation. Our results revealed a signaling system that directly senses both extracytoplasmic and intracellular iron to modulate bacterial iron homeostasis.

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“…Previous reports revealed that Fur is a critical cytoplasmic regulator of iron homeostasis in X . campestris as in other bacteria [16, 27]. Our study revealed that in X .…”

Section: Discussionsupporting

confidence: 59%

“…campestris pv. campestris resulted in increased production of siderophores, reduced resistance to oxidative stress and decreased virulence [16]. Recently, a two-component signal transduction system, VgrR–VgrS (also named ColR-ColS), was identified as a canonical modulator controlling virulence of X .…”

Section: Introductionmentioning

confidence: 99%

Two-Component Signaling System VgrRS Directly Senses Extracytoplasmic and Intracellular Iron to Control Bacterial Adaptation under Iron Depleted Stress

et al. 2016

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“…Endpoint reverse transcription-PCR (RT-PCR) was carried out as previously described (31) to determine the expression level of tpx in P. aeruginosa under exposure to oxidative stress. Total RNA samples were isolated from the exponential-phase cultures of PAO1 induced with 250 M H 2 O 2 , CHP, menadione (MD), plumbagin (PB), or 100 M N-ethylmaleimide (NEM) for 20 min.…”

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confidence: 99%

“…Total RNA samples were isolated from the exponential-phase cultures of PAO1 induced with 250 M H 2 O 2 , CHP, menadione (MD), plumbagin (PB), or 100 M N-ethylmaleimide (NEM) for 20 min. The RT reaction was performed as described previously (31). After reverse transcription, the cDNA concentration was measured using a NanoDrop spectrophotometer.…”

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confidence: 99%

Pseudomonas aeruginosa Thiol Peroxidase Protects against Hydrogen Peroxide Toxicity and Displays Atypical Patterns of Gene Regulation

et al. 2012

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The Pseudomonas aeruginosa PAO1 thiol peroxidase homolog (Tpx) belongs to a family of enzymes implicated in the removal of toxic peroxides. We have shown the expression of tpx to be highly inducible with redox cycling/superoxide generators and diamide and weakly inducible with organic hydroperoxides and hydrogen peroxide (H 2 O 2 ). The PAO1 tpx pattern is unlike the patterns for other peroxide-scavenging genes in P. aeruginosa. Analysis of the tpx promoter reveals the presence of a putative IscR binding site located near the promoter. The tpx expression profiles in PAO1 and the iscR mutant, together with results from gel mobility shift assays showing that purified IscR specifically binds the tpx promoter, support the role of IscR as a transcriptional repressor of tpx that also regulates the oxidant-inducible expression of the gene. Recombinant Tpx has been purified and biochemically characterized. The enzyme catalyzes thioredoxin-dependent peroxidation and can utilize organic hydroperoxides and H 2 O 2 as substrates. The ⌬tpx mutant demonstrates differential sensitivity to H 2 O 2 only at moderate concentrations (0.5 mM) and not at high (20 mM) concentrations, suggesting a novel protective role of tpx against H 2 O 2 in P. aeruginosa. Altogether, P. aeruginosa tpx is a novel member of the IscR regulon and plays a primary role in protecting the bacteria from submillimolar concentrations of H 2 O 2 .

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“…Bacterial cells from the unin- duced and NaOCl-induced cultures were collected. The total RNA was prepared and qRT-PCR was performed as described (Jittawuttipoka et al 2010). The reverse transcription reaction was conducted with a RevertAid TM M-MuLV Reverse Transcriptase kit (Fermentas) using random hexamers according to the manufacturer's recommendation.…”

Section: Real-time Reverse Transcription -Polymerase Chain Reaction (mentioning

confidence: 99%

The roles of peroxide protective regulons in protecting Xanthomonas campestris pv. campestris from sodium hypochlorite stress

et al. 2015

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The exposure of Xanthomonas campestris pv. campestris to sublethal concentrations of a sodium hypochlorite (NaOCl) solution induced the expression of genes that encode peroxide scavenging enzymes within the OxyR and OhrR regulons. Sensitivity testing in various X. campestris mutants indicated that oxyR, katA, katG, ahpC, and ohr contributed to protection against NaOCl killing. The pretreatment of X. campestris cultures with oxidants, such as hydrogen peroxide (H2O2), t-butyl hydroperoxide, and the superoxide generator menadione, protected the bacteria from lethal concentrations of NaOCl in an OxyR-dependent manner. Treating the bacteria with a low concentration of NaOCl resulted in the adaptive protection from NaOCl killing and also provided cross-protection from H2O2 killing. Taken together, the results suggest that the toxicity of NaOCl is partially mediated by the generation of peroxides and other reactive oxygen species that are removed by primary peroxide scavenging enzymes, such as catalases and AhpC, as a part of an overall strategy that protects the bacteria from the lethal effects of NaOCl.

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Mutations of ferric uptake regulator (fur) impair iron homeostasis, growth, oxidative stress survival, and virulence of Xanthomonas campestris pv. campestris

Cited by 42 publications

References 54 publications

Two-Component Signaling System VgrRS Directly Senses Extracytoplasmic and Intracellular Iron to Control Bacterial Adaptation under Iron Depleted Stress

Two-Component Signaling System VgrRS Directly Senses Extracytoplasmic and Intracellular Iron to Control Bacterial Adaptation under Iron Depleted Stress

Pseudomonas aeruginosa Thiol Peroxidase Protects against Hydrogen Peroxide Toxicity and Displays Atypical Patterns of Gene Regulation

The roles of peroxide protective regulons in protecting Xanthomonas campestris pv. campestris from sodium hypochlorite stress

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