A genomic island of the sulfate‐reducing bacterium <i>Desulfovibrio vulgaris</i> Hildenborough promotes survival under stress conditions while decreasing the efficiency of anaerobic growth

Johnston, Shawna; Lin, Shiping; Lee, Phoebe; Caffrey, Sean; Wildschut, Janine; Voordouw, Johanna K.; Silva, Sofia M. da; Pereira, Inês A. C.; Voordouw, Gerrit

doi:10.1111/j.1462-2920.2008.01823.x

Cited by 20 publications

(43 citation statements)

References 25 publications

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“…However, the incomplete recovery of the mutant strains observed upon inhibition of iNOS suggests that they also participate in protection against other stresses, such as oxidative stress, imposed by the macrophages. Studies in oxygenated environments showing that the roo and hcp mutations decrease D. vulgaris survival under conditions of oxidative stress corroborate this hypothesis (18,24,27,28,39).…”

Section: Discussionsupporting

confidence: 62%

“…with known genome sequences, D. vulgaris Hildenborough contains two homologues of the FDPs (ROO1 and ROO2) and of HCPs (HCP1 and HCP2). The genes encoding ROO1 (DVU2014) and HCP1 (DVU2013) are adjacent within a genomic island (24), while the genes encoding ROO2 (DVU3185) and HCP2 (DVU2543) are located elsewhere and are separated in the genome. In Desulfovibrio spp., these proteins are proposed to promote survival in oxygenated environments and to remove RNS generated by nitrite reduction (24)(25)(26)(27)(28).…”

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confidence: 99%

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Hybrid Cluster Proteins and Flavodiiron Proteins Afford Protection to Desulfovibrio vulgaris upon Macrophage Infection

et al. 2013

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bDesulfovibrio species are Gram-negative anaerobic sulfate-reducing bacteria that colonize the human gut. Recently, Desulfovibrio spp. have been implicated in gastrointestinal diseases and shown to stimulate the epithelial immune response, leading to increased production of inflammatory cytokines by macrophages. Activated macrophages are key cells of the immune system that impose nitrosative stress during phagocytosis. Hence, we have analyzed the in vitro and in vivo responses of Desulfovibrio vulgaris Hildenborough to nitric oxide (NO) and the role of the hybrid cluster proteins (HCP1 and HCP2) and rubredoxin oxygen oxidoreductases (ROO1 and ROO2) in NO protection. Among the four genes, hcp2 was the gene most highly induced by NO, and the hcp2 transposon mutant exhibited the lowest viability under conditions of NO stress. Studies in murine macrophages revealed that D. vulgaris survives incubation with these phagocytes and triggers NO production at levels similar to those stimulated by the cytokine gamma interferon (IFN-␥). Furthermore, D. vulgaris hcp and roo mutants exhibited reduced viability when incubated with macrophages, revealing that these gene products contribute to the survival of D. vulgaris during macrophage infection. Desulfovibrio spp. are anaerobic sulfate-reducing bacteria (SRB) that occur in several environmental niches, such as marine and freshwater sediments, as well as in humans as part of the normal oral cavity and gut flora. In particular, four Desulfovibrio spp., namely, D. fairfieldensis, D. desulfuricans, D. piger, and D. vulgaris, were detected in healthy humans (1-3). Furthermore, Desulfovibrio spp. have also been implicated in gastrointestinal diseases, such as inflammatory bowel diseases and periondontitis, since Desulfovibrio strains were isolated from biopsy specimens of patients with ulcerative colitis, brain, abdominal wall, and liver abscesses, and appendicitis (4-6).Recently, D. desulfuricans and D. fairfieldensis were shown to be able to invade nonprofessional phagocytic cells such as the oral epithelial cells and to stimulate the epithelial immune response by increasing the production of inflammatory interleukins (7). Nonetheless, the ability of Desulfovibrio spp. to survive professional phagocytes, such as macrophages, remains to be evaluated.Two of the main weapons of the innate immune system to eradicate pathogens are the generation of reactive oxygen species (ROS) and the generation of reactive nitrogen species (RNS), which are derived from the superoxide and nitric oxide produced by the NADPH oxidase and the mammalian inducible nitric oxide synthase (iNOS), respectively (8, 9). These chemicals can inflict serious damage in bacteria, which employ the expression of several detoxification systems to avoid such damage (9). The flavodiiron proteins (FDP) constitute a large family of enzymes widespread among archaea and bacteria, including in Desulfovibrio spp. They are believed to contribute to bacterial survival under oxidative and nitrosative stress conditions (10). FDPs a...

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Section: Discussionsupporting

confidence: 62%

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confidence: 99%

Hybrid Cluster Proteins and Flavodiiron Proteins Afford Protection to Desulfovibrio vulgaris upon Macrophage Infection

et al. 2013

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“…However, there were no significant changes in EhFdp1 transcript abundance under a variety of conditions, including response to NO-derived stress (1, 2, 11, 13, 42). FDPs have been shown to be highly and constitutively expressed both in prokaryotes (in some cases incorporating an oxidative stress response operon [8,18]) and in protozoa (10,25,32). However, an increase in expression upon oxygen exposure has been observed for only one other FDP, that from the hyperthermophilic bacterium Thermotoga maritima, which shows an increase in protein levels with unmatched transcriptional levels and is proposed to sustain the growth of this "strict" anaerobe under microaerophilic conditions (20)(21)(22).…”

Section: Methodsmentioning

confidence: 99%

A Detoxifying Oxygen Reductase in the Anaerobic Protozoan Entamoeba histolytica

et al. 2012

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ABSTRACTWe report the characterization of a bacterial-type oxygen reductase abundant in the cytoplasm of the anaerobic protozoan parasiteEntamoeba histolytica. Upon host infection,E. histolyticais confronted with various oxygen tensions in the host intestine, as well as increased reactive oxygen and nitrogen species at the site of local tissue inflammation. Resistance to oxygen-derived stress thus plays an important role in the pathogenic potential ofE. histolytica. The genome ofE. histolyticahas four genes that encode flavodiiron proteins, which are bacterial-type oxygen or nitric oxide reductases and were likely acquired by lateral gene transfer from prokaryotes. TheEhFdp1gene has higher expression in virulent than in nonvirulentEntamoebastrains and species, hinting that the response to oxidative stress may be one correlate of virulence potential. We demonstrate that EhFdp1 is abundantly expressed in the cytoplasm ofE. histolyticaand that the protein levels are markedly increased (up to ∼5-fold) upon oxygen exposure. Additionally, we produced fully functional recombinant EhFdp1 and demonstrated that this enzyme is a specific and robust oxygen reductase but has poor nitric oxide reductase activity. This observation represents a new mechanism of oxygen resistance in the anaerobic protozoan pathogenE. histolytica.

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“…These include DVU3183 superoxide reductase (sor), as well as the NADH peroxidases DVU3094 rubrerythrin-1 (rbr1), DVU2310 rubrerythrin-2 (rbr2) and DVU0019 nigerythrin (ngr). D. vulgaris also removes oxygen by protective respiration using membrane-bound oxygen reductases Cox (DVU1811-1815) and Cyd (DVU3270-3271), as well as the cytoplasmic rubredoxin:oxygen oxidoreductases DVU2014 Roo1 and DVU3185 Roo2 (Frazão et al 2000;Johnston et al 2009;Lemos et al 2001;Lobo et al 2008). Deletion analysis has indicated that Roo1 and Roo2 confer resistance to oxygen-mediated killing under microaerophilic conditions, whereas Sor protects against killing under fully aerobic conditions (Johnston et al 2009;Wildschut et al 2006).…”

Section: Introductionmentioning

confidence: 97%

“…The effect of oxygen-and H 2 O 2 -stress on geneexpression in D. vulgaris has been studied extensively (Brioukhanov et al 2010;Johnston et al 2009;Mukhopadhyay et al 2007;Pereira et. al.…”

Section: Introductionmentioning

confidence: 99%

Oxygen exposure increases resistance of Desulfovibrio vulgaris Hildenborough to killing by hydrogen peroxide

Wildschut¹,

Caffrey

Voordouw

et al. 2011

Antonie van Leeuwenhoek

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Inactivation of PerR by oxidative stress and a corresponding increase in expression of the perR regulon genes is part of the oxidative stress defense in a variety of anaerobic bacteria. Diluted anaerobic, nearly sulfide-free cultures of mutant and wild-type Desulfovibrio vulgaris (10(5)-10(6) colony-forming units/ml) were treated with 0 to 2,500 μM H(2)O(2) for only 5 min to prevent readjustment of gene expression. Survivors were then scored by plating. The wild type and perR mutant had 50% survival at 58 and 269 μM H(2)O(2), respectively, indicating the latter to be 4.6-fold more resistant to killing by H(2)O(2) under these conditions. Significantly increased resistance of the wild type (38-fold; 50% killing at 2188 μM H(2)O(2)) was observed if cells were pretreated with full air for 30 min, conditions that did not affect cell viability. The resistance of the perR mutant increased less (4.6-fold; 50% killing at 1230 μM H(2)O(2)), when similarly pretreated. Interestingly, no increased resistance of either was achieved by exposure with 10.6 μM H(2)O(2) for 30 min, the highest concentration that could be used without killing the cells. Hence, in environments with low D. vulgaris biomass only the presence of external O(2) effectively activates the perR regulon. As a result, mutant strains lacking one of the perR regulon genes ahpC, dvu0772, rbr1 or rbr2 displayed decreased resistance to H(2)O(2) stress only following pretreatment with air.

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A genomic island of the sulfate‐reducing bacterium Desulfovibrio vulgaris Hildenborough promotes survival under stress conditions while decreasing the efficiency of anaerobic growth

Cited by 20 publications

References 25 publications

Hybrid Cluster Proteins and Flavodiiron Proteins Afford Protection to Desulfovibrio vulgaris upon Macrophage Infection

Hybrid Cluster Proteins and Flavodiiron Proteins Afford Protection to Desulfovibrio vulgaris upon Macrophage Infection

A Detoxifying Oxygen Reductase in the Anaerobic Protozoan Entamoeba histolytica

Oxygen exposure increases resistance of Desulfovibrio vulgaris Hildenborough to killing by hydrogen peroxide

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