Function of Oxygen Resistance Proteins in the Anaerobic, Sulfate-Reducing Bacterium
            <i>Desulfovibrio vulgaris</i>
            Hildenborough

Fournier, Marjorie; Zhang, Yi; Wildschut, Janine; Dolla, Alain; Voordouw, Johanna K.; Schriemer, David C.; Voordouw, Gerrit

doi:10.1128/jb.185.1.71-79.2003

Cited by 101 publications

(82 citation statements)

References 43 publications

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“…Because of the periplasmic location of the D. vulgaris Hildenborough [Fe] superoxide dismutase, it has been proposed that this enzyme is involved in the protection of periplasmic ironsulfur proteins against superoxide-induced damage (25). One of these sensitive enzymes could be the periplasmic [Fe] hydrogenase.…”

Section: Resultsmentioning

confidence: 99%

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A New Function of the Desulfovibrio vulgaris Hildenborough [Fe] Hydrogenase in the Protection against Oxidative Stress

Fournier

Dermoun

Durand

et al. 2004

Journal of Biological Chemistry

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Sulfate-reducing bacteria, like Desulfovibrio vulgarisHildenborough, have developed a set of reactions allowing them to survive in oxic environments and even to reduce molecular oxygen to water. D. vulgaris contains a cytoplasmic superoxide reductase (SOR) and a periplasmic superoxide dismutase (SOD) involved in the elimination of superoxide anions. To assign the function of SOD, the periplasmic [Fe] hydrogenase activity was followed in both wild-type and sod deletant strains. This activity was lower in the strain lacking the SOD than in the wild-type when the cells were exposed to oxygen for a short time. The periplasmic SOD is thus involved in the protection of sensitive iron-sulfur-containing enzyme against superoxide-induced damages. Surprisingly, production of the periplasmic Microbial sulfate reduction has been reported to be an ancient process as old as 3.47 gigayears. Sulfate reduction thus represents an early specific metabolic pathway, allowing time calibration of a deep node on the tree of life (1). Sulfate-reducing bacteria (SRB) 1 are universally distributed in marine and microbial mats where sulfate reduction is the dominant anaerobic biomineralization pathway. They constitute a group of anaerobic prokaryotes, which are unified by sharing the capacity to carry out dissimilatory sulfate reduction to sulfide as a major component of their bioenergetic processes. Although sulfate reduction is generally considered to be an anaerobic process, the abundance and metabolic activity of SRB in oxic zones is frequently evaluated as higher than those in neighboring anoxic zones in numerous biotopes (2, 3). In situ detection of sulfate reducing activity and SRB populations in these biotopes showed that SRB species did not have the same capability of resisting oxygen. Analysis of the photooxic zone of cyanobacterial mats revealed a well-defined SRB distribution. Although Desulfobacter and Desulfobacterium were restricted to the deepest levels in the mats, Desulfococcus were predominant in the photooxic zone with Desulfovibrio also present. This distribution suggests that both groups contain oxygen-tolerant members (4). It is thus clear that SRB exhibit a differentiated set of reactions to oxygen: first, many SRB form aggregates (5), resulting in a higher tolerance to oxygen exposure; second, at least Desulfovibrio species migrate in response to the oxygen concentration in their environment (5); and third, many species respire with oxygen (6). However, although it has been demonstrated that aerobic respiration is coupled with proton translocation and ATP conservation, aerobic growth in pure culture has never been proved (7). The high respiration rate merely seems to have a protective function. In an oxygen gradient, bacteria form bands at the outer edge of the oxic zone, suggesting both negative and positive aerotaxis responses (8). The capability of SRB to move toward oxygen and reduce it might play an ecological role in the zone of transition from an oxic to an anoxic environment, protecting themselves and other...

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Section: Resultsmentioning

confidence: 99%

“…Following gene deletion, it was proposed that SOR might play a key role in oxygen defense (18,24). Because of its periplasmic location, SOD is thought to remove the periplasmic-generated superoxide (25) that could induce oxidative damage on sensitive iron-sulfur enzymes.…”

Section: Sulfate-reducing Bacteria Like Desulfovibrio Vulgarismentioning

confidence: 99%

A New Function of the Desulfovibrio vulgaris Hildenborough [Fe] Hydrogenase in the Protection against Oxidative Stress

Fournier

Dermoun

Durand

et al. 2004

Journal of Biological Chemistry

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“…This protein gradually disappeared from air-exposed D. vulgaris H cells (46), presumably because of damaging reactions in the increasingly oxidizing environment. In its natural growth habitat D. vulgaris may more often be exposed to subaerobic levels of dioxygen (44,47,48), which may be lowered even further by reduction in the periplasm (46,49). The cytoplasmic superoxide flux under such conditions is unknown but is unlikely to be significantly higher than that of dioxygenrespiring aerobic bacteria.…”

Section: Discussionmentioning

confidence: 99%

“…One possible function is dioxygen scavenging upon exposure to air, which would thereby generate a superoxide flux. D. vulgaris H, which remains viable after up to a few hours incubation in air-saturated media (8,46), contains a periplasmic SOD and a single cytoplasmic SOR, the 2Fe-SOR examined in this work (8). A mutant D. vulgaris H strain in which the SOR is inactivated was clearly more sensitive than the wild type to both air exposure and to paraquat-induced increases in cytoplasmic superoxide fluxes (8,46).…”

Section: Discussionmentioning

confidence: 99%

“…The D. vulgaris strain Hildenborough (H) is the source of the rubredoxin and 2Fe-SOR examined in this work. The D. vulgaris H genome contains genes encoding both cytochrome c-and bd-type membrane-bound terminal oxidases (46). The function of these "respiratory" oxidases is unclear, because these sulfate-reducing bacteria do not grow aerobically.…”

Section: Discussionmentioning

confidence: 99%

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Kinetics of the Superoxide Reductase Catalytic Cycle

Emerson

Coulter

Phillips

et al. 2003

Journal of Biological Chemistry

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The steady state kinetics of a Desulfovibrio (D.) vulgaris superoxide reductase (SOR) turnover cycle, in which superoxide is catalytically reduced to hydrogen peroxide at a [Fe(His) 4 (Cys)] active site, are reported. A proximal electron donor, rubredoxin, was used to supply reducing equivalents from NADPH via ferredoxin: NADP ؉ oxidoreductase, and xanthine/xanthine oxidase was used to provide a calibrated flux of superoxide. SOR turnover in this system was well coupled, i.e. ؊10 M, during which SOR turns over about once every 6 s, (ii) the diffusion-controlled reaction of reduced SOR with superoxide is the slowest process during turnover, and (iii) neither ligation nor deligation of the active site carboxylate of SOR limits the turnover rate. An intracellular SOR concentration on the order of 10 M is estimated to be the minimum required for lowering superoxide to sublethal levels in aerobically growing SOD knockout mutants of Escherichia coli. SORs from Desulfovibrio gigas and Treponema pallidum showed similar turnover rates when substituted for the D. vulgaris SOR, whereas superoxide dismutases showed no SOR activity in our assay. These results provide quantitative support for previous suggestions that, in times of oxidative stress, SORs efficiently divert intracellular reducing equivalents to superoxide.An emerging paradigm for protecting air-sensitive bacteria and Archaea from the toxic reduction products of dioxygen involves reduction of superoxide and hydrogen peroxide, rather than the classical disproportionation route for their removal characteristic of aerobic microoorganisms (1-9). The reduction of superoxide via Reaction 1 is catalyzed by a novel class of non-heme iron enzymes called superoxide reductases (SORs).

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Superoxide Reductase

Nivière¹,

Bonnot²,

Bourgeois³

2004

Handbook of Metalloproteins

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Superoxide reductase (SOR) is a small bacterial metalloprotein, which is present in the cytoplasm of some anaerobic or microaerophilic microorganisms. SOR is involved in the detoxification of the superoxide radical and catalyzes its one‐electron reduction into hydrogen peroxide. Three different classes of SOR have been identified and structurally characterized. They all contain a similar active site, which consists of an unusual nonheme iron center, coordinated in a square‐pyramidal geometry to four nitrogens from four histidine side chains in the equatorial plane and the sulfur of one cysteine residue along the fifth axial position. In the reduced state, the sixth axial coordinating site of the iron is vacant, suggesting the most obvious site for initial binding of the superoxide substrate. The reaction mechanism of SOR has been studied by pulse radiolysis. SOR reacts specifically at a nearly diffusion‐controlled rate with O 2 •− , generating H 2 O 2 and the oxidized Fe 3+ active site. Reaction intermediates have been observed and proposed to be Fe 3+ ‐(hydro)peroxo species, resulting from the fast electron transfer from the ferrous iron to the superoxide anion and from protonation step. Formation of Fe 3+ ‐(hydro)peroxo intermediate species in the active site of SOR has been supported by resonance Raman spectroscopy and X‐ray structures of iron(III) peroxide species in the SOR from Desulfoarculus baarsii .

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Function of Oxygen Resistance Proteins in the Anaerobic, Sulfate-Reducing Bacterium Desulfovibrio vulgaris Hildenborough

Cited by 101 publications

References 43 publications

A New Function of the Desulfovibrio vulgaris Hildenborough [Fe] Hydrogenase in the Protection against Oxidative Stress

A New Function of the Desulfovibrio vulgaris Hildenborough [Fe] Hydrogenase in the Protection against Oxidative Stress

Kinetics of the Superoxide Reductase Catalytic Cycle

Superoxide Reductase

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