Aerobic Metabolism of Carbon Reserves by the "Obligate Anaerobe" Desulfovibrio gigas

Santos, Helena; Fareleira, Paula; Xavier, António V.; Chen, Liang; Liu, M.-Y.; LeGall, Jean

doi:10.1006/bbrc.1993.2081

Cited by 83 publications

(61 citation statements)

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“…It has been proposed that the Rbo protein catalyses the reduction of the superoxide anion to H 2 O 2 at the expense of cellular reducing agents such NAD(P)H (Liochev & Fridovich, 1997;Emerson et al, 2002;. It has also been proposed that the flavohaemoprotein is a rubredoxin-oxygen oxidoreductase (Roo), the final component of a soluble electron transfer chain that produces energy by recycling NAD(P)+ from carbon reserves in an aerobic environment (Santos et al, 1993). The fact that in C. perfringens these genes might be regulated by a CRP-like protein, which controls the response to glucose starvation, and that the size of the colonies of the mutants impaired in these regulatory genes is smaller than those of the wild-type strain when plated after oxidative stress, favour the latter hypothesis.…”

Section: Discussionmentioning

confidence: 99%

Oxidative stress response in Clostridium perfringens

2004

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Clostridium perfringens, a strictly anaerobic bacterium, is able to survive when exposed to oxygen for short periods of time and exhibits a complex adaptive response to reactive oxygen species, both under aerobic and anaerobic conditions. However, this adaptive response is not completely understood. C. perfringens possesses specialized genes that might be involved in this adaptive process, such as those encoding superoxide dismutase (SOD), superoxide reductase and alkyl hydroperoxide reductase, but their contribution to the oxidative stress response and their control mechanisms are unknown. By a combination of functional complementation of Escherichia coli strains impaired in either SOD, alkyl hydroperoxide reductase (AhpC) or catalase activity (Cat), transcription analysis and characterization of mutants impaired in regulatory genes, it was concluded that: (i) the product of the sod gene is certainly essential to scavenge superoxide radicals, (ii) the ahpC gene, which is fully induced in all oxidative stress conditions, is probably involved in the scavenging of all intracellular peroxides, (iii) the three rubrerythrin (rbr) genes of C. perfringens do not encode proteins with in vivo H 2 O 2 reductase activity, and (iv) the two rubredoxin (rub) genes do not contribute to the hypothetical superoxide reductase activity, but are likely to belong to an electron transfer chain involved in energy metabolism.

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Section: Discussionmentioning

confidence: 99%

Oxidative stress response in Clostridium perfringens

2004

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“…Polyglucose in D. gigus can be used as a carbon and energy source (Stams et al, 1983; Santos et al, 1993). One of the functions of polyphosphates is energy storage (Kornberg, 1995).…”

Section: Discussionmentioning

confidence: 99%

Electron‐Dense Granules in Desulfovibrio gigas do not Consist of Inorganic Triphosphate but of a Glucose Pentakis(Diphosphate)

Hensgens

Santos

Zhang

et al. 1996

European Journal of Biochemistry

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Under certain growth conditions the sulfate-reducing bacterium Desulfovibrio gigas forms electrondense granules in the cells which had been claimed to consist of a magnesium triphosphate). We observed granules after cultivation in media with a low Fez+ or NH,' concentration and reinvestigated the nature of the electron-dense bodies. Energy-dispersive X-ray analysis of the granules in the cells showed that they contain large amounts of P, Mg, and K. Gel electrophoresis and chromatographic analyses of isolated granules which had been dissolved in 20 mM EDTA, however, revealed discrepancies with commercially available polyphosphates. "P-NMR spectra also lacked the peaks in the -22-ppm region which are characteristic for inner phosphates of polyphosphates confirming that the phosphocompound as isolated from the electron-dense bodie? of D. gigas did not consist of polyphosphates. Using multinuclear NMR spectroscopy we showed that the electron-dense bodies of D. gigas contained a novel metabolite which was identified as a-glucose 1,2,3,4,6-pentakis(diphosphate).Keywords: polyphosphates ; electron-dense granules ; glucose pentakis(phosphate) ; Desulfovibrio gigas.Recently, a novel phosphorus-containing metabolite was detected in the sulfate-reducing bacterium Desulfovibrio desulfiricans ATCC 27774, in Brevibacterium amrnoniagenes and in Micrococcus luteus and identified as 3-methyl-l,2,3,4-tetrahydroxybutane-I ,3-cyclic bisphosphate (Santos et al., 1991 ;Turner et al., 1992;Ostrovsky et al., 1992a). This compound was not detected in four other Desulfovibrio strains (Santos et al., 1991). In B. amrnoniagenes and M. luteus the compound was synthesized in response to oxidative stress which led Ostrovsky et al. (1992b) to suggest an antistressor role for it.The novel compound was not detected in D. gigas NCIMB 9332 but this strain can respond to the stress imposed by certain media by synthesizing intracellular spherical granules which were reported to consist of a magnesium triphosphate (Jones and Chambers, 1975). Such a compound is most likely synthesized with pyrophosphate as a precursor. The thermodynamics of the activation of sulfate to adenosine 5'-phosphosulfate imply that the pyrophosphate concentration must be kept very low (Widdel and Hansen, 1992); this is usually effected by an active pyrophosphatase. This raised the question of how D. gigas can synthesize the inorganic triphosphate from pyrophosphate and led us to reinvestigate the nature of the electron-dense granules of D. gigas.Here we provide evidence that the granules do not consist of tris(po1yphosphate) but of a novel metabolite which was identified as a-glucose-1,2,3,4,6-pentakis(diphosphate). MATERIALS AND METHODSMicroorganisms. Growth of bacteria. Bacteria were grown in a bicarbonatebuffered medium (Pfennig et al., 1981) supplemented with trace elements (Pfennig and Lippert, 1966), 0.1 pM sodium tungstate, 0.1 pM sodium selenite, vitamin solution (Stams et al., 1983), and Na,S (2 mM). Standard substrate was 20 mM lactate. D. gigas (NCIMB 9332) was als...

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“…Although growth on hexoses has never been demonstrated in D. vulgaris, genes for enzymes catalyzing each of the steps in glycolysis are readily recognized in the genome sequence 29 , suggesting enzymatic activities similar to those demonstrated for the close relative Desulfovibrio gigas 30 . The metabolic capacity to store glycogen would also appear to be present in D. vulgaris, and this polymer has been proposed to be a source of reductant for oxygen consumption 31 . Clearly, during growth on organic acids, a full complement of enzymes for gluconeogenesis is needed for cell wall biosynthesis and modification.…”

Section: Energy Metabolismmentioning

confidence: 99%

The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough

Heidelberg¹,

Seshadri²,

et al. 2004

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Sulfate-reducing bacteria (SRB) are anaerobic prokaryotes found ubiquitously in nature. SRB were the first nonphotosynthetic, anaerobic bacteria shown to generate energy (ATP) through electron transfer-coupled phosphorylation. For this process, the SRB typically use sulfate as the terminal electron acceptor for respiration of hydrogen or various organic acids, which results in the production of sulfide, a highly reactive and toxic end-product. Beyond their obvious function in the sulfur cycle, SRB play an important role in global cycling of numerous other elements 1 . For example, in the carbon cycle, the SRB form part of microbial consortia that completely mineralize organic carbon in anaerobic environments; polymeric materials (e.g., cellulose) are first depolymerized and metabolized by fermentative microorganisms, and the resulting organic acid and reduced gas (that is, CO and H 2 ) end-products are further fermented or oxidized by other microbes, including SRB. The latter are particularly active in sulfate-rich (e.g., marine) environments, where they effectively link the global sulfur and carbon cycles 1,2 .Beyond these ecological roles, SRB also have a major economic impact because of their involvement in biocorrosion of ferrous metals in anaerobic environments 3 , described as "industrial venereal disease-it's expensive, everybody has it, and nobody wants to talk about it" 4 . For example, because SRB are abundant in oil fields, their metabolism has many negative consequences for the petroleum industry (e.g., corrosion of drilling and pumping machinery and storage tanks, souring of oil by sulfide production, plugging of machinery and rock pores with biomass and sulfide precipitates). The SRB also contribute to bioremediation of toxic metal ions 5,6 . Their metabolism increases the pH, causing toxic metal ions like copper (II), nickel (II) and cadmium (II) to precipitate as metal sulfides in acidic aquatic environments (e.g., mine effluents). Additionally, SRB can deliver electrons directly to oxidized toxic metal ions, including uranium (VI), technetium (VII), and chromium (VI), converting these into less soluble, reduced forms. Hence, SRB-mediated reduction represents a potentially useful mechanism for the bioremediation of metal ion contaminants from anaerobic sediments 6 .Most research on the metabolism and biochemistry of SRB has been done on the genus Desulfovibrio, a member of the δ-proteobacteria The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough Desulfovibrio vulgaris Hildenborough is a model organism for studying the energy metabolism of sulfate-reducing bacteria (SRB) and for understanding the economic impacts of SRB, including biocorrosion of metal infrastructure and bioremediation of toxic metal ions. The 3,570,858 base pair (bp) genome sequence reveals a network of novel c-type cytochromes, connecting multiple periplasmic hydrogenases and formate dehydrogenases, as a key feature of its energy metabolism. The relative arrangement of genes encod...

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Aerobic Metabolism of Carbon Reserves by the "Obligate Anaerobe" Desulfovibrio gigas

Cited by 83 publications

References 0 publications

Oxidative stress response in Clostridium perfringens

Oxidative stress response in Clostridium perfringens

Electron‐Dense Granules in Desulfovibrio gigas do not Consist of Inorganic Triphosphate but of a Glucose Pentakis(Diphosphate)

The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough

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