Electron transfer between hydrogenases and mono- and multiheme cytochromes in Desulfovibrio ssp

Pereira, Inês A. C.; Romão, Célia V.; Xavier, António V.; LeGall, Jean; Teixeira, Miguel

doi:10.1007/s007750050259

Cited by 87 publications

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“…Hydrogenase activity and electron storage occur in the periplasm whereas sulfate reduction occurs in the cytoplasm, therefore, electrons must cross the cytoplasmic membrane. Before genome analysis, the Hmc complex (DVU0531-36, containing a hexadecaheme c-type cytochrome) represented the only known D. vulgaris transmembrane electron circuit [15][16][17] . However, genome analysis indicates the presence of four alternate transmembrane electron conduits ( Fig.…”

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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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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“…In vivo, c 3 has been suggested to be the redox partner of the periplasmic hydrogenases (5, 22), a role supported by the finding that this cytochrome is tightly associated with hydrogenases during purification of the latter (17). A model in which tetraheme cytochrome c 3 shuttles electrons from hydrogenases to the various polyheme cytochromes (Hmc, nineheme cytochrome, or octaheme cytochrome c 3 ) has been proposed (2,15,18). In addition to having periplasmically located redox partners, tetraheme cytochrome c has been shown to form functional complexes with a number of cytosolic electron carriers, including ferredoxin (9), rubredoxin (28), and flavodoxin (16).…”

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confidence: 99%

Cytochrome c ₃ Mutants of Desulfovibrio desulfuricans

Casalot

et al. 2000

Appl Environ Microbiol

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To explore the physiological role of tetraheme cytochrome c 3 in the sulfate-reducing bacterium Desulfovibrio desulfuricans G20, the gene encoding the preapoprotein was cloned, sequenced, and mutated by plasmid insertion. The physical analysis of the DNA from the strain carrying the integrated plasmid showed that the insertion was successful. The growth rate of the mutant on lactate with sulfate was comparable to that of the wild type; however, mutant cultures did not achieve the same cell densities. Pyruvate, the oxidation product of lactate, served as a poor electron source for the mutant. Unexpectedly, the mutant was able to grow on hydrogensulfate medium. These data support a role for tetraheme cytochrome c 3 in the electron transport pathway from pyruvate to sulfate or sulfite in D. desulfuricans G20.The anaerobic sulfate-reducing bacteria have several lowpotential c-type cytochromes that are located in the periplasm and presumably function in electron transfer events. Several members of the genus Desulfovibrio have been shown to have three cytochromes in this class, monoheme cytochrome c 553 , tetraheme cytochrome c 3 , and a high-molecular-weight cytochrome c (Hmc) with 16 hemes (20,21). Of these cytochromes, the most abundant, and that for which the most structural information has been gathered, is tetraheme cytochrome c 3 (8, 21).The physiological role of tetraheme cytochrome c 3 remains enigmatic. This cytochrome has been reported to interact effectively with an almost unrealistic list of electron donors and acceptors. In vivo, c 3 has been suggested to be the redox partner of the periplasmic hydrogenases (5, 22), a role supported by the finding that this cytochrome is tightly associated with hydrogenases during purification of the latter (17). A model in which tetraheme cytochrome c 3 shuttles electrons from hydrogenases to the various polyheme cytochromes (Hmc, nineheme cytochrome, or octaheme cytochrome c 3 ) has been proposed (2,15,18). In addition to having periplasmically located redox partners, tetraheme cytochrome c has been shown to form functional complexes with a number of cytosolic electron carriers, including ferredoxin (9), rubredoxin (28), and flavodoxin (16). In vitro studies have shown that tetraheme cytochrome c 3 and an [NiFe] hydrogenase will mediate reduction of metals, including Fe(III), Cr(VI), and U(VI), with hydrogen as the electron donor (13).The reactive nature of tetraheme cytochrome c 3 makes biochemical characterization of redox partners and functional analysis problematic; therefore, a genetic approach was initiated. As a first step, it was necessary to determine whether this cytochrome is essential for cell growth. Construction of a strain with an interrupted gene encoding tetraheme cytochrome c 3 (cycA) allowed confirmation that this cytochrome is not required for growth with lactate as the primary source of carbon and reductant and with sulfate as the terminal electron acceptor. However, the mutant grew poorly, if at all, on pyruvatesulfate medium. We infer that the fi...

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“…The Hmc complex has been proposed to constitute the missing link between periplasmic hydrogen oxidation and cytoplasmic sulfate reduction (21), accepting electrons from the hydrogenases via the TpI-c 3 and transferring them across the membrane to the cytoplasm for reduction of sulfate. This role of the Hmc complex is corroborated by growth and expression studies with wild type and mutant strains of SRB (23)(24)(25) and by electron transfer experiments (26).…”

mentioning

confidence: 66%

“…The three cytochromes HmcA, 9HcA, and TpII-c 3 share a common electron donor, the TpI-c 3 , which acts as a mediator for electron transfer from hydrogenases. Indeed, catalytic amounts of this cytochrome increase the rate of reduction of either HmcA, 9HcA, or TpII-c 3 by hydrogenases (16,18,26). This is particularly true in the case of DvH HmcA for which reduction by either of the three hydrogenases is extremely slow in the absence of TpI-c 3 (26).…”

Section: Resultsmentioning

confidence: 99%

“…Indeed, catalytic amounts of this cytochrome increase the rate of reduction of either HmcA, 9HcA, or TpII-c 3 by hydrogenases (16,18,26). This is particularly true in the case of DvH HmcA for which reduction by either of the three hydrogenases is extremely slow in the absence of TpI-c 3 (26). Surface charge mapping of TpII-c 3 (18) and 9HcA (15) indicates that they share similar characteristics that distinguish them from the TpI-c 3 : contrary to TpI-c 3 , heme 1 is exposed and surrounded by a negative surface region, whereas heme 4 (9HcA heme 9) lacks the TpI-c 3 characteristic positive surface patch proposed to be the site of interaction with hydrogenases.…”

Section: Resultsmentioning

confidence: 99%

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Sulfate Respiration in Desulfovibrio vulgaris Hildenborough

Matías

Coelho

Valente

et al. 2002

Journal of Biological Chemistry

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The crystal structure of the high molecular mass cytochrome c HmcA from Desulfovibrio vulgaris Hildenborough is described. HmcA contains the unprecedented number of sixteen hemes c attached to a single polypeptide chain, is associated with a membranebound redox complex, and is involved in electron transfer from the periplasmic oxidation of hydrogen to the cytoplasmic reduction of sulfate. The structure of HmcA is organized into four tetraheme cytochrome c 3 -like domains, of which the first is incomplete and contains only three hemes, and the final two show great similarity to the nine-heme cytochrome c from Desulfovibrio desulfuricans. An isoleucine residue fills the vacant coordination space above the iron atom in the five-coordinated high-spin Heme 15. The characteristics of each of the tetraheme domains of HmcA, as well as its surface charge distribution, indicate this cytochrome has several similarities with the nine-heme cytochrome c and the Type II cytochrome c 3 molecules, in agreement with their similar genetic organization and mode of reactivity and further support an analogous physiological function for the three cytochromes. Based on the present structure, the possible electron transfer sites between HmcA and its redox partners (namely Type I cytochrome c 3 and other proteins of the Hmc complex), as well as its physiological role, are discussed.

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Electron transfer between hydrogenases and mono- and multiheme cytochromes in Desulfovibrio ssp

Cited by 87 publications

References 0 publications

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

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

Cytochrome c ₃ Mutants of Desulfovibrio desulfuricans

Sulfate Respiration in Desulfovibrio vulgaris Hildenborough

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Electron transfer between hydrogenases and mono- and multiheme cytochromes in Desulfovibrio ssp

Cited by 87 publications

References 0 publications

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

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

Cytochrome c 3 Mutants of Desulfovibrio desulfuricans

Sulfate Respiration in Desulfovibrio vulgaris Hildenborough

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Cytochrome c ₃ Mutants of Desulfovibrio desulfuricans