Biochemistry, physiology and biotechnology of sulfate-reducing bacteria.

Chemolithotrophic bacteria that use sulfate as terminal electron acceptor (sulfate-reducing bacteria) constitute a unique physiological group of microorganisms that couple anaerobic electron transport to ATP synthesis. These bacteria (220 species of 60 genera) can use a large variety of compounds as electron donors and to mediate electron flow they have a vast array of proteins with redox active metal groups. This chapter deals with the distribution in the environment and the major physiological and metabolic characteristics of sulfate-reducing bacteria (SRB). This chapter presents our current knowledge of soluble electron transfer proteins and transmembrane redox complexes that are playing an essential role in the dissimilatory sulfate reduction pathway of SRB of the genus Desulfovibrio. Environmentally important activities displayed by SRB are a consequence of the unique electron transport components or the production of high levels of H(2)S. The capability of SRB to utilize hydrocarbons in pure cultures and consortia has resulted in using these bacteria for bioremediation of BTEX (benzene, toluene, ethylbenzene and xylene) compounds in contaminated soils. Specific strains of SRB are capable of reducing 3-chlorobenzoate, chloroethenes, or nitroaromatic compounds and this has resulted in proposals to use SRB for bioremediation of environments containing trinitrotoluene and polychloroethenes. Since SRB have displayed dissimilatory reduction of U(VI) and Cr(VI), several biotechnology procedures have been proposed for using SRB in bioremediation of toxic metals. Additional non-specific metal reductase activity has resulted in using SRB for recovery of precious metals (e.g. platinum, palladium and gold) from waste streams. Since bacterially produced sulfide contributes to the souring of oil fields, corrosion of concrete, and discoloration of stonework is a serious problem, there is considerable interest in controlling the sulfidogenic activity of the SRB. The production of biosulfide by SRB has led to immobilization of toxic metals and reduction of textile dyes, although the process remains unresolved, SRB play a role in anaerobic methane oxidation which not only contributes to carbon cycle activities but also depletes an important industrial energy reserve.

[1]  Maria Arménia Carrondo,et al.  Sulfate Respiration in Desulfovibrio vulgaris Hildenborough , 2002, The Journal of Biological Chemistry.

[2]  A. Zehnder Biology of anaerobic microorganisms , 1988 .

[3]  K. Suzuki,et al.  Caldivirga maquilingensis gen. nov., sp. nov., a new genus of rod-shaped crenarchaeote isolated from a hot spring in the Philippines. , 1999, International journal of systematic bacteriology.

[4]  H. Naveau,et al.  Bioaugmentation of a soil bioreactor designed for pilot-scale anaerobic bioremediation studies. , 1999 .

[5]  Oliver J. Hao,et al.  Sulfate‐reducing bacteria , 1996 .

[6]  M. Teixeira,et al.  The anaerobe Desulfovibrio desulfuricans ATCC 27774 grows at nearly atmospheric oxygen levels , 2007, FEBS letters.

[7]  C. Whiteley,et al.  Decolorization and Degradation of Textile Dyes with Biosulfidogenic Hydrogenases , 2007, Biotechnology progress.

[8]  D. Craw,et al.  The geomicrobiology of gold , 2007, The ISME Journal.

[9]  R. Huber,et al.  Cytochrome c Nitrite Reductase from Desulfovibrio desulfuricans ATCC 27774 , 2003, The Journal of Biological Chemistry.

[10]  J. Wall,et al.  Sulphate-reducing Bacteria: Evaluation of stress response in sulphate-reducing bacteria through genome analysis , 2007 .

[11]  M. Bruschi,et al.  Enzymatic reduction of chromate: comparative studies using sulfate-reducing bacteria , 2001, Applied Microbiology and Biotechnology.

[12]  Edward R. Landa,et al.  Microbial reduction of uranium , 1991, Nature.

[13]  D. Kurtz,et al.  The mechanism(s) of superoxide reduction by superoxide reductases in vitro and in vivo , 2002, JBIC Journal of Biological Inorganic Chemistry.

[14]  Hatchikian Ec Desulfofuscidin: dissimilatory, high-spin sulfite reductase of thermophilic, sulfate-reducing bacteria. , 1994 .

[15]  C. Brondino,et al.  Purification and characterization of a tungsten-containing formate dehydrogenase from Desulfovibrio gigas. , 1999, Biochemistry.

[16]  W. Hagen,et al.  Novel electron paramagnetic resonance signals from an Fe/S protein containing six iron atoms , 1989 .

[17]  I. Moura,et al.  Characterization of three proteins containing multiple iron sites: rubrerythrin, desulfoferrodoxin, and a protein containing a six-iron cluster. , 1994, Methods in enzymology.

[18]  R. Cammack,et al.  ESR studies of cytochrome c3 from Desulfovibrio desulfuricans strain Norway 4: Midpoint potentials of the four haems, and interactions with ferredoxin and colloidal sulphur , 1984 .

[19]  M. Fournier,et al.  Oxygen defense in sulfate-reducing bacteria. , 2006, Journal of biotechnology.

[20]  T. Hansen,et al.  Immunocytochemical localization of APS reductase and bisulfite reductase in three Desulfovibrio species , 1988, Archives of Microbiology.

[21]  Hai Shen,et al.  Modelling Cr(VI) reduction by pure bacterial cultures , 1997 .

[22]  J. Moura,et al.  ADENYLYLSULFATE REDUCTASES FROM SULFATE-REDUCING BACTERIA , 1994 .

[23]  B. Ollivier,et al.  Reclassification of the sulfate- and nitrate-reducing bacterium Desulfovibrio vulgaris subsp. oxamicus as Desulfovibrio oxamicus sp. nov., comb. nov. , 2006, International journal of systematic and evolutionary microbiology.

[24]  J. Conca,et al.  An Apatite II permeable reactive barrier to remediate groundwater containing Zn, Pb and Cd , 2006 .

[25]  G. Voordouw Emerging Oil Field Biotechnologies: Prevention of Oil Field Souring by Nitrate Injection , 2008 .

[26]  W. Hamilton,et al.  Utilization of cathodic hydrogen by Desulfovibrio vulgaris (Hildenborough) , 1986 .

[27]  J. Puhakka,et al.  Sulfate Reduction Potential in Sediments in the Norilsk Mining Area, Northern Siberia , 2005 .

[28]  H. Biebl,et al.  Growth of sulfate-reducing bacteria with sulfur as electron acceptor , 1977, Archives of Microbiology.

[29]  Gerrit Voordouw,et al.  Physiological and Gene Expression Analysis of Inhibition of Desulfovibrio vulgaris Hildenborough by Nitrite , 2004, Journal of bacteriology.

[30]  M. Bruschi,et al.  Purification and some properties of cytochrome C553(550) isolated from Desulfovibrio desulfuricans Norway. , 1979, Biochemical and biophysical research communications.

[31]  Yanan Shen,et al.  The antiquity of microbial sulfate reduction , 2004 .

[32]  W. Dilling,et al.  Aerobic respiration in sulfate‐reducing bacteria* , 1990 .

[33]  K. Suzuki,et al.  Thermocladium modestius gen. nov., sp. nov., a new genus of rod-shaped, extremely thermophilic crenarchaeote. , 1998, International journal of systematic bacteriology.

[34]  D. Wise Remediation of Hazardous Waste Contaminated Soils , 1994 .

[35]  S. Miyazawa,et al.  Numerical Evaluation of Biocide Treatment against Sulfate Reducing Bacteria in Oilfield Water Pipelines , 2007 .

[36]  I. Pereira,et al.  A Membrane‐Bound Cytochrome c3: A Type II Cytochrome c3 from Desulfovibrio vulgaris Hildenborough , 2001, Chembiochem : a European journal of chemical biology.

[37]  S. Macnaughton,et al.  Diversity and Characterization of Sulfate-Reducing Bacteria in Groundwater at a Uranium Mill Tailings Site , 2001, Applied and Environmental Microbiology.

[38]  I. R. Harris,et al.  Bioreduction and biocrystallization of palladium by Desulfovibrio desulfuricans NCIMB 8307 , 2002, Biotechnology and bioengineering.

[39]  Meiying Xu,et al.  Respiration and Growth of Shewanella decolorationis S12 with an Azo Compound as the Sole Electron Acceptor , 2006, Applied and Environmental Microbiology.

[40]  M. Teixeira,et al.  The three classes of hydrogenases from sulfate-reducing bacteria of the genus Desulfovibrio. , 1988, FEMS microbiology reviews.

[41]  Martin Stratmann,et al.  Iron corrosion by novel anaerobic microorganisms , 2004, Nature.

[42]  J. Calvete,et al.  ATP sulfurylases from sulfate-reducing bacteria of the genus Desulfovibrio. A novel metalloprotein containing cobalt and zinc. , 1998, Biochemistry.

[43]  L. Daniels,et al.  Thiosulfate, polythionates and elemental sulfur assimilation and reduction in the bacterial world. , 1990, FEMS microbiology reviews.

[44]  L. Barton,et al.  Kinetic coefficients for simultaneous reduction of sulfate and uranium by Desulfovibrio desulfuricans , 1996, Applied Microbiology and Biotechnology.

[45]  R. Meckenstock,et al.  Methylation is the initial reaction in anaerobic naphthalene degradation by a sulfate-reducing enrichment culture. , 2006, Environmental microbiology.

[46]  E. A. Greene,et al.  Gene expression analysis of the mechanism of inhibition of Desulfovibrio vulgaris Hildenborough by nitrate-reducing, sulfide-oxidizing bacteria. , 2005, Environmental microbiology.

[47]  K. Deplanche,et al.  Biorecovery of gold by Escherichia coli and Desulfovibrio desulfuricans , 2008, Biotechnology and bioengineering.

[48]  Lynne E. Macaskie,et al.  Enzymatic Recovery of Elemental Palladium by Using Sulfate-Reducing Bacteria , 1998, Applied and Environmental Microbiology.

[49]  M. Teixeira,et al.  Nickel containing hydrogenases , 1983 .

[50]  D. Lovley Environmental Microbe-Metal Interactions , 2000 .

[51]  C. Liang,et al.  Effect of Sulfate Reduced Bacterium on Corrosion Behavior of 10CrMoAl Steel , 2007 .

[52]  R. Boopathy,et al.  Metabolism of 2,4,6-trinitrotoluene (TNT) by Desulfovibrio sp. (B strain) , 1993, Applied Microbiology and Biotechnology.

[53]  L. Melo,et al.  Interaction of Desulfovibrio desulfuricans biofilms with stainless steel surface and its impact on bacterial metabolism , 2006, Journal of applied microbiology.

[54]  L. Young,et al.  Molecular characterization of a sulfate-reducing consortium which mineralizes benzene , 1998 .

[55]  W. Sackett Microbial mats: Stromatolites: Edited by Yehuda Cohen, Richard W. Castenholz and Harlyn O. Halvorson. Alan R. Liss, New York, 1984, 498 pp , 1985 .

[56]  K. Knittel,et al.  Sulphate-reducing Bacteria: Anaerobic degradation of hydrocarbons with sulphate as electron acceptor , 2007 .

[57]  N. A. Rowson,et al.  A novel electrobiotechnology for the recovery of precious metals from spent automotive catalysts , 2003, Environmental technology.

[58]  C. Costa,et al.  [21] Hexaheme nitrite reductase from Desulfovibrio desulfuricans (ATCC 27774) , 1994 .

[59]  A. Lino,et al.  Characterization of two dissimilatory sulfite reductases (desulforubidin and desulfoviridin) from the sulfate-reducing bacteria. Moessbauer and EPR studies , 1988 .

[60]  L. Barton,et al.  Reduction of Cr, Mo, Se and U by Desulfovibrio desulfuricans immobilized in polyacrylamide gels , 1998, Journal of Industrial Microbiology and Biotechnology.

[61]  R. Meckenstock,et al.  Anaerobic Degradation of p-Xylene by a Sulfate-Reducing Enrichment Culture , 2005, Current Microbiology.

[62]  K. Kvenvolden,et al.  Potential effects of gas hydrate on human welfare. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[63]  F. Elbaz-Poulichet,et al.  Thermodesulfovibrio hydrogeniphilus sp. nov., a new thermophilic sulphate-reducing bacterium isolated from a Tunisian hot spring. , 2008, Systematic and applied microbiology.

[64]  F. Morel,et al.  Dissimilatory arsenate and sulfate reduction in Desulfotomaculum auripigmentum sp. nov. , 1997, Archives of Microbiology.

[65]  L. Barton,et al.  Oxidative phosphorylation linked to the dissimilatory reduction of elemental sulphur by Desulfovibrio. , 1979, Ciba Foundation symposium.

[66]  W. Hamilton,et al.  Microbially Influenced Corrosion as a Model System for the Study of Metal Microbe Interactions: A Unifying Electron Transfer Hypothesis , 2003, Biofouling.

[67]  F. Glöckner,et al.  Anaerobic Degradation of Ethylbenzene by a New Type of Marine Sulfate-Reducing Bacterium , 2003, Applied and Environmental Microbiology.

[68]  M. Romão,et al.  Crystal structure of the 16 heme cytochrome from Desulfovibrio gigas: a glycosylated protein in a sulphate-reducing bacterium. , 2007, Journal of molecular biology.

[69]  M. Dworkin Ecophysiology and biochemistry , 2006 .

[70]  Willy Verstraete,et al.  Microbial ecology meets electrochemistry: electricity-driven and driving communities , 2007, The ISME Journal.

[71]  Lynne E. Macaskie,et al.  Palladium and gold removal and recovery from precious metal solutions and electronic scrap leachates by Desulfovibrio desulfuricans , 2006, Biotechnology Letters.

[72]  R. Williams,et al.  Microbiology of extreme environments and its potential for biotechnology , 1989 .

[73]  F. Widdel,et al.  Dissimilatory Sulfate- and Sulfur-Reducing Prokaryotes , 2006 .

[74]  C. Rodrigues-Pousada,et al.  Studies on the Redox Centers of the Terminal Oxidase fromDesulfovibrio gigas and Evidence for Its Interaction with Rubredoxin* , 1997, The Journal of Biological Chemistry.

[75]  J. Lloyd,et al.  Reduction of Technetium by Desulfovibrio desulfuricans: Biocatalyst Characterization and Use in a Flowthrough Bioreactor , 1999, Applied and Environmental Microbiology.

[76]  H. Cypionka,et al.  The preferred electron acceptor of Desulfovibrio desulfuricans CSN , 1995 .

[77]  J. Santini,et al.  Two new arsenate/sulfate-reducing bacteria: mechanisms of arsenate reduction , 2000, Archives of Microbiology.

[78]  H. Whiteley,et al.  REDUCTION OF INORGANIC COMPOUNDS WITH MOLECULAR HYDROGEN BY MICROCOCCUS LACTILYTICUS I , 1962, Journal of bacteriology.

[79]  G. Southam,et al.  Bioaccumulation of gold by sulfate-reducing bacteria cultured in the presence of gold(I)-thiosulfate complex , 2006 .

[80]  L. Barton,et al.  The bacterial metallome: composition and stability with specific reference to the anaerobic bacterium Desulfovibrio desulfuricans , 2007, BioMetals.

[81]  D. Westlake,et al.  Distribution of Hydrogenase Genes in Desulfovibrio spp. and Their Use in Identification of Species from the Oil Field Environment , 1990, Applied and environmental microbiology.

[82]  E. Seagren,et al.  Review of Natural Attenuation of BTEX and MTBE in Groundwater , 2002 .

[83]  E. Landa Microbial biogeochemistry of uranium mill tailings. , 2005, Advances in applied microbiology.

[84]  H. Sigel,et al.  Nickel and its role in biology , 1988 .

[85]  R. Bryant,et al.  Localization of cytochromes in the outer membrane of Desulfovibrio vulgaris (Hildenborough) and their role in anaerobic biocorrosion. , 1995, Anaerobe.

[86]  Alice Dohnalkova,et al.  Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[87]  I. Pereira,et al.  Sulfate-reducing bacteria in human feces and their association with inflammatory bowel diseases. , 2002, FEMS microbiology ecology.

[88]  F. Guerlesquin,et al.  The crystal structure of the hexadeca-heme cytochrome Hmc and a structural model of its complex with cytochrome c(3). , 2002, Structure.

[89]  E. Roden,et al.  Enzymatic iron and uranium reduction by sulfate-reducing bacteria , 1993 .

[90]  D. Lovley,et al.  Novel Processes for Anaerobic Sulfate Production from Elemental Sulfur by Sulfate-Reducing Bacteria , 1994, Applied and environmental microbiology.

[91]  Tori M. Hoehler,et al.  Field and laboratory studies of methane oxidation in an anoxic marine sediment: Evidence for a methanogen‐sulfate reducer consortium , 1994 .

[92]  G. Gadd,et al.  An integrated microbial process for the bioremediation of soil contaminated with toxic metals , 1998, Nature Biotechnology.

[93]  C. Rodrigues-Pousada,et al.  Deletion of flavoredoxin gene in Desulfovibrio gigas reveals its participation in thiosulfate reduction , 2005, FEBS letters.

[94]  G. De Luca,et al.  Reduction of Technetium(VII) byDesulfovibrio fructosovorans Is Mediated by the Nickel-Iron Hydrogenase , 2001, Applied and Environmental Microbiology.

[95]  L. Barton,et al.  Characteristics and Activities of Sulfate-Reducing Bacteria , 1995 .

[96]  H. Cypionka,et al.  Oxygen respiration by desulfovibrio species. , 2000, Annual review of microbiology.

[97]  J. Storhoff,et al.  A DNA-based method for rationally assembling nanoparticles into macroscopic materials , 1996, Nature.

[98]  W. Lutze,et al.  Using Cytochrome c{sub 3} to Make Selenium Nanowires , 1999 .

[99]  D. R. Bond,et al.  Shewanella secretes flavins that mediate extracellular electron transfer , 2008, Proceedings of the National Academy of Sciences.

[100]  C. Gomes,et al.  The ‘strict’ anaerobe Desulfovibrio gigas contains a membrane‐bound oxygen‐reducing respiratory chain , 2001, FEBS letters.

[101]  B. Guigliarelli,et al.  Hydrogenases in sulfate-reducing bacteria function as chromium reductase , 2003, Applied Microbiology and Biotechnology.

[102]  J. García,et al.  Characterization of Desulfovibrio fructosovorans sp. nov. , 1988, Archives of Microbiology.

[103]  O. Drzyzga,et al.  Coexistence of a sulphate-reducing Desulfovibrio species and the dehalorespiring Desulfitobacterium frappieri TCE1 in defined chemostat cultures grown with various combinations of sulfate and tetrachloroethene. , 2001, Environmental microbiology.

[104]  A. Bull Microbial Diversity and Bioprospecting , 2003 .

[105]  F. Widdel,et al.  The Genus Desulfuromonas and Other Gram-Negative Sulfur-Reducing Eubacteria , 1992 .

[106]  G. Goth,et al.  Third wire or third rail? [Broadband Internet access] , 2004, IEEE Internet Computing.

[107]  F. Widdel,et al.  Corroding iron as a hydrogen source for sulphate reduction in growing cultures of sulphate-reducing bacteria , 1986, Applied Microbiology and Biotechnology.

[108]  D. Lovley,et al.  Reduction of uranium by cytochrome c3 of Desulfovibrio vulgaris , 1993, Applied and environmental microbiology.

[109]  Anna Obraztsova,et al.  Sulfate-reducing bacterium grows with Cr(VI), U(VI), Mn(IV), and Fe(III) as electron acceptors , 1998 .

[110]  Derek R. Lovley,et al.  Enzymic uranium precipitation , 1992 .

[111]  J. A. Hardy Utilisation of Cathodic Hydrogen by Sulphate-Reducing Bacteria , 1983 .

[112]  B. Patel,et al.  Desulforegula conservatrix gen. nov., sp. nov., a long-chain fatty acid-oxidizing, sulfate-reducing bacterium isolated from sediments of a freshwater lake. , 2001, International journal of systematic and evolutionary microbiology.

[113]  M. Teixeira,et al.  Characterization of a heme c nitrite reductase from a non-ammonifying microorganism, Desulfovibrio vulgaris Hildenborough. , 2000, Biochimica et biophysica acta.

[114]  A. Stolz Basic and applied aspects in the microbial degradation of azo dyes , 2001, Applied Microbiology and Biotechnology.

[115]  R. Cord-Ruwisch Microbially influenced corrosion of steel , 2000 .

[116]  D. Hervé,et al.  Structure-function relationship in hemoproteins: The role of cytochrome c3 in the reduction of colloidal sulfur by sulfate-reducing bacteria , 1979, Archives of Microbiology.

[117]  H. D. Peck,et al.  Inorganic microbial sulfur metabolism , 1994 .

[118]  N. Pfennig,et al.  Chemolithotrophic growth of Desulfovibrio sulfodismutans sp. nov. by disproportionation of inorganic sulfur compounds , 1987, Archives of Microbiology.

[119]  L. Barton,et al.  Sulphate-reducing bacteria: environmental and engineered systems. , 2007 .

[120]  R. S. Burkhalter,et al.  Iron Uroporphyrin I and a Heme c-Derivative Are Prosthetic Groups in Desulfovibrio gigas Rubredoxin Oxidase1 , 1994 .

[121]  Byung Hong Kim,et al.  Petroleum desulfurization byDesulfovibrio desulfuricans M6 using electrochemically supplied reducing equivalent , 1990, Biotechnology Letters.

[122]  B. Patel,et al.  Desulfovibrio aminophilus sp. nov., a novel amino acid degrading and sulfate reducing bacterium from an anaerobic dairy wastewater lagoon. , 1998, Systematic and applied microbiology.

[123]  A. Lino,et al.  Anaerobic reduction of a sulfonated azo dye, Congo Red, by sulfate-reducing bacteria , 2002, Applied biochemistry and biotechnology.

[124]  R. Huber,et al.  Crystal structure of the first dissimilatory nitrate reductase at 1.9 A solved by MAD methods. , 1999, Structure.

[125]  Purification and Preliminary Characterization of Tetraheme Cytochrome c3 and Adenylylsulfate Reductase from the Peptidolytic Sulfate-Reducing Bacterium Desulfovibrio aminophilus DSM 12254 , 2005, Bioinorganic chemistry and applications.

[126]  M. Reinhard,et al.  Anaerobic degradation of toluene and xylene by aquifer microorganisms under sulfate-reducing conditions , 1992, Applied and environmental microbiology.

[127]  G. Voordouw,et al.  Sulphate-reducing Bacteria: Biochemical, genetic and genomic characterization of anaerobic electron transport pathways in sulphate-reducing Delta proteobacteria , 2007 .

[128]  J. Zeyer,et al.  Activity and Diversity of Sulfate-Reducing Bacteria in a Petroleum Hydrocarbon-Contaminated Aquifer , 2002, Applied and Environmental Microbiology.

[129]  T. J. Britz,et al.  Isolation of saccharolytic dissimilatory sulfate-reducing bacteria , 1987 .

[130]  B. Ollivier,et al.  Anaerobes: the Sulfate‐Reducing Bacteria as an Example of Metabolic Diversity , 2004 .

[131]  S. Ezaki,et al.  Isolation and transcriptional analysis of novel tetrachloroethene reductive dehalogenase gene from Desulfitobacterium sp. strain KBC1 , 2005, Applied Microbiology and Biotechnology.

[132]  M. Bruschi,et al.  Kinetic studies on the electron transfer between various c-type cytochromes and iron (III) using a voltammetric approach , 1998 .

[133]  H. Cypionka,et al.  Chemolithotrophic growth ofDesulfovibrio desulfuricans with hydrogen coupled to ammonification of nitrate or nitrite , 1986, Archives of Microbiology.

[134]  M. Teixeira,et al.  Characterization of the Desulfovibrio desulfuricans ATCC 27774 DsrMKJOP complex--a membrane-bound redox complex involved in the sulfate respiratory pathway. , 2006, Biochemistry.

[135]  A. Ogram,et al.  Phylogeny of sulfate‐reducing bacteria , 2000 .

[136]  R. Taylor,et al.  Thermophilic biodegradation of BTEX by two consortia of anaerobic bacteria , 1997, Applied Microbiology and Biotechnology.

[137]  P. Barnes,et al.  Bioremediation of benzene, ethylbenzene, and xylenes in groundwater under iron‐amended, sulfate‐reducing conditions , 2007, Environmental toxicology and chemistry.

[138]  D. Strik,et al.  Application of redox mediators to accelerate the transformation of reactive azo dyes in anaerobic bioreactors. , 2001, Biotechnology and bioengineering.

[139]  J. Moura,et al.  Simple and Complex Iron-Sulfur Proteins in Sulfate Reducing Bacteria , 1999 .

[140]  J. Wall,et al.  Uranium Reduction by Desulfovibrio desulfuricans Strain G20 and a Cytochrome c3 Mutant , 2002, Applied and Environmental Microbiology.

[141]  F. Widdel,et al.  Anaerobic bacterial metabolism of hydrocarbons , 1998 .

[142]  L. Barton,et al.  Energy coupling to nitrite respiration in the sulfate-reducing bacterium Desulfovibrio gigas , 1983, Journal of bacteriology.

[143]  G. Fauque [24] Sulfur reductase from thiophilic sulfate-reducing bacteria , 1994 .

[144]  A. Stams,et al.  The ecology and biotechnology of sulphate-reducing bacteria , 2008, Nature Reviews Microbiology.

[145]  R. Parkes,et al.  Sulphate-reducing Bacteria: The sub-seafloor biosphere and sulphate-reducing prokaryotes: their presence and significance , 2007 .

[146]  P. Lawson,et al.  Desulfitobacterium sp. strain PCE1, an anaerobic bacterium that can grow by reductive dechlorination of tetrachloroethene or ortho-chlorinated phenols , 1996, Archives of Microbiology.

[147]  O. Drzyzga,et al.  Dehalogenation of chlorinated ethenes and immobilization of nickel in anaerobic sediment columns under sulfidogenic conditions. , 2002, Environmental science & technology.

[148]  J. Fry,et al.  Bacterial populations and processes in sediments containing gas hydrates (ODP Leg 146: Cascadia Margin) , 1996 .

[149]  J. Le Gall,et al.  Anaerobes response to oxygen: the sulfate-reducing bacteria. , 1996, Anaerobe.

[150]  O. Klimmek,et al.  [25] Sulfur reductases from spirilloid mesophilic sulfur-reducing eubacteria , 1994 .

[151]  D. Blowes,et al.  Rates of sulfate reduction and metal sulfide precipitation in a permeable reactive barrier , 2002 .

[152]  W. Ludwig,et al.  Complete oxidation of toluene under strictly anoxic conditions by a new sulfate-reducing bacterium , 1993, Applied and environmental microbiology.

[153]  L. Barton,et al.  Reduction and Immobilization of Molybdenum by Desulfovibrio desulfuricans , 1997 .

[154]  C. Soares,et al.  Sulphate respiration from hydrogen in Desulfovibrio bacteria: a structural biology overview. , 2005, Progress in biophysics and molecular biology.

[155]  L. Young,et al.  Anaerobic degradation of toluene by a denitrifying bacterium , 1991, Applied and environmental microbiology.

[156]  V. Shnyrov,et al.  A new type of metal-binding site in cobalt- and zinc-containing adenylate kinases isolated from sulfate-reducers Desulfovibrio gigas and Desulfovibrio desulfuricans ATCC 27774. , 2008, Journal of inorganic biochemistry.

[157]  M. Santana Presence and expression of terminal oxygen reductases in strictly anaerobic sulfate-reducing bacteria isolated from salt-marsh sediments. , 2008, Anaerobe.

[158]  M. Teixeira,et al.  A novel membrane-bound respiratory complex from Desulfovibrio desulfuricans ATCC 27774. , 2003, Biochimica et biophysica acta.

[159]  W. Babel,et al.  A Desulfovibrio sp. capable of growing by reducing U(VI) , 1999 .

[160]  H. Cypionka Solute Transport and Cell Energetics , 1995 .

[161]  M. Inui,et al.  Complete Genome Sequence of the Dehalorespiring Bacterium Desulfitobacterium hafniense Y51 and Comparison withDehalococcoides ethenogenes 195 , 2006, Journal of bacteriology.

[162]  J. Libra,et al.  Reduction of azo dyes by desulfovibrio desulfuricans , 2000 .

[163]  Rekha Seshadri,et al.  The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough , 2004, Nature Biotechnology.

[164]  E. Delong,et al.  Growth and Population Dynamics of Anaerobic Methane-Oxidizing Archaea and Sulfate-Reducing Bacteria in a Continuous-Flow Bioreactor , 2005, Applied and Environmental Microbiology.

[165]  M. Teixeira,et al.  Hemeproteins in anaerobes , 1998 .

[166]  K. Nealson,et al.  Iron and manganese in anaerobic respiration: environmental significance, physiology, and regulation. , 1994, Annual review of microbiology.

[167]  D. Dervartanian Desulforubidin: dissimilatory, high-spin sulfite reductase of Desulfomicrobium species. , 1994, Methods in enzymology.

[168]  R. Bartha,et al.  The Sulphate-Reducing Bacteria , 1979 .

[169]  Shi Liang,et al.  導電性ナノワイヤーをShewanella oneidensis菌MR‐1菌株その他の微生物が生成する , 2006 .

[170]  Ramaraj Boopathy,et al.  Characterization of partial anaerobic metabolic pathway for 2,4,6-trinitrotoluene degradation by a sulfate-reducing bacterial consortium. , 1996, Canadian journal of microbiology.

[171]  K. Knöller,et al.  Sulfur and oxygen isotope fractionation during benzene, toluene, ethyl benzene, and xylene degradation by sulfate-reducing bacteria. , 2006, Environmental science & technology.

[172]  A. Jayaraman,et al.  Inhibiting sulfate-reducing bacteria in biofilms by expressing the antimicrobial peptides indolicidin and bactenecin , 1999, Journal of Industrial Microbiology and Biotechnology.

[173]  A. Spormann,et al.  Lactate conversion to acetate, CO2 and H2 in cell suspensions of Desulfovibrio vulgaris (Marburg): indications for the involvement of an energy driven reaction , 1988, Archives of Microbiology.

[174]  A. Luptáková,et al.  Bioremediation of acid mine drainage contaminated by SRB , 2005 .

[175]  S. Hanada,et al.  A novel lineage of sulfate-reducing microorganisms: Thermodesulfobiaceae fam. nov., Thermodesulfobium narugense, gen. nov., sp. nov., a new thermophilic isolate from a hot spring , 2003, Extremophiles.

[176]  C. Dahl,et al.  Dissimilatory sulphite reductase from Archaeoglobus fulgidus: physico-chemical properties of the enzyme and cloning, sequencing and analysis of the reductase genes. , 1993, Journal of general microbiology.

[177]  G. Diekert,et al.  Anaerobic transformation of 2,4,6-trinitrotoluene (TNT) , 2004, Archives of Microbiology.

[178]  B. Ollivier,et al.  Biochemical and spectroscopic characterization of an aldehyde oxidoreductase isolated from Desulfovibrio aminophilus. , 2006, Journal of inorganic biochemistry.

[179]  I. Moura,et al.  Low-spin sulfite reductases , 1994 .

[180]  L. Barton,et al.  TEM investigation of U{sup 6+} and Re{sup 7+} reduction by Desulfovibrio desulfuricans, a sulfate-reducing bacterium , 1999 .

[181]  J. Sunner,et al.  Sulphate-reducing Bacteria: Sulphate-reducing bacteria and their role in corrosion of ferrous materials , 2007 .

[182]  M. Y. Liu,et al.  Purification and characterization of desulfoferrodoxin. A novel protein from Desulfovibrio desulfuricans (ATCC 27774) and from Desulfovibrio vulgaris (strain Hildenborough) that contains a distorted rubredoxin center and a mononuclear ferrous center. , 1990, The Journal of biological chemistry.

[183]  L. Macaskie,et al.  Biorecovered precious metals from industrial wastes: single-step conversion of a mixed metal liquid waste to a bioinorganic catalyst with environmental application. , 2006, Environmental science & technology.

[184]  H. D. Peck THE ATP-DEPENDENT REDUCTION OF SULFATE WITH HYDROGEN IN EXTRACTS OF DESULFOVIBRIO DESULFURICANS. , 1959, Proceedings of the National Academy of Sciences of the United States of America.

[185]  H. Cypionka,et al.  Sulfate formation via ATP sulfurylase in thiosulfate- and sulfite-disproportionating bacteria , 1989, Archives of Microbiology.

[186]  G. Aromí,et al.  Synthesis of 3d metallic single-molecule magnets , 2006 .

[187]  M. A. Carrondo,et al.  The primary and three-dimensional structures of a nine-haem cytochrome c from Desulfovibrio desulfuricans ATCC 27774 reveal a new member of the Hmc family. , 1999, Structure.

[188]  Jeffrey A Cunningham,et al.  Enhanced in situ bioremediation of BTEX-contaminated groundwater by combined injection of nitrate and sulfate. , 2001, Environmental science & technology.

[189]  E. Hatchikian A cobalt porphyrin containing protein reducible by hydrogenase isolated from Desulfovibrio desulfuricans (Norway). , 1981, Biochemical and biophysical research communications.

[190]  L. Barton,et al.  Variations in autotrophic life , 1991 .

[191]  O. Drzyzga,et al.  Influence of Different Electron Donors and Acceptors on Dehalorespiration of Tetrachloroethene byDesulfitobacterium frappieri TCE1 , 1999, Applied and Environmental Microbiology.

[192]  C. Dahl,et al.  Enzymology and molecular biology of sulfate reduction in extremely thermophilic archaeon Archaeoglobus fulgidus. , 1994, Methods in enzymology.

[193]  Derek R. Lovley,et al.  Reduction of Chromate by Desulfovibrio vulgaris and Its c3 Cytochrome , 1994, Applied and environmental microbiology.

[194]  D. Jones,et al.  Anaerobic hydrocarbon biodegradation in deep subsurface oil reservoirs , 2004, Nature.

[195]  Jules B van Lier,et al.  Review paper on current technologies for decolourisation of textile wastewaters: perspectives for anaerobic biotechnology. , 2007, Bioresource technology.

[196]  P G Whitehead,et al.  Chemical behaviour of the Wheal Jane bioremediation system. , 2005, The Science of the total environment.

[197]  D. Lovley Microbial Reduction of Iron, Manganese, and other Metals , 1995 .

[198]  L. Barton,et al.  Transformation of selenate and selenite to elemental selenium byDesulfovibrio desulfuricans , 1995, Journal of Industrial Microbiology.

[199]  R. Louro,et al.  Iron‐coproporphyrin III is a natural cofactor in bacterioferritin from the anaerobic bacterium Desulfovibrio desulfuricans , 2000, FEBS letters.

[200]  D. Cullimore,et al.  Microbiology of Well Biofouling , 1999 .

[201]  F. Widdel,et al.  Anaerobic Oxidation of o -Xylene, m -Xylene, and Homologous Alkylbenzenes by New Types of Sulfate-Reducing Bacteria , 1999, Applied and Environmental Microbiology.

[202]  F. Lépine,et al.  Spectrum of the Reductive Dehalogenation Activity of Desulfitobacterium frappieri PCP-1 , 1998, Applied and Environmental Microbiology.

[203]  M. Teixeira,et al.  Biochemical, proteomic and genetic characterization of oxygen survival mechanisms in sulphate-reducing bacteria of the genus Desulfovibrio , 2007 .

[204]  M. Bruschi,et al.  Kinetic studies on the electron transfer between bacterial c-type cytochromes and metal oxides , 1998 .

[205]  Dianne K. Newman,et al.  A role for excreted quinones in extracellular electron transfer , 2000, Nature.

[206]  L. M. Saraiva,et al.  In the facultative sulphate/nitrate reducer Desulfovibrio desulfuricans ATCC 27774, the nine-haem cytochrome c is part of a membrane-bound redox complex mainly expressed in sulphate-grown cells. , 2001, Biochimica et biophysica acta.

[207]  M. Bruschi,et al.  A cobalt containing protein isolated from Desulfovibrio gigas, a sulfate reducer. , 1980, Biochemical and biophysical research communications.

[208]  R. Sanford,et al.  Fraction of Electrons Consumed in Electron Acceptor Reduction and Hydrogen Thresholds as Indicators of Halorespiratory Physiology , 1999, Applied and Environmental Microbiology.

[209]  L. Macaskie,et al.  Biosorption of palladium and platinum by sulfate‐reducing bacteria , 2004 .

[210]  P. Alvarez,et al.  Assessment of anaerobic benzene degradation potential using 16S rRNA gene-targeted real-time PCR. , 2007, Environmental microbiology.

[211]  B. Ollivier,et al.  Sulphate-reducing Bacteria: Sulphate-reducing bacteria from oil field environments and deep-sea hydrothermal vents , 2007 .

[212]  I. Moura,et al.  Spectroscopic properties of desulfoferrodoxin from Desulfovibrio desulfuricans (ATCC 27774). , 1994, The Journal of biological chemistry.

[213]  Guy D. Fauque,et al.  Ecology of Sulfate-Reducing Bacteria , 1995 .

[214]  R. Iwakiri,et al.  Isolation and Characterization of Desulfitobacterium sp. strain Y51 Capable of Efficient Dehalogenation of Tetrachloroethene and Polychloroethanes , 2001, Bioscience, biotechnology, and biochemistry.

[215]  J. Odom,et al.  The Sulfate-Reducing Bacteria: Contemporary Perspectives , 1993, Brock/Springer Series in Contemporary Bioscience.

[216]  E. A. Greene,et al.  Synergistic Inhibition of Microbial Sulfide Production by Combinations of the Metabolic Inhibitor Nitrite and Biocides , 2006, Applied and Environmental Microbiology.

[217]  L. Young,et al.  Dehalogenation of lindane (γ-hexachlorocyclohexane) by anaerobic bacteria from marine sediments and by sulfate-reducing bacteria , 1999 .

[218]  G. Gadd,et al.  Sulphate-reducing Bacteria: Bioremediation of metals and metalloids by precipitation and cellular binding , 2007 .

[219]  C. Dahl,et al.  Spectroscopic studies on APS reductase isolated from the hyperthermophilic sulfate-reducing archaebacterium Archaeglobus fulgidus. , 1991, Biochemical and biophysical research communications.

[220]  Joseph M. Suflita,et al.  Metabolism of Environmental Contaminants by Mixed and Pure Cultures of Sulfate-Reducing Bacteria , 1995 .

[221]  F. Widdel,et al.  Anaerobic degradation of benzene by a marine sulfate-reducing enrichment culture, and cell hybridization of the dominant phylotype. , 2007, Environmental microbiology.

[222]  B. Thomson,et al.  LONG-TERM STABILITY OF METALS IMMOBILIZED BY MICROBIAL REDUCTION , 2000 .

[223]  D. Lovley,et al.  Reduction of uranium by Desulfovibrio desulfuricans , 1992, Applied and environmental microbiology.

[224]  K. Schleifer,et al.  The Prokaryotes. A handbook on the biology of bacteria: ecophysiology, isolation, identification, applications. Volumes I-IV. , 1992 .

[225]  C. Dahl,et al.  Microbial sulfur metabolism , 2008 .

[226]  Olivier Braissant,et al.  Exopolymeric substances of sulfate‐reducing bacteria: Interactions with calcium at alkaline pH and implication for formation of carbonate minerals , 2007 .

[227]  C. Costa,et al.  Nitrate and nitrite utilization in sulfate-reducing bacteria. , 1997, Anaerobe.