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Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals

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Abstract

The gram-negative metal-reducing microorganism, previously known as strain GS-15, was further characterized. This strict anaerobe oxidizes several short-chain fatty acids, alcohols, and monoaromatic compounds with Fe(III) as the sole electron acceptor. Furthermore, acetate is also oxidized with the reduction of Mn (IV), U (VI), and nitrate. In whole cell suspensions, the c-type cytochrome(s) of this organism was oxidized by physiological electron acceptors and also by gold, silver, mercury, and chromate. Menaquinone was recovered in concentrations comparable to those previously found in gram-negative sulfate reducers. Profiles of the phospholipid ester-linked fatty acids indicated that both the anaerobic desaturase and the branched pathways for fatty acid biosynthesis were operative. The organism contained three lipopolysaccharide hydroxy fatty acids which have not been previously reported in microorganisms, but have been observed in anaerobic freshwater sediments. The 16S rRNA sequence indicated that this organism belongs in the delta proteobacteria. Its closest known relative is Desulfuromonas acetoxidans. The name Geobacter metallireducens is proposed.

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References

  • Balashova VV, Zavarzin GA (1980) Anaerobic reduction of ferric iron by hydrogen bacteria. Microbiology 48: 635–639

    Google Scholar 

  • Blakemore RP (1982) Magnetotactic bacteria. Ann Rev Microbiol 36: 217–238

    Google Scholar 

  • Blakemore RP, Frankel RB (1989) Biomineralization by magnetogenic bacteria. In: Poole RK, Gadd GM (eds) Metal-microbe interactions. IRL Press, New York, pp 85–98

    Google Scholar 

  • Bligh EG, Dyer WJ (1959) A rapid method of total lipid extration and purification. Can J Biochem Physiol 37: 911–917

    Google Scholar 

  • Brandis-Heep A, Gebhardt NA, Thauer RK, Widdel F, Pfennig N (1983) Anaerobic acetate oxidation to CO2 by Desulfobacter postgatei. Arch Microbiol 136: 222–229

    Google Scholar 

  • Britschgi TB, Giovannoni SJ (1991) Phylogenetic analysis of a natural marine bacterioplankton population by rRNA gene cloning and sequencing. Appl Environ Microbiol 57: 1707–1713

    Google Scholar 

  • Brosius J, Dull TJ, Sleeter DD, Noller HF (1981) Gene organization and primary structure of a ribosomal RNA operon from Escherichia coli. J Mol Biol 148: 107–127

    Google Scholar 

  • Caccavo FJr, Blakemore RP, Lovley DR (1992) A hydrogenoxidizing, Fe(III)-reducing microorganism from the Great Bay Estuary, New Hampshire. Appl Environ Microbiol 58: 3211–3216

    Google Scholar 

  • Champine JE, Goodwin S (1991) Acetate catabolism in the dissimilatory iron-reducing isolate GS-15. J Bacteriol 173: 2704–2706

    Google Scholar 

  • Christie WW (1989). Gas chromatography and lipids. The Oily Press, Ayr, Scotland

    Google Scholar 

  • Collins MD, Jones D (1981) Distribution of isoprenoid quinone structural types in bacteria and their taxonomic implications. Microbiol Rev 45: 316–354

    Google Scholar 

  • Conti SF, Gettner ME (1962) Electron microscopy of cellular division in Escherichia coli. J Bacteriol 83: 544–550

    Google Scholar 

  • Dowling NJE, Widdel F, White DC (1986) Phospholipid esterlinked fatty acid biomarkers of acetate-oxidizing sulfate reducers and other sulfide forming bacteria. J Gen Microbiol 132: 1815–1825

    Google Scholar 

  • Eden PA, Schmidt TM, Blakemore RP, Pace NR (1991). Phylogenetic analysis of Aquaspirillum magnetotacticum using PCR-Amplified 16S ribosomal RNA-Specific DNA. In: Frankel RB, Blakemore RP (eds) Iron biominerals. Plenum Press, New York, NY, pp 127–130

    Google Scholar 

  • Edlund A, Nichols PD, Roffey R, White DC (1985) Extractable and lipopolysaccharide fatty acid and hydroxy acid profiles from Desulfovibrio species. J Lipid Res 26: 982–988

    Google Scholar 

  • Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 155: 279–284

    Google Scholar 

  • Giovannoni SJ (1991) The polymerase chain reduction. In: Stakkebrandt E., Goodfellow M (eds) Modern microbial methods: sequencing and hybridization techniques in bacterial systematics. Wiley, Chichester, pp 177–203

    Google Scholar 

  • Gorby Y, Lovley DR (1991) Electron transport in the dissimilatory iron-reducer, GS-15. Appl Environ Microbiol 57: 867–870

    Google Scholar 

  • Gorby YA, Lovley DR (1992) Enzymatic uranium precipitation. Environ Sci Technol 26: 205–207

    Google Scholar 

  • Guckert JB, Antworth CP, Nichols PD, White DC (1985) Phospholipid, ester-linked fatty acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sediments. FEMS Microbiol Ecol 31: 147–158

    Google Scholar 

  • Jones JG, Davison W, Gardener S (1984) Iron reduction by bacteria: range of organisms involved and metals reduced. FEMS Microbiol Lett 21: 133–136

    Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism. Academic Press, New York, pp 21–132

    Google Scholar 

  • Krivankova L, Dadak V (1980) Semimicro extraction of ubiquinone and menaquinone from bacteria. Methods Enzymol 67: 111–114

    Google Scholar 

  • Kroger A (1978) Determination of contents and redox states of ubiquinone and menaquinone. Methods Enzymol 53: 579–591

    Google Scholar 

  • Lane DL, Pace B, Olsen GJ, Stahl D, Sogin ML, Pace NR (1985) Rapid determination of 16S ribosomal RNA sequences for phylogenetic analysis. Proc Natl Acad Sci USA 82: 6955–6959

    Google Scholar 

  • LeGall J, Fauque G (1988) Dissimilatory reduction of sulfur compounds. In: Zehnder AJB (ed) Biology of anaerobic microorganisms. Wiley, New York, pp 587–639

    Google Scholar 

  • Lovley DR (1991a) Dissimilatory Fe(III) and Mn(IV) reduction. Microbiol Rev 55: 259–287

    Google Scholar 

  • Lovley DR (1991b) Magnetite formation during microbial dissimilatory iron reduction. In: Frankel RB, Blakemore RP (eds) Iron biominerals. Plenum Press, New York, pp 151–166

    Google Scholar 

  • Lovley DR, Baedecker MJ, Lonergan DJ, Cozzarelli IM, Phillips EJP, Siegel DI (1989a) Oxidation of aromatic contaminants coupled to microbial iron reduction. Nature 339: 297–299

    Google Scholar 

  • Lovley DR, Chapelle FH, Phillips EJP (1990)Fe(III)-reducing bacteria in deeply buried sediments of the Atlantic Coastal Plain. Geology 18: 954–957

    Google Scholar 

  • Lovley DR, Lonergan DJ (1990) Anaerobic oxidation of toluene, phenol, and p-cresol by the dissimilatory iron-reducing organism, GS-15. Appl Environ Microbiol 56: 1858–1864

    Google Scholar 

  • Lovley DR, Phillips EJP (1986) Organic matter mineralization with reduction of ferric iron in anaerobic sediments. Appl Environ Microbiol 51: 683–689

    Google Scholar 

  • Lovley DR, Phillips EJP (1988a) Manganese inhibition of microbial iron reduction in anaerobic sediments. Geomicrobiol J 6: 145–155

    Google Scholar 

  • Lovley DR, Phillips EJP (1988b) Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese. Appl Environ Microbiol 54: 1472–1480

    Google Scholar 

  • Lovley DR, Phillips EJP (1989) Requirement for a microbial consortium to completely oxidize glucose in Fe(III)-reducing sediments. Appl Environ Microbiol 55: 3234–3236

    Google Scholar 

  • Lovley DR, Phillips EJP (1991) Reduction of U(VI) by Desulfovibrio desulfuricans. Appl Environ Microbiol 58: 850–856

    Google Scholar 

  • Lovley DR, Phillips EJP, Gorby YA, Landa ER (1991a) Microbial reduction of uranium. Nature 350: 413–416

    Google Scholar 

  • Lovley DR, Phillips EJP, Lonergan DJ (1989b) Hydrogen and formate oxidation coupled to dissimilatory reduction of iron or manganese by Alteromonas putrefaciens. Appl Environ Microbiol 55: 700–706

    Google Scholar 

  • Lovley DR, Phillips EJP, Lonergan DJ (1991b) Enzymatic versus nonenzymatic mechanisms for Fe(III) reduction in aquatic sediments. Environ Sci Technol 25: 1062–1067

    Google Scholar 

  • Lovley DR, Stolz JF, Nord GL, Phillips EJP (1987) Anaerobic production of magnetite by a dissimilatory iron-reducing microorganism. Nature 330: 252–254

    Google Scholar 

  • MacDonell MT, Colwell RR (1985) A phylogeny for the Vibrionaceae, and recommendation for two new genera, Listonella and Shewanella. Syst Appl Microbiol 6: 171–182

    Google Scholar 

  • Marmur J, Doty P (1962) Determination of the base composition of deoxyribonucleic acid from its thermal denaturation temperature J Mol Biol 5: 109–118

    Google Scholar 

  • Myers CR, Nealson KH (1988) Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science 240: 1319–1321

    Google Scholar 

  • Nichols PD, Guckert JB, White DC (1986) Determination of monounsaturated fatty acid double-bond position and geometry for microbial monocultures and complex consortia by capillary GC-MS of their dimethyl disulphide adducts. J Microbiol Methods 5: 49–55

    Google Scholar 

  • Nichols PD, Smith GA, Antworth CP, Hanson RS, White DC (1985) Phospholipid and lipopolysaccharide normal and hydroxy fatty acids as potential signatures for the methaneoxidizing bacteria. FEMS Microbiol Ecol 31: 327–335

    Google Scholar 

  • Parker JH, Smith GA, Fredrickson HL, Vestal JR, White DC (1982) Sensitive assay, based on hydroxy-fatty acids from lipopolysaccharide lipid A for gram-negative bacteria in sediments. Appl Environ Microbiol 44: 1170–1177

    Google Scholar 

  • Parkes RJ, Calder AG (1985) The cellular fatty acids of three strains of Desulfobulbus, a propionate-utilizing sulfate-reducing bacterium. FEMS Microbiol Ecol 31: 361–363

    Google Scholar 

  • Ponnamperuma FN (1972) The chemistry of submerged soils. Adv Agron 24: 29–96

    Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17: 208–212

    Google Scholar 

  • Ringelberg DB, Davis JD, Smith GA, Pfiffner SM, Nichols PD, Nickels JB, Hensen JM, Wilson JT, Yates M, Kampbell DH, Reed HW, Stocksdale TT, White DC (1988) Validation of signature polarlipid fatty acid biomarkers for alkane-utilizing bacteria in soils and subsurface aquifer materials. FEMS Microbiol Ecol 62: 39–50

    Google Scholar 

  • Schmitz RA, Bonch-Osmolovskaya EA, Thauer RK (1990) Different mechanisms fo acetate activation in Desulfurella acetivorans and Desulfuromonas acetooxidans. Arch Microbiol 154: 274–279

    Google Scholar 

  • Steed P, Murray RGE (1966) The cell wall and cell division in gram-negative bacteria. Can J Microbiol 12: 263–270

    Google Scholar 

  • Szewzyk R, Pfennig N (1987) Complete oxidation of catechol by the strictly anaerobic sulfate-reducing Desulfobacterium catecholicum sp. nov. Arch Microbiol 147: 163–168

    Google Scholar 

  • Thauer RK, Moller-Zinkhan D, Spormann AM (1989) Biochemistry of acetate catabolism in anaerobic chemotrophic bacteria. Ann Rev Microbiol 43: 43–67

    Google Scholar 

  • Tulloch AP (1990) Glycosides of hydroxy fatty acids. In: Kates M (ed) Handbook of lipid research, vol 6. Glycolipids, phosphoglycolipids, and sulfoglycolipids. Plenum Press, New York NY, pp 463–487

    Google Scholar 

  • Vestal JR, White DC (1989) Lipid analysis in microbial ecology. Quantitative approaches to the study of microbial communities. Bioscience 39: 535–541

    Google Scholar 

  • White DC (1988) Validation of quantitative analysis for microbial biomass, community structure, and metabolic activity. Adv Limnol 31: 1–18

    Google Scholar 

  • White DC, Davis WM, Nickels JS, King JD, Bobbie RJ (1979) Determination of the sedimentary microbial biomass by extractible lipid phosphate. Oecologia 40: 51–62

    Google Scholar 

  • Widdel F (1988) Microbiology and exology of sulfate- and sulfur-reducing bacteria. In: Zehnder AJB (ed) Biology of anaerobic microorganisms. Wiley, New York, pp 469–585

    Google Scholar 

  • Wilkinson SG (1988) Gram-negative Bacteria. In: Ratledge C, Wilkinson SG (eds) Microbial lipids. Academic Press, New York, NY, pp 299–488

    Google Scholar 

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Authors and Affiliations

  1. Water Resources Division, 430 National Center, U.S. Geological Survey, 22092, Reston, VA, USA

    D. R. Lovley, E. J. P. Phillips & Y. A. Gorby

  2. Department of Microbiology, Oregon State University, 97331, Corvallis, OR, USA

    S. J. Giovannoni

  3. Center for Environmental Biotechnology, University of Tennessee, 37932, Knoxville, TN, USA

    D. C. White

  4. Department of Microbiology, University of Massachusetts, 01003, Amherst, MA, USA

    J. E. Champine & S. Goodwin

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  1. D. R. Lovley
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  2. S. J. Giovannoni
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  7. S. Goodwin
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Lovley, D.R., Giovannoni, S.J., White, D.C. et al. Geobacter metallireducens gen. nov. sp. nov., a microorganism capable of coupling the complete oxidation of organic compounds to the reduction of iron and other metals. Arch. Microbiol. 159, 336–344 (1993). https://doi.org/10.1007/BF00290916

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  • DOI: https://doi.org/10.1007/BF00290916

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