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Anaerobic Hydrocarbon-Degrading Microorganisms: An Overview

  • F. Widdel
  • K. Knittel
  • A. Galushko

Abstract:

Anaerobic microorganisms that utilize hydrocarbons became known when aerobic microorganisms with such capacity had been already under study for many decades. Hydrocarbons may be utilized anaerobically with nitrate, iron(III), or sulfate as electron acceptor, under conditions of methanogenesis, or by anoxygenic photosynthesis. The most important degraders of the simplest hydrocarbon, methane, are distinct groups of archaea in association with bacteria that apparently reduce sulfate. Axenic cultures have not been isolated to date. Methane oxidation may be also coupled to denitrification. Degraders of non-methane hydrocarbons are phylogenetically diverse; they are members of the Proteobacteria and Firmicutes. Many species have been isolated in pure cultures. Anaerobic microorganisms utilizing hydrocarbons always exhibit much slower growth than their aerobic counterparts.

Keywords

Aromatic Hydrocarbon Sulfate Reduction Anaerobic Oxidation Anaerobic Biodegradation Anoxic Habitat 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Aeckersberg F, Bak F, Widdel F (1991) Anaerobic oxidation of saturated hydrocarbons to CO2 by a new type of sulfate-reducing bacterium. Arch Microbiol 156: 5–14.Google Scholar
  2. Aeckersberg F, Rainey FA, Widdel, F (1998) Growth, natural relationships, cellular fatty acids and metabolic adaptation of sulfate-reducing bacteria that utilize long-chain alkanes under anoxic conditions. Arch Microbiol 170: 361–369.PubMedGoogle Scholar
  3. Alperin MJ, Reeburgh WS (1985) Inhibition experiments on anaerobic methane oxidation. Appl Environ Microbiol 50: 940–945.PubMedGoogle Scholar
  4. Anders HJ, Kaetzke A, Kämpfer P, Ludwig W, Fuchs G (1995) Taxonomic position of aromatic-degrading denitrifying pseudomonad strains K 172 and KB 740 and their description as new members of the genera Thauera, as Thauera aromatica sp. nov., and Azoarcus, as Azoarcus evansii sp. nov., respectively, members of the beta subclass of the Proteobacteria. Int J Syst Bacteriol 45: 327–333.PubMedGoogle Scholar
  5. Anderson RT, Lovley DR (2000) Hexadecane decay by methanogenesis. Nature 404: 722–723.PubMedGoogle Scholar
  6. Annweiler E, Materna A, Safinowski M, Kappler A, Richnow HH, Michaelis W, Meckenstock RU (2000) Anaerobic degradation of 2-methylnaphthalene by a sulfate-reducing enrichment culture. Appl Environ Microbiol 66: 5329–5333.PubMedGoogle Scholar
  7. Annweiler E, Michaelis W, Meckenstock RU (2002) Identical ring cleavage products during anaerobic degradation of naphthalene, 2-methylnaphthalene, and tetralin indicate a new metabolic pathway. Appl Environ Microbiol 68: 852–858.PubMedGoogle Scholar
  8. Ball HA, Johnson HA, Reinhard M, Spormann AM (1996) Initial reactions in anaerobic ethylbenzene oxidation by a denitrifying bacterium, strain EB1. J Bacteriol 178: 5755–5761.PubMedGoogle Scholar
  9. Barnes RO, Goldberg ED (1976) Methane production and consumption in anoxic marine sediments. Geology 4: 297–300.Google Scholar
  10. Bastin ES, Greer FE, Merritt CA, Moulton G (1926) The presence of sulphate reducing bacteria in oil field waters. Science 63: 21–24.PubMedGoogle Scholar
  11. Beller HR (2000) Metabolic indicators for detecting in situ anaerobic alkylbenzene degradation. Biodegradation 11: 125–139.PubMedGoogle Scholar
  12. Beller HR, Edwards EA (2000) Anaerobic toluene activation by benzylsuccinate synthase in a highly enriched methanogenic culture. Appl Environ Microbiol 66: 5503–5505.PubMedGoogle Scholar
  13. Beller HR, Spormann AM (1997) Anaerobic activation of toluene and o-xylene by addition to fumarate in denitrifying strain T. J Bacteriol 179: 670–676.PubMedGoogle Scholar
  14. Beller HR, Reinhard M, Grbić-Galić D (1992) Metabolic by-products of anaerobic toluene degradation by sulfate-reducing enrichment cultures. Appl Environ Microbiol 58: 3192–3195.PubMedGoogle Scholar
  15. Beller HR, Ding W-H, Reinhard M (1995) Byproducts of anaerobic alkylbenzene metabolism useful as indicators of in situ bioremediation. Environ Sci Technol 29: 2864–2870.Google Scholar
  16. Beller HR, Spormann AM, Sharma PK, Cole JR, Reinhard M (1996) Isolation and characterization of a novel toluene-degrading sulfate-reducing bacterium. Appl Environ Microbiol 62: 1188–1196.PubMedGoogle Scholar
  17. Biegert T, Fuchs F, Heider J (1996) Evidence that anaerobic oxidation of toluene in the denitrifying bacterium Thauera aromatica is initiated by formation of benzylsuccinate from toluene and fumarate. Eur J Biochem 238: 661–668.PubMedGoogle Scholar
  18. Boetius A, Ravenschlag K, Schubert CJ, Rickert D, Widdel F, Gieseke A, Amann R, Jørgensen BB, Witte U, Pfannkuche O (2000) A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407: 623–626.PubMedGoogle Scholar
  19. Bonin P, Cravo-Laureau C, Michetey V, Hirschler-Réa A (2004) The anaerobic hydrocarbon-degrading bacteria: an overview. Ophelia 58: 243–254.Google Scholar
  20. Bonin PC, Michotey VD, Mouzdahir A, Rontani JF (2002) Anaerobic biodegradation of squalene: using DGGE to monitor the isolation of denitrifying bacteria taken from enrichment cultures. FEMS Microbiol Ecol 42: 37–49.PubMedGoogle Scholar
  21. Botton S, Parsons JR (2007) Degradation of BTX by dissimilatory iron-reducing cultures. Biodegradation 18: 371–381.PubMedGoogle Scholar
  22. Botton S, van Harmelen M, Braster M, Parsons JR, Röling WF (2007) Dominance of Geobacteraceae in BTX-degrading enrichments from an iron-reducing aquifer. FEMS Microbiol Ecol 62: 118–130.PubMedGoogle Scholar
  23. Bregnard TP, Haner A, Hohener P, Zeyer J (1997) Anaerobic degradation of pristane in nitrate-reducing microcosms and enrichment cultures. Appl Environ Microbiol 63: 2077–2081.PubMedGoogle Scholar
  24. Brysch K, Schneider C, Fuchs G, Widdel F (1987) Lithoautotrophic growth of sulfate-reducing bacteria, and description of Desulfobacterium autotrophicum gen. nov., sp. nov. Arch Microbiol 148: 264–274.Google Scholar
  25. Caldwell ME, Suflita JM (2000) Detection of phenol and benzoate as intermediates of anaerobic benzene biodegradation under different terminal electron-accepting conditions. Environ Sci Technol 34: 1216–1220.Google Scholar
  26. Callaghan AV, Gieg LM, Kropp KG, Suflita JM, Young LY (2006) Comparison of mechanisms of alkane metabolism under sulfate-reducing conditions among two bacterial isolates and a bacterial consortium. Appl Environ Microbiol 72: 4274–4282.Google Scholar
  27. Callaghan AV, Tierney M, Phelps CD, Young LY (2009) Anaerobic biodegradation of n-hexadecane by a nitrate-reducing consortium. Appl Environ Microbiol 75: 1339–1344.PubMedGoogle Scholar
  28. Coates JD, Chakraborty R, Lack JG, O’Connor SM, Cole KA, Bender KS, Achenbach LA (2001) Anaerobic benzene oxidation coupled to nitrate reduction in pure culture by two strains of Dechloromonas. Nature 411: 1039–1043.PubMedGoogle Scholar
  29. Cravo-Laureau C, Hirschler-Réa A, Matheron R, Grossi V (2004a) Growth and cellular fatty-acid composition of a sulphate-reducing bacterium, Desulfatibacillum aliphaticivorans strain CV2803T, grown on n-alkenes. Compt Rend Biol 327: 687–694.Google Scholar
  30. Cravo-Laureau C, Matheron R, Cayol J-L, Joulian C, Hirschler-Réa A (2004b) Desulfatibacillum aliphaticivorans gen. nov., sp. nov., an n-alkane- and n-alkene-degrading, sulfate-reducing bacterium. Int J Syst Evol Microbiol 54: 77–83.PubMedGoogle Scholar
  31. Cravo-Laureau C, Matheron R, Joulian C, Cayol JL, Hirschler-Réa A (2004c) Desulfatibacillum alkenivorans sp. nov., a novel n-alkene-degrading, sulfate-reducing bacterium, and emended description of the genus Desulfatibacillum. Int J Syst Evol Microbiol 54: 1639–1642.PubMedGoogle Scholar
  32. Cravo-Laureau C, Labat C, Joulian C, Matheron R, Hirschler-Réa A (2007) Desulfatiferula olefinivorans gen. nov., sp. nov., a long-chain n-alkene-degrading, sulfate-reducing bacterium. Int J Syst Evol Microbiol 57: 2699–2702.PubMedGoogle Scholar
  33. Davidova IA, Suflita JM (2005) Enrichment and isolation of anaerobic hydrocarbon-degrading bacteria. In Methods in Enzymology, vol. 397. JR Leadbetter (ed.). Amsterdam: Elsevier, pp. 17–34.Google Scholar
  34. Davidova IA, Duncan KE, Choi OK, Suflita JM (2006) Desulfoglaeba alkanexedens gen. nov., sp. nov., an n-alkane-degrading, sulfate-reducing bacterium. Int J Syst Evol Microbiol 56: 2737–2742.PubMedGoogle Scholar
  35. Davidova IA, Gieg LM, Duncan KE, Suflita JM (2007) Anaerobic phenanthrene mineralization by a carboxylating sulfate-reducing bacterial enrichment. ISME J 1: 436–442.PubMedGoogle Scholar
  36. Dolfing J, Zeyer J, Binder-Eicher P, Schwarzenbach RP (1990) Isolation and characterization of a bacterium that mineralizes toluene in the absence of molecular oxygen. Arch Microbiol 154: 336–341.PubMedGoogle Scholar
  37. Ehrenreich P (1996) Anaerobes Wachstum neuartiger sulfatreduzierende und nitratreducierende Bakterien auf n-Alkanen und Erdöl. Dissertation, University of Bremen. Shaker Verlag, Aachen.Google Scholar
  38. Ehrenreich P, Behrends A, Harder J, Widdel F (2000) Anaerobic oxidation of alkanes by newly isolated denitrifying bacteria. Arch Microbiol 173: 58–64.PubMedGoogle Scholar
  39. Elmén J, Pan W, Leung SY, Magyarosy A, Keasling JD (1997) Kinetics of toluene degradation by a nitrate-reducing bacterium isolated from a groundwater aquifer. Biotechnol Bioeng 55: 82–90.PubMedGoogle Scholar
  40. Elshahed MS, Gieg LM, McInerney MJ, Suflita JM (2001) Signature metabolites attesting to the in situ attenuation of alkylbenzenes in anaerobic environments. Environ Sci Technol 35: 682–689.PubMedGoogle Scholar
  41. Elvert M, Suess E, Whiticar MJ (1999) Anaerobic methane oxidation associated with marine gas hydrates: superlight C-isotopes from saturated and unsaturated C20 and C25 irregular isoprenoids. Naturwiss 86: 295–300.Google Scholar
  42. Ettwig KF, Shima S, van de Pas-Schoonen KT, Kahnt J, Medema MH, Op den Camp HJ, Jetten MS, Strous M (2008) Denitrifying bacteria anaerobically oxidize methane in the absence of Archaea. Environ Microbiol 10: 3164–3173.PubMedGoogle Scholar
  43. Evans PJ, Mang DT, Kim KS, Young LY (1991) Anaerobic degradation of toluene by a denitrifying bacterium. Appl Environ Microbiol 57: 1139–1145.PubMedGoogle Scholar
  44. Ficker M, Krastel K, Orlicky S, Edwards E (1999) Molecular characterization of a toluene-degrading methanogenic consortium. Appl Environ Microbiol 65: 5576–5585.PubMedGoogle Scholar
  45. Fischer-Romero C, Tindall B, Jüttner F (1996) Tolumonas auensis gen. nov., sp. nov., a toluene-producing bacterium from anoxic sediments of a freshwater lake. Int J Syst Bacteriol 46: 183–188.PubMedGoogle Scholar
  46. Foss S, Heyen U, Harder J (1998) Alcaligenes defragrans sp. nov., description of four strains isolated on alkenoic monoterpenes ((+)-menthene, alpha-pinene, 2-carene, and alpha-phellandrene) and nitrate. Syst Appl Microbiol 21: 237–244.PubMedGoogle Scholar
  47. Fries MR, Zhou J, Chee-Sandford J, Tiedje JM (1994) Isolation, characterization, and distribution of denitrifying toluene degraders from a variety of habitats. Appl Environ Microbiol 60: 2802–2810.PubMedGoogle Scholar
  48. Galushko A, Minz D, Schink B, Widdel F (1999) Anaerobic degradation of naphthalene by a pure culture of a novel type of marine sulphate-reducing bacterium. Environ Microbiol 1: 415–420.PubMedGoogle Scholar
  49. Galushko AS, Kiesele-Lang U, Kappler A (2003) Degradation of 2-methylnaphthalene by a sulfate-reducing enrichment culture of mesophilic freshwater bacteria. Polyc Arom Comp 23: 207–218.Google Scholar
  50. Gieg LM, Suflita JM (2002) Detection of anaerobic metabolites of saturated and aromatic hydrocarbons in petroleum-contaminated aquifers. Environ Sci Technol 36: 3755–3762.PubMedGoogle Scholar
  51. Gilewicz M, Monpert G, Acquaviva M, Mille G, Bertand J-C (1991) Anaerobic oxidation of 1-n-heptadecene by a marine denitrifying bacterium. Appl Microbiol Biotechnol 36: 252–256.Google Scholar
  52. Girguis PR, Orphan VJ, Hallam SJ, DeLong EF (2003) Growth and methane oxidation rates of anaerobic methanotrophic archaea in a continuous-flow bioreactor. Appl Environ Microbiol 69: 5472–5482.PubMedGoogle Scholar
  53. Girguis PR, Cozen AE, DeLong EF (2005) Growth and population dynamics of anaerobic methane-oxidizing archaea and sulphate-reducing bacteria in a continuous-flow bioreactor. Appl Environ Microbiol 71: 3725–3733.PubMedGoogle Scholar
  54. Grbić-Galić D, Vogel TM (1987) Transformation of toluene and benzene by mixed methanogenic cultures. Appl Environ Microbiol 53: 254–260.PubMedGoogle Scholar
  55. Grishchenkov VG, Slepen’kin AV, Boronin AM (2002) Anaerobic degradation of biphenyl by the facultative anaerobic strain Citrobacter freundii BS2211. Appl Biochem Microbiol 38: 125–128.Google Scholar
  56. Grossi V, Cravo-Laureau C, Méou A, Raphel D, Garzino F, Hirschler-Réa A (2007) Anaerobic 1-alkene metabolism by the alkane- and alkene-degrading sulfate reducer Desulfatibacillum aliphaticivorans strain CV2803 T. Appl Environ Microbiol 73: 7882–7890.PubMedGoogle Scholar
  57. Grossi V, Cravo-Laureau C, Guyoneaud R, Ranchou-Peyruse A, Hirschler-Réa A (2008) Metabolism of n-alkanes and n-alkenes by anaerobic bacteria: a summary. Org Geochem 39: 1197–1203.Google Scholar
  58. Hallam SJ, Girguis PR, Preston CM, Richardson PM, DeLong EF (2003) Identification of methyl coenzyme M reductase A (mcrA) genes associated with methane-oxidizing archaea. Appl Environ Microbiol 69: 5483–5491.PubMedGoogle Scholar
  59. Hallam SJ, Putnam N, Preston CM, Detter JC, Rokhsar D, Richardson PM, DeLong EF (2004) Reverse methanogenesis: testing the hypothesis with environmental genomics. Science 305: 1457–1462.PubMedGoogle Scholar
  60. Harder J (1997) Anaerobic methane oxidation by bacteria employing 14C-methane uncontaminated with 14C-carbon monoxide. Marine Geol 137: 13–23.Google Scholar
  61. Harms G, Rabus R, Widdel F (1999a) Anaerobic oxidation of the aromatic plant hydrocarbon p-cymene by newly isolated denitrifying bacteria. Arch Microbiol 172: 303–312.PubMedGoogle Scholar
  62. Harms G, Zengler K, Aeckersberg F., Minz D, Rabus R, Widdel F (1999b) Anaerobic oxidation of o-xylene, m-xylene, and homologous alkylbenzenes by new types of sulfate-reducing bacteria. Appl Environ Microbiol 65: 999–1004.PubMedGoogle Scholar
  63. Hess A, Zarda B, Hahn D, Häner A, Stax D, Höhener P, Zeyer J (1997) In situ analysis of denitrifying toluene- and m-xylene-degrading bacteria in a diesel fuel-contaminated laboratory aquifer column. Appl Environ Microbiol 63: 2136–2141.PubMedGoogle Scholar
  64. Higashioka Y, Kojima H, Nakagawa T, Sato S, Fukui M (2009) A novel n-alkane-degrading bacterium as a minor member of p-xylene-degrading sulfate-reducing consortium. Biodegradation 20: 383–390.Google Scholar
  65. Hinrichs KU, Boetius AB (2002) Anaerobic oxidation of methane: new insights in microbial ecology and biochemistry. In Ocean Margin Systems. G Wefer, D Hebbeln, BB Jørgensen, M Schlüter, T van Weering (eds.). Heidelberg: Springer, pp. 457–477.Google Scholar
  66. Hinrichs KU, Hayes JM, Sylva SP, Brewer PG, DeLong EF (1999) Methane-consuming archaebacteria in marine sediments. Nature 398: 802–805.PubMedGoogle Scholar
  67. Hylemon PB, Harder J (1998) Biotransformation of monoterpenes, bile acids, and other isoprenoids in anaerobic ecosystems. FEMS Microbiol Rev 22: 475–488.PubMedGoogle Scholar
  68. Iversen N, Jørgensen BB (1985) Anaerobic methane oxidation rates at the sulfate methane transition in marine-sediments from Kattegat and Skagerrak (Denmark). Limnol Oceanogr 30: 944–955.Google Scholar
  69. Johnson HA, Pelletier DA, Spormann AM (2001) Isolation and characterization of anaerobic ethylbenzene dehydrogenase, a novel Mo-Fe-S enzyme. J Bacteriol 183: 4536–4542.PubMedGoogle Scholar
  70. Jones DM, Head IM, Gray ND, Adams JJ, Rowan AK, Aitken CM, Bennett B, Huang H, Brown A, Bowler BF, Oldenburg T, Erdmann M, Larter SR (2008) Crude-oil biodegradation via methanogenesis in subsurface petroleum reservoirs. Nature 451: 176–180.PubMedGoogle Scholar
  71. Jones WD (2000) Conquering the carbon-hydrogen bond. Science 287: 1942–1943.Google Scholar
  72. Kämpfer P, Denger K, Cook AM, Lee ST, Jäckel U, Denner EB, Busse HJ (2006) Castellaniella gen. nov., to accommodate the phylogenetic lineage of Alcaligenes defragrans, and proposal of Castellaniella defragrans gen. nov., comb. nov. and Castellaniella denitrificans sp. nov. Int J Syst Evol Microbiol 56: 815–819.PubMedGoogle Scholar
  73. Kasai Y, Takahata Y, Manefield M, Watanabe K (2006) RNA-based stable isotope probing and isolation of anaerobic benzene-degrading bacteria from gasoline-contaminated groundwater. Appl Environ Microbiol 72: 3586–3592.PubMedGoogle Scholar
  74. Kleinsteuber S, Schleinitz KM, Breitfeld J, Harms H, Richnow HH, Voigt C (2008) Molecular characterization of bacterial communities mineralizing benzene under sulfate-reducing conditions. FEMS Microbiol Ecol 66: 143–157.PubMedGoogle Scholar
  75. Kloer DP, Hagel C, Heider J, Schulz GE (2006) Crystal structure of ethylbenzene dehydrogenase from Aromatoleum aromaticum. Structure 14: 1377–1388.PubMedGoogle Scholar
  76. Kniemeyer O, Heider J (2001) Ethylbenzene dehydrogenase, a novel hydrocarbon-oxidizing molybdenum/iron-sulfur/heme enzyme. J Biol Chem 276: 21381–21386.PubMedGoogle Scholar
  77. Kniemeyer O, Fischer T, Wilkes H, Glöckner F-O, Widdel F (2003) Anaerobic degradation of ethylbenzene by a new type of marine sulfate-reducing bacterium. Appl Environ Microbiol 69: 760–768.PubMedGoogle Scholar
  78. Kniemeyer O, Musat F, Sievert S, Knittel K., Wilkes H, Blumenberg M, Michaelis W, Classen A, Bolm C, Joye S, Widdel F (2007) Anaerobic oxidation of short-chain hydrocarbons by marine sulphate-reducing bacteria. Nature 449: 898–902.PubMedGoogle Scholar
  79. Knöller K, Vogt C, Richnow HH, Weise SM (2006) Sulfur and oxygen isotope fractionation during benzene, toluene, ethyl benzene, and xylene degradation by sulfate-reducing bacteria. Environ Sci Technol 40: 3879–3885.PubMedGoogle Scholar
  80. Krüger M, Meyerdierks A, Glöckner FO, Amann R, Widdel F, Kube M, Reinhardt R, Kahnt J, Böcher R, Thauer RK, Shima S (2003) A conspicuous nickel protein in microbial mats that oxidize methane anaerobically. Nature 426: 878–881.PubMedGoogle Scholar
  81. Kuhn EP, Colberg PJ, Schnoor JL, Wanner O, Zehnder AJB, Schwarzenbach RP (1985) Microbial transformation of substituted benzenes during infiltration of river water to groundwater: laboratory column studies. Environ Sci Technol 19: 961–968.Google Scholar
  82. Kunapuli U, Lueders T, Meckenstock RU (2007) The use of stable isotope probing to identify key iron-reducing microorganisms involved in anaerobic benzene degradation. ISME J 1: 643–653.PubMedGoogle Scholar
  83. Lovley DR, Baedecker MJ, Lonergan DJ, Cozzarelli IM, Phillips EJP, Siegel OI (1989) Oxidation of aromatic contaminants coupled to microbial iron reduction. Nature 339: 297–300.Google Scholar
  84. Lovley DR, Giovannoni SJ, White DC, Champine JE, Phillips EJ, Gorby YA, Goodwin S (1993) 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.PubMedGoogle Scholar
  85. Martens CS, Berner RA (1974) Methane production in the interstitial waters of sulfate-depleted marine sediment. Science 185: 1167–1169.PubMedGoogle Scholar
  86. Mayr S, Latkoczy C, Krüger M, Günther D, Shima S, Thauer RK, Widdel F, Jaun B (2008) Structure of an F430 variant from archaea associated with anaerobic oxidation of methane. J Am Chem Soc 130: 10758–10767.PubMedGoogle Scholar
  87. Meckenstock RU (1999) Fermentative toluene degradation in anaerobic defined syntrophic cocultures. FEMS Microbiol Lett 177: 67–73.PubMedGoogle Scholar
  88. Meckenstock RU, Krieger R, Ensign S, Kroneck PM, Schink B (1999) Acetylene hydratase of Pelobacter acetylenicus. Molecular and spectroscopic properties of the tungsten iron-sulfur enzyme. Eur J Biochem 264: 176–182.PubMedGoogle Scholar
  89. Meckenstock RU, Annweiler E, Michaelis W, Richnow HH, Schink B (2000) Anaerobic naphthalene degradation by a sulfate-reducing enrichment culture. Appl Environ Microbiol 66: 2743–2747.PubMedGoogle Scholar
  90. Meyerdierks A, Kube M, Lombardot T, Knittel K, Bauer M, Glöckner FO, Reinhardt R, Amann R (2005) Insights into the genomes of archaea mediating the anaerobic oxidation of methane. Environ Microbiol 7: 1937–1951.PubMedGoogle Scholar
  91. Michaelis W, Seifert R, Nauhaus K, Treude T, Thiel V, Blumenberg M, Knittel K, Gieseke A, Peterknecht K, Pape T, Boetius A, Amann R, Jørgensen BB, Widdel F, Peckmann J, Pimenov NV, Gulin MB (2002) Microbial reefs in the Black Sea fueled by anaerobic oxidation of methane. Science 297: 1013–1015.PubMedGoogle Scholar
  92. Moran JJ, Beal EJ, Vrentas JM, Orphan VJ, Freeman KH, House CH (2008) Methyl sulfides as intermediates in the anaerobic oxidation of methane. Environ Microbiol 10: 162–173.PubMedGoogle Scholar
  93. Morasch B, Meckenstock RU (2005) Anaerobic degradation of p-xylene by a sulfate-reducing enrichment culture. Curr Microbiol 51: 127–130.PubMedGoogle Scholar
  94. Morasch B, Schink B, Tebbe CC, Meckenstock RU (2004) Degradation of o-xylene and m-xylene by a novel sulfate-reducer belonging to the genus Desulfotomaculum. Arch Microbiol 181: 407–417.PubMedGoogle Scholar
  95. Musat F, Widdel F (2008) Anaerobic degradation of benzene by a marine sulfate-reducing enrichment culture, and cell hybridization of the dominant phylotype. Environ Microbiol 10: 10–19.PubMedGoogle Scholar
  96. Musat F, Galushko A, Jacob J, Widdel F, Kube M, Reinhardt R, Wilkes H, Schink B, Rabus R (2009) Anaerobic degradation of naphthalene and 2-methylnaphthalene by strains of marine sulfate-reducing bacteria. Environ Microbiol 11: 209–219.PubMedGoogle Scholar
  97. Nakagawa T, Sato S, Fukui M (2008) Anaerobic degradation of p-xylene in sediment-free sulfate-reducing enrichment culture. Biodegradation 19: 909–913.PubMedGoogle Scholar
  98. Nauhaus K, Boetius A, Krüger M, Widdel F (2002) In vitro demonstration of anaerobic oxidation of methane coupled to sulphate reduction in sediment from a marine gas hydrate area. Environ Microbiol 4: 296–305.PubMedGoogle Scholar
  99. Nauhaus K, Treude T, Boetius A, Krüger M (2005) Environmental regulation of the anaerobic oxidation of methane: a comparison of ANME-I and ANME-II communities. Environ Microbiol 7: 98–106.PubMedGoogle Scholar
  100. Nauhaus K, Albrecht M, Elvert M, Boetius A, Widdel F (2007) In vitro cell growth of marine archaeal-bacterial consortia during anaerobic oxidation of methane with sulphate. Einviron Microbiol 9: 187–196.Google Scholar
  101. Novelli GD, ZoBell EC (1944) Assimilation of petroleum hydrocarbons by sulfate-reducing bacteria. J Bacteriol 47: 447–448.Google Scholar
  102. Ommedal H, Torsvik T (2007) Desulfotignum toluenicum sp. nov., a novel toluene-degrading, sulphate-reducing bacterium isolated from an oil-reservoir model column. Int J Syst Evol Microbiol 57: 2865–2869.PubMedGoogle Scholar
  103. Oremland RS, Voytek MA (2008) Acetylene as fast food: implications for development of life on anoxic primordial Earth and in the outer solar system. Astrobiol 8: 45–58.Google Scholar
  104. Overmann J, Sandmann G, Hall KJ, Northcote TG (1993) Fossil carotenoids and paleolimnology of meromictic Mahoney Lake, British Columbia, Canada. Aquat Sci 55: 31–39.Google Scholar
  105. Oka AR, Phelps CD, McGuinness LM, Mumford A, Young LY, Kerkhof LJ (2008) Identification of critical members in a sulfidogenic benzene-degrading consortium by DNA stable isotope probing. Appl Environ Microbiol 74: 6476–6480.PubMedGoogle Scholar
  106. Pancost RD, Sinninghe Damste JS, de Lint S, van der Maarel MJEC, Gottschal JC (2000) Biomarker evidence for widespread anaerobic methane oxidation in Mediterranean sediments by a consortium of methanogenic Archaea and Bacteria. Appl Environ Microbiol 66: 1126–1132.PubMedGoogle Scholar
  107. Paull CK, Chanton J, Neumann AC, Coston JA, Martens CS, Showers W (1992) Indicators of methane-derived carbonates and chemosynthetic organic carbon deposits: examples from the Florida Escarpment. Palaios 7: 361–375.Google Scholar
  108. Phelps CD, Kerkhof LJ, Young LY (1998) Molecular characterization of a sulfate-reducing consortium which mineralizes benzene. FEMS Microbiol Ecol 27: 269–279.Google Scholar
  109. Phelps CD, Zhang X, Young LY (2001) Use of stable isotopes to identify benzoate as a metabolite of benzene degradation in a sulphidogenic consortium. Environ Microbiol 3: 600–603.PubMedGoogle Scholar
  110. Rabus R, Nordhaus R, Ludwig W, Widdel F (1993) Complete oxidation of toluene under strictly anoxic conditions by a new sulfate-reducing bacterium. Appl Environ Microbiol 59: 1444–1451.PubMedGoogle Scholar
  111. Rabus R, Widdel F (1995) Anaerobic degradation of ethylbenzene and other aromatic hydrocarbons by new denitrifying bacteria. Arch Microbiol 163: 96–103.PubMedGoogle Scholar
  112. Rabus R, Widdel F (1996) Utilization of alkylbenzenes during anaerobic growth of pure cultures of denitrifying bacteria on crude oil. Appl Environ Microbiol 62: 1238–1241.PubMedGoogle Scholar
  113. Rabus R, Fukui M, Wilkes H, Widdel F (1996) Degradative capacities and 16S rRNA-targeted whole-cell hybridization of sulfate-reducing bacteria in an anaerobic enrichment culture utilizing alkylbenzenes from crude oil. Appl Environ Microbiol 62: 3605–3613.PubMedGoogle Scholar
  114. Rabus R, Wilkes H, Schramm A, Harms G, Behrends A, Amann R, Widdel F (1999) Anaerobic utilization of alkylbenzenes and n-alkanes from crude oil in an enrichment culture of denitrifying bacteria affiliating with the β-subclass of Proteobacteria. Environ Microbiol 1: 145–157.PubMedGoogle Scholar
  115. Rabus R, Kube M, Heider J, Beck A, Heitmann K, Widdel F, Reinhardt R (2005) The genome sequence of an anaerobic aromatic-degrading denitrifying bacterium, strain EbN1. Arch Microbiol 183: 27–36.PubMedGoogle Scholar
  116. Raghoebarsing AA, Pol A, van de Pas-Schoonen KT, Smolders AJP, Ettwig KE, Rijpstra WIC, Schouten S, Sinninghe Damsté JS, Op den Camp HJM, Jetten M, Strous M (2006) A microbial consortium couples anaerobic methane oxidation to denitrification. Nature 440: 918–921.PubMedGoogle Scholar
  117. Rahn O (1906) Ein Paraffin zersetzender Schimmelpilz. Zentralbl Bakteriol Parasitenk Infekt, II. Abt, 16: 382–384.Google Scholar
  118. Reeburgh WS (1976) Methane consumption in Cariaco Trench waters and sediments. Earth Planet Sci Lett 28: 337–344.Google Scholar
  119. Reeburgh WS (1980) Anaerobic methane oxidation: rate depth distributions in Skan Bay sediments. Earth Planet Sci Lett 47: 345–352.Google Scholar
  120. Richnow HH, Annweiler E, Michaelis W, Meckenstock RU (2003) Microbial in situ degradation of aromatic hydrocarbons in a contaminated aquifer monitored by carbon isotope fractionation. J Contam Hydrol 65: 101–120.PubMedGoogle Scholar
  121. Rios-Hernandez LA, Gieg LM, Suflita JM (2003) Biodegradation of an alycyclic hydrocarbon by a sulfate-reducing enrichment from a gas condensate-contaminated aquifer. Appl Environ Microbiol 69: 434–443.PubMedGoogle Scholar
  122. Ritger S, Carson B, Suess E (1987) Methane-derived authigenic carbonates formed by subduction-induced pore-water expulsion along the Oregon/Washington margin. Geol Soc Am Bull 98: 147–156.Google Scholar
  123. Rockne KJ, Chee-Sanford JC, Sanford RA, Hedlund BP, Staley JT, Strand SE (2000) Anaerobic naphthalene degradation by microbial pure cultures under nitrate-reducing conditions. Appl Environ Microbiol 66: 1595–1601.PubMedGoogle Scholar
  124. Rontani JF, Mouzdahir A, Michotey V, Bonin P (2002) Aerobic and anaerobic metabolism of squalene by a denitrifying bacterium isolated from marine sediment. Arch Microbiol 178: 279–287.PubMedGoogle Scholar
  125. Rosenfeld WD (1947) Anaerobic oxidation of hydrocarbons by sulfate-reducing bacteria. J Bacteriol 54: 664–665.Google Scholar
  126. Rosner B, Schink B (1995) Purification and characterization of acetylene hydratase of Pelobacter acetylenicus, a tungsten iron-sulfur protein. J Bacteriol 177: 5767–5772.PubMedGoogle Scholar
  127. Rosner BM, Rainey FA, Kroppenstedt RM, Schink B (1997) Acetylene degradation by new isolates of aerobic bacteria and comparison of acetylene hydratase enzymes. FEMS Microbiol Lett 148: 175–180.PubMedGoogle Scholar
  128. Ruckmick JC, Wimberly BH, Edwards AF (1979) Classification and genesis of biogenic sulfur deposits. Econ Geol 74: 469–474.Google Scholar
  129. Rueter P, Rabus R, Wilkes H, Aeckersberg F, Rainey FA, Jannasch HW, Widdel F (1994) Anaerobic oxidation of hydrocarbons in crude oil by new types of sulphate-reducing bacteria. Nature 372: 455–458.PubMedGoogle Scholar
  130. Savithiry N, Cheong TK, Oriel P (1997) Production of α-terpineol from Escherichia coli cells expressing thermostable limonene hydratase. Appl Biochem Biotechnol 63–65: 213–220.PubMedGoogle Scholar
  131. Schink B (1985a) Degradation of unsaturated hydrocarbons by methanogenic enrichment cultures. FEMS Microbiol Lett 31: 69–77.Google Scholar
  132. Schink B (1985b) Fermentation of acetylene by an obligate anaerobe, Pelobacter acetylenicus. Arch Microbiol 142: 295–301.Google Scholar
  133. Seiffert GB, Ullmann GM, Messerschmidt A, Schink B, Kroneck PM, Einsle O (2007) Structure of the non-redox-active tungsten/[4Fe:4S] enzyme acetylene hydratase. Proc Nat Acad Sci USA 104: 3073–3077.PubMedGoogle Scholar
  134. Shilov AE, and Shul’pin B (1997) Activation of C–H bonds by metal complexes. Chem Rev 97: 2879–2932.PubMedGoogle Scholar
  135. Shinoda Y, Sakai Y, Uenishi H, Uchihashi Y, Hiraishi A, Yukawa Hm Yurimoto H, Kato N (2004) Aerobic and anaerobic toluene degradation by a newly isolated denitrifying bactgerium, Thauera sp. strain DNT-1. Appl Environ Microbiol 70: 1384–1392.Google Scholar
  136. Shinoda Y, Akagi J, Uchihashi Y, Hiraishi A, Yukawa H, Yurimoto H, Sakai Y, Kato N (2005) Anaerobic degradation of aromatic compounds by Magnetospirillum strains: isolation and degradation genes. Biosci Biotechnol Biochem 69: 1483–1491.PubMedGoogle Scholar
  137. So CM, Young LY (1999) Isolation and characterization of a sulfate-reducing bacterium that anaerobically degrades alkanes. Appl Environ Microbiol 65: 2969–2976.PubMedGoogle Scholar
  138. Söhngen NL (1905) Methane as carbon-food and source of energy for bacteria. Proc Kon Akad Wetensch Amsterdam 8: 327.Google Scholar
  139. Söhngen NL (1913) Oxidation of petroleum, paraffin, paraffin-oil and benzene by microbes. Proc Kon Akad Wetensch Amsterdam 15: 1145.Google Scholar
  140. Song B, Häggblom MM, Zhou J, Tiedje JM, Palleroni NJ (1999) Taxonomic characterization of denitrifying bacteria that degrade aromatic compounds and description of Azoarcus toluvorans sp. nov. and Azoarcus toluclasticus sp. nov. Int J Syst Bacteriol. 49: 1129–1140.PubMedGoogle Scholar
  141. Spormann AM, Widdel F (2000) Metabolism of alkylbenzenes, alkanes, and other hydrocarbons in anaerobic bacteria. Biodegradation 11: 85–105.PubMedGoogle Scholar
  142. Szaleniec M, Hagel C, Menke M, Nowak P, Witko M, Heider J (2007) Kinetics and mechanism of oxygen-independent hydrocarbon hydroxylation by ethylbenzene dehydrogenase. Biochemistry 46: 7637–7646.PubMedGoogle Scholar
  143. Tausson WO, Aleshina WA (1932) Über die bakterielle Sulfatreduktion bei Anwesenheit der Kohlenwasserstoffe (in Russian with German summary). Mikrobiologiya 1: 229–261.Google Scholar
  144. Thauer RK (1998) Biochemistry of methanogenesis: a tribute to Marjory Stephenson. Microbiology (UK) 144: 2377–2406.Google Scholar
  145. Tissot BP, Welte DH (1984) Petroleum formation and occurrence. Berlin: Springer.Google Scholar
  146. Townsend GT, Prince RC, Suflita JM (2003) Anaerobic oxidation of crude oil hydrocarbons by the resident microorganism of a contaminated anoxic aquifer. Environ Sci Technol 37: 5213–5218.PubMedGoogle Scholar
  147. Ulrich AC, Edwards EA (2003) Physiological and molecular characterization of anaerobic benzene-degrading mixed cultures. Environ Microbiol 5: 92–102.PubMedGoogle Scholar
  148. Wegener G, Niemann H, Elvert M, Hinrichs KU, Boetius A (2008) Assimilation of methane and inorganic carbon by microbial communities mediating the anaerobic oxidation of methane. Environ Microbiol 10: 2287–2298.PubMedGoogle Scholar
  149. Widdel F (1988) Microbiology and ecology of sulfate- and sulfur-reducing bacteria. In Biology of Anaerobic Microorganisms. AJB Zehnder (ed.). New York: Wiley, pp. 469–585.Google Scholar
  150. Widdel F, Rabus R (2001) Anaerobic biodegradation of saturated and aromatic hydrocarbons. Curr Opin Biotechnol 12: 259–276.PubMedGoogle Scholar
  151. Winderl C, Schaefer S, Lueders T (2007) Detection of anaerobic toluene and hydrocarbon degraders in contaminated aquifers using benzylsuccinate synthase (bssA) genes as a functional marker. Environ Microbiol 9: 1035–1046.PubMedGoogle Scholar
  152. Wöhlbrand L, Kallerhoff B, Lange D, Hufnagel P, Thiermann J, Reinhardt R, Rabus R (2007) Functional proteomic view of metabolic regulation in “Aromatoleum aromaticum” strain EbN1. Proteomics 7: 2222–2239.PubMedGoogle Scholar
  153. Zehnder AJ, Brock TD (1979) Methane formation and methane oxidation by methanogenic bacteria. J Bacteriol 137: 420–432.PubMedGoogle Scholar
  154. Zengler K, Richnow HH, Rosselló-Mora R, Michaelis W, Widdel F (1999a) Methane formation from long-chain alkanes by anaerobic microorganisms. Nature 401: 266–269.PubMedGoogle Scholar
  155. Zengler K, Heider J, Roselló-Mora R, Widdel F (1999b) Phototrophic utilization of toluene under anoxic conditions by a new strain of Blastochloris sulfoviridis. Arch Microbiol 172: 204–212.PubMedGoogle Scholar
  156. Zhang X, Young LY (1997) Carboxylation as an initial reaction in the anaerobic metabolism of naphthalene and phenanthrene by sulfidogenic consortia. Appl Environ Microbiol 63: 4759–4764.PubMedGoogle Scholar
  157. Zhou J, Fries MR, Chee-Sanford JC, Tiedje JM (1995) Phylogenetic analyses of a new group of denitrifiers capable of anaerobic growth of toluene and description of Azoarcus tolulyticus sp. nov. Int J Syst Bacteriol 45: 500–506.PubMedGoogle Scholar
  158. ZoBell CE (1946) Action of microorganisms on hydrocarbons. Bacteriol Rev 10: 1–49.Google Scholar
  159. ZoBell CE (1959) Ecology of sulphate reducing bacteria. Prod Mon 22: 12–29.Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  • F. Widdel
    • 1
  • K. Knittel
    • 1
  • A. Galushko
    • 1
  1. 1.Max Planck Institute for Marine MicrobiologyBremenGermany

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