Advertisement

Applied Microbiology and Biotechnology

, Volume 67, Issue 5, pp 600–618 | Cite as

Biodegradation of xenobiotics by anaerobic bacteria

  • Chunlong Zhang
  • George N. Bennett
Mini-Review

Abstract

Xenobiotic biodegradation under anaerobic conditions such as in groundwater, sediment, landfill, sludge digesters and bioreactors has gained increasing attention over the last two decades. This review gives a broad overview of our current understanding of and recent advances in anaerobic biodegradation of five selected groups of xenobiotic compounds (petroleum hydrocarbons and fuel additives, nitroaromatic compounds and explosives, chlorinated aliphatic and aromatic compounds, pesticides, and surfactants). Significant advances have been made toward the isolation of bacterial cultures, elucidation of biochemical mechanisms, and laboratory and field scale applications for xenobiotic removal. For certain highly chlorinated hydrocarbons (e.g., tetrachlorethylene), anaerobic processes cannot be easily substituted with current aerobic processes. For petroleum hydrocarbons, although aerobic processes are generally used, anaerobic biodegradation is significant under certain circumstances (e.g., O2-depleted aquifers, oil spilled in marshes). For persistent compounds including polychlorinated biphenyls, dioxins, and DDT, anaerobic processes are slow for remedial application, but can be a significant long-term avenue for natural attenuation. In some cases, a sequential anaerobic-aerobic strategy is needed for total destruction of xenobiotic compounds. Several points for future research are also presented in this review.

Keywords

PCBs Atrazine Dioxin Linear Alkylbenzene Sulfonate BTEX 
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.

Notes

Acknowledgements

Research in authors’ laboratories has been supported by the Welch Foundation (C-1268) and BC-0022, DSWA, EIH and SERDP. This material is also based on work supported in part by the United States Army Research Laboratory and the United States Army Research Office (Grant DOD Army W911NF-04-1-0179)

References

  1. Abramowicz DA (1990) Aerobic and anaerobic biodegradation of PCBs: a review. Crit Rev Biotechnol 10:241–251Google Scholar
  2. Adrian NR, Chow T (2001) Identification of hydroxylamino-dinitroso-1,3,5-triazine as a transient intermediate formed during the anaerobic biodegradation of hexahydro-1,3,5-trinitro-1,3,5-triazine. Environ Toxicol Chem 20:1874–1877Google Scholar
  3. Aeckersberg F, Bak F, Widdel F (1991) Anaerobic oxidation of saturated hydrocarbons to CO2 by a new type of sulfate-reducing bacterium. Arch Microbiol 156:5–14Google Scholar
  4. Ahmad F, Hughes JB (2000) Anaerobic transformation of TNT by Clostridium. In: Spain JC, Hughes JB, Knackmuss H-J (eds) Biodegradation of nitroaromatic compounds and explosives, Lewis, Boca Raton, Fla., pp 185–212Google Scholar
  5. AISE and CESIO (1999) Environmental relevance of anaerobic biodegradability of surfactants. http://www.aise-net.org/PDF/anaerobicBiopub1.pdf, p 6
  6. Alexander M (1981) Biodegradation of chemicals of environmental concern. Science 211:132–138Google Scholar
  7. Annweiler E, Materna A, Safinowski S, Kappler A, Richnow HH, Michaelis W, Meckensrock RU (2000) Anaerobic degradation of 2-methylnaphthalene by a sulfate reducing enrichment culture. Appl Environ Microbiol 66:5329–5333Google Scholar
  8. 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 68:852–858Google Scholar
  9. Bagley DM, Gossett JM (1990) Tetrachloroethene transformation to trichloroethene and cis-1,2-dichloroethene by sulfate-reducing enrichment cultures. Appl Environ Microbiol 56:2511–2516Google Scholar
  10. Baker KH, Herson DS (1994) Bioremediation. McGraw Hill, New York, NYGoogle Scholar
  11. Ball HA, Johnson HA, Reinhard M, Spormann AM (1996) Initial reactions in anaerobic ethylbenzene oxidation by a denitrifying bacterium, strain EB1. J Bacteriol 178:5755–5761Google Scholar
  12. Barik S, Wahid PA, Ramakrishna C, Sethunathan N (1979) A change in the degradation pathway of parathion after repeated applications to flooded soil. J Agric Food Chem 27:1391–1392Google Scholar
  13. Barker JF, Patrick GC, Major DW (1987) Natural attenuation of aromatic hydrocarbons in a shallow sand aquifer. Ground Water Monit Rev 7:64–71Google Scholar
  14. Batterman G (1983) A large scale experiment on in situ biodegradation of hydrocarbon in the subsurface. In: Ground water in water resources planning, vol II. Proc Int Symp. IASA Publication 142. International Association of Hydrological Sciences, London, p 93Google Scholar
  15. Beaudet R, Levesque MJ, Villemur R, Lanthier M, Chenier M, Lepine F, Bisaillon JG (1998) Anaerobic biodegradation of pentachlorophenol in a contaminated soil inoculated with a methanogenic consortium or with Desulfitobacterium frappieri strain PCP-1. Appl Microbiol Biotechnol 50:135–141Google Scholar
  16. Bedard DL (2003) Polychlorinated biphenyls in aquatic sediments: environmental fate and outlook for biological treatment. In: Bossert ID, Haggblom MM (eds) Dehalogenation. Kluwer, Norwell, Mass., pp 443–465Google Scholar
  17. Beller HR, Spormann AM (1998) Analysis of the novel benzylsuccinate synthase reaction for anaerobic toluene activation based on structural studies of the product. J Bacteriol 180:5454–5457Google Scholar
  18. Bhushan B, Halasz A, Spain J, Thiboutot S, Ampleman G, Hawari J (2002) Biotransformation of hexahydro-1,3,5-trinitro-1,3,5-triazine catalyzed by a NAD(P)H: nitrate oxidoreductase from Aspergillus niger. Environ Sci Technol 36:3104–3108Google Scholar
  19. Biegert T, Fuchs G, 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 238:661–668Google Scholar
  20. Boll M, Fuchs G, Heider J (2002) Anaerobic oxidation of aromatic compounds and hydrocarbons. Curr Opin Chem Biol 6:604–611CrossRefPubMedGoogle Scholar
  21. Boopathy R, Gurgas M, Ullian J, Manning JF (1998) Metabolism of explosive compounds by sulfate-reducing bacteria. Curr Microbiol 37:127–131Google Scholar
  22. Boopathy R, Kulpa CF (1992) Trinitrotoluene as a sole nitrogen source for a sulfate-reducing bacterium Desulfovibrio sp. (B strain) isolated from an anaerobic digester. Curr Microbiol 25:235–241Google Scholar
  23. Bossert ID, Young LY (1986) Anaerobic oxidation of p-cresol by a denitrifying bacterium. Appl Environ Microbiol 52:1117–1122Google Scholar
  24. Bossert ID, Whited G, Gibson DT, Young LY (1989) Anaerobic oxidation of p-cresol mediated by a partially purified methylhydroxylase denitrifying bacterium. J Bacteriol 171:2956–2962Google Scholar
  25. Bouchard B, Beaudet R, Villemur R, McSween G, Lepine F, Bisaillon JG (1996) Isolation and characterization of Desulfitobacterium frappieri sp. nov., an anaerobic bacterium which reductively dechlorinates pentachlorophenol to 3-chlorophenol. Int J Syst Bacteriol 46:1010–1015Google Scholar
  26. Bryant FO, Hale DD, Rogers JE (1991) Regiospecific dechlorination of pentachlorophenol by dichlorophenol-adapted microorganisms in freshwater, anaerobic sediment slurries. Appl Environ Microbiol 57:2293–2301Google Scholar
  27. Bunge M, Adrian L, Kraus A, Lorenz WG, Andreesen JR, Gorisch H, Lechner U (2003) Reductive dehalogenation of chlorinated dioxins by the anaerobic bacterium Dehalococcoides ethenogenes sp. strain CBDB1. Nature 421:357–360CrossRefPubMedGoogle Scholar
  28. Cerniglia CE (1992) Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3:351–368Google Scholar
  29. Chacko CI, Lockwood JL, Zabik M (1966) Chlorinated hydrocarbon pesticides: degradation by microbes. Science 154:893–895Google Scholar
  30. Chakraborty R, Coates JD (2004) Anaerobic degradation of monoaromatic hydrocarbons. Appl Microbiol Biotechnol 64:437–446Google Scholar
  31. Chen G (2004) Reductive dehalogenation of tetrachloroethylene by microorganisms: current knowledge and application strategies. Appl Microbiol Biotechnol 63:373–377Google Scholar
  32. Chen ST, Berthouex PM (2001) Treating an aged pentachlorophenol- (PCP-) contaminated soil through three sludge handling processes, anaerobic sludge digestion, post-sludge digestion and sludge land application. Water Sci Technol 44:149–56Google Scholar
  33. 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 411:1039–1043Google Scholar
  34. Coleman NV, Mattes TE, Gossett JM, Spain JC (2002a) Biodegradation of cis-dichloroethene as the sole carbon source by a beta-proteobacterium. Appl Environ Microbiol 68:2726–2730Google Scholar
  35. Coleman NV, Mattes TE, Gossett JM, Spain JC (2002b) Phylogenetic and kinetic diversity of aerobic vinyl chloride-assimilating bacteria from contaminated sites. Appl Environ Microbiol 68:6162–6171Google Scholar
  36. Cookson JT Jr (1995) Bioremediation engineering: design and application. McGraw-Hill, New York, NYGoogle Scholar
  37. Crawford JJ, Sims GK, Mulvaney RL, Radosevich M (1998) Biodegradation of atrazine under denitrifying conditions. Appl Microbiol Biotechnol 49:618–623Google Scholar
  38. Cupples AM, Spormann AM, McCarty PL (2004) Comparative evaluation of chloroethene dechlorination to ethene by Dehalococcoides-like microorganisms. Environ Sci Technol 38:4768–4774Google Scholar
  39. Daun G, Lenke H, Reuss M, Knackmuss H-J (1998) Biological treatment of TNT-contaminated soil. 1. Anaerobic cometabolic reduction and interaction of TNT and metabolites with soil components. Environ Sci Technol 32:1956–1963Google Scholar
  40. De Bruin WP, Koterman MJJ, Posthumus MA, Schraa G, Zehnder AJB (1992) Complete biological reductive transformation of tetrachloroethene to ethane. Appl Environ Microbiol 58:1996–2000Google Scholar
  41. Denger K, Cook AM (1999) Linear alkylbenzenesulphonate (LAS) bioavailable to anaerobic bacteria as a source of sulphur. J Appl Microbiol 86:165–168Google Scholar
  42. Deweerd KA, Bedard DL (1999) Use of halogenated benzoates and other halogenated aromatic compounds to stimulate the microbial dechlorination of PCBs. Environ Sci Technol 33:2057–2063Google Scholar
  43. DiStefano TD, Gossett JM, Zinder SH (1992) Hydrogen as an electron donor for dechlorination of tetrachloroethene by an anaerobic mixed culture. Appl Environ Microbiol 58:3622–3629Google Scholar
  44. Dolfing J, Beurskens JEM (1995) The microbial logic and environmental significance of reductive dehalogenation. Adv Microbial Ecol 14:143–206Google Scholar
  45. Dybas MJ, Barcelona M, Bezborodnikov S, Davies S, Forney L, Heuer H, Kawka O, Mayotte T, Sepulveda-Torres L, Smalla K, Sneathen M, Tiedje J, Voice T, Wiggert DC, Witt ME, Criddle CS (1998) Pilot-scale evaluation of bioaugmentation for in-situ remediation of a carbon tetrachloride-contaminated aquifer. Environ Sci Technol 32:3598–3611Google Scholar
  46. Ehrenreich P, Behrends A, Harder J, Widdel F (2000) Anaerobic oxidation of alkanes by newly isolated denitrifying bacteria. Arch Microbiol 173:58–64Google Scholar
  47. El Fantroussi S, Naveau H, Agathos SN (1998) Anaerobic dechlorinating bacteria. Biotechnol Prog 14:167–188CrossRefPubMedGoogle Scholar
  48. ElFantroussi S, Belkacemi M, Top EM, Mahillon J, Vaveau H, Agathos SN (1999) Bioaugmentation of a soil bioreactor designed for pilot-scale anaerobic bioremediation studies. Environ Sci Technol 33:2992–3001Google Scholar
  49. Ellis DE, Lutz EJ, Odom JM, Buchanan RJ Jr, Bartlett CL, Lee MD, Harkness MR, Deweerd KA (2000) Bioaugmentation for accelerated in situ anaerobic bioremediation. Environ Sci Technol 34:2254–2260Google Scholar
  50. Eriksson M, Sodersten E, Yu Z, Dalhammar G, Mohn WW (2003) Degradation of polycyclic aromatic hydrocarbons at low temperature under aerobic and nitrate-reducing conditions in enrichment cultures from northern soils. Appl Environ Microbiol 69:275–84Google Scholar
  51. Ernst C, Rehm HJ (1995) Utilization of chlorinated s-triazines by a new strain of Klebsiella pneumoniae. Appl Microbiol Biotechnol 42:763–768CrossRefPubMedGoogle Scholar
  52. Esteve-Nuñez A, Ramos JL (1998) Metabolism of 2,4,6-trinitrotoluene (TNT) by Pseudomonas sp. JLR11. Environ Sci Technol 32:3802–3808Google Scholar
  53. Esteve-Nuñez A, Luchessi, Phillipps B, Schink B, Ramos JL (2000) Respiration of 2,4,6-trinitrotoluene by Pseudomonas sp. strain JLR11. J Bacteriol 182:1352–1355Google Scholar
  54. Esteve-Nuñez A, Caballero A, Ramos JL (2001) Biological degradation of 2,4,6-trinitrotoluene. Microbiol Mol Biol Rev 65:335–352CrossRefPubMedGoogle Scholar
  55. Fathepure BZ, Boyd SA (1988) Dependence of tetrachloroethylene dechlorination on methanogenic substrate consumption by Methanosarcina sp. strain DCM. Appl Environ Microbiol 54:2976–2980Google Scholar
  56. Fayolle F, Vandecasteele J-P, Monot F (2001) Microbial degradation and fate in the environment of methyl tert-butyl ether and related fuel oxygenates. Appl Microbiol Biotechnol 56:339–349Google Scholar
  57. Federle TW, Pastwa GM (1988) Biodegradation of surfactants in saturated subsurface sediments: a field study. Ground Water 26:761–770Google Scholar
  58. Fennell DE, Nijenhuis I, Wilson SF, Zinder SH, Haggblom MM (2004) Dehalococcoides ethenogenes strain 195 reductively dechlorinates diverse chlorinated aromatic pollutants. Environ Sci Technol 38:2075–2081Google Scholar
  59. Ferguson PL, Brownawell BJ (2003) Degradation of nonylphenol ethoxylates in estuarine sediment under aerobic and anaerobic conditions. Environ Toxicol Chem 22:1189–1199Google Scholar
  60. Fetzner S (1998) Bacterial dehalogenation. Appl Microbiol Biotechnol 50:633–657CrossRefPubMedGoogle Scholar
  61. Finneran KT, Lovley DR (2001) Anaerobic degradation of methyl tert-butyl ether (MTBE) and tert-butyl alcohol (TBA). Environ Sci Technol 35:1785–1790CrossRefPubMedGoogle Scholar
  62. Funk SB, Crawford DL, Crawford RL, Mead G, Davis-Hooker W (1995) Full-scale anaerobic bioremediation of trinitrotoluene contaminated soils. Appl Biochem Biotechnol 51:625–633Google Scholar
  63. 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 1:415–420Google Scholar
  64. Gaus C, Brunskill GJ, Connell DW, Prange J, Muller JF, Papke O, Webber R (2002) Transformation processes, pathways, and possible sources of distinctive polychlorinated dibenzo-p-dioxin signatures in sink environments. Environ Sci Technol 36:3452–3549Google Scholar
  65. Gerritse J, Renard V, Gomes TMP, Lawson PA, Collins MD, Gottschal J (1996) Desulfitobacterium sp. strain, an anaerobic bacterium that can grow by reductive dechlorination of tetrachloroethene or ortho-chlorinated phenols. Arch Microbiol 165:132–140Google Scholar
  66. Gerritse J, Drzyzga O, Kloetstra G, Keijmel M, Wiersum LP, Hutson R, Collins MD, Gottschal JC (1999) Influence of different electron donors and acceptors on dehalorespiration of tetrachloroethene by Desulfitobacterium frappieri TCE1. Appl Environ Microbiol 65:5212–5221Google Scholar
  67. Ghosh PK, Philip L (2004) Atrazine degradation in anaerobic environment by a mixed microbial consortium. Water Res 38:2276–2283Google Scholar
  68. Gieg LM, Suflita JM (2002) Detection of anaerobic metabolites of saturated and aromatic hydrocarbons in petroleum-contaminated aquifers. Environ Sci Technol 36:3755–3762Google Scholar
  69. Gorontzy T, Drzyzga O, Kahl MW, Bruns-Nagel D, Breitung J, von Loew E, Blotevogel KH (1994) Microbial degradation of explosives and related compounds. Crit Rev Microbiol 20:265–284Google Scholar
  70. Guenzi WD, Beard WE (1967) Anaerobic biodegradation of DDT to DDD in soil. Science 156:1116–1117Google Scholar
  71. Haggblom MM, Young LY (1990) Chlorophenol degradation coupled to sulfate reduction. Appl Environ Microbiol 56:3255–3260Google Scholar
  72. Haggblom MM, Young LY (1995) Anaerobic degradation of halogenated phenols by sulfate-reducing consortia. Appl Environ Microbiol 61:1546–1550Google Scholar
  73. Haggblom MM, Knight VK, Kerkhof LJ (2000) Anaerobic decomposition of halogenated aromatic compounds. Environ Pollut 107:199–207Google Scholar
  74. Haggblom MM, Ahn YB, Fennell DE, Kerkhof LJ, Rhee SK (2003) Anaerobic dehalogenation of organohalide contaminants in the marine environment. Adv Appl Microbiol 53:61–84Google Scholar
  75. Haggensen F, Mogensen AS, Angelidaki I, Ahring BK (2002) Anaerobic treatment of sludge: focusing on reduction of LAS concentration in sludge. Water Sci Technol 46:159–165Google Scholar
  76. Hammill TB, Crawford RL (1996) Degradation of 2-sec-butyl-4,6-dinitrophenol (Dinoseb) by Clostridium bifermentans KMR-1. Appl Environ Microbiol 62:1842–1846Google Scholar
  77. Harms G, Zengler K, Rabus R, Aeckersberg F, Minz D, Rosselló-Mora R, Widdel F (1999) Anaerobic oxidation of o-xylene, m-xylene, and homologous alkylbenzenes by new types of sulfate-reducing bacteria. Appl Environ Microbiol 65:999–1004Google Scholar
  78. Hawari J, Beaudet S, Halasz A, Thiboutots S, Ampleman G (2000) Microbial degradation of explosives: biotransformation versus mineralization. Appl Microbiol Biotechnol 54:605–618Google Scholar
  79. He J, Ritalahti KM, Yang K-L, Koenigsberg SS, Löffler FE (2003) Detoxification of vinyl chloride to ethene coupled to an anaerobic bacterium. Nature 424:62–65Google Scholar
  80. Heider J, Fuchs G (1997) Anaerobic metabolism of aromatic compounds. Eur J Biochem 243:577–96CrossRefPubMedGoogle Scholar
  81. Hendriksen HV, Larsen S, Ahring BK (1992) Influence of a supplemental carbon source on anaerobic dechlorination of pentachlorophenol in granular sludge. Appl Environ Microbiol 58:365–370Google Scholar
  82. Hermuth K, Leuthner B, Heider J (2002) Operon structure and expression of the genes for benzylsuccinate synthase in Thauera aromatica strain K172. Arch Microbiol 177:132–138Google Scholar
  83. Hess A, Zarda B, Hahn D, Haner A, Stax D, Hohener 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 65:2136–2141Google Scholar
  84. Holliger C, Wohlfarth G, Diekert G (1999) Reductive dechlorination in the energy metabolism of anaerobic bacteria. FEM Microbiol Rev 22:383–398Google Scholar
  85. Huang S, Lindahl PA, Wang C, Bennett GN, Rudolph FB, Hughes JB (2000) 2,4,6-Trinitrotoluene reduction by carbon monoxide dehydrogenase from Clostridium thermoaceticum. Appl Environ Microbiol 66:1474–1478Google Scholar
  86. Huber M, Meyer U, Rys P (2000) Biodegradation mechanisms of linear alcohol ethoxylates under anaerobic conditions. Environ Sci Technol 34:1737–1741Google Scholar
  87. Hutchins SR, Down WC, Wilson JT, Smith GB, Kovacs DA, Fine DD, Douglass RH, Hendrix DJ (1991) Effect of nitrate addition on bioremediation of fuel-contaminated aquifer: field demonstration. Ground Water 29:571–580Google Scholar
  88. Hughes JB, Wang C, Yesland K, Richardson A, Bhadra R, Bennett G, Rudolph F (1998) Bamberger rearrangement during TNT metabolism by Clostridium acetobutylicum. Environ Sci Technol 32:494–500CrossRefGoogle Scholar
  89. Hughes JB, Wang CY, Zhang C (1999) Anaerobic Biotransformation of 2,4-dinitrotoluene and 2,6-dinitrotoluene by Clostridium acetobutylicum: a pathway through dihydroxylamino intermediates. Environ Sci Technol 33:1065–1070Google Scholar
  90. Jablonski PE, Ferry JG (1992) Reductive dechlorination of trichloroethylene by the CO-reduced CO dehydrogenase enzyme complex from Methanosarcina thermophila. FEMS Microbiol Lett 96:55–60Google Scholar
  91. Janke D, Fritsche W (1985) Nature and significance of microbial cometabolism of xenobiotics. J Basic Microbiol 25:603–619Google Scholar
  92. Jewell WJ (1987) Anaerobic sewage treatment, part 6. Environ Sci Technol 21:14–21Google Scholar
  93. Kao CM, Wang JY, Wu MJ (2001) Evaluation of atrazine removal processes in a wetland. Water Sci Technol 44:539–544Google Scholar
  94. Kazumi J, Haggblom MM, Young LY (1995) Diversity of anaerobic microbial processes in chlorobenzoate degradation: nitrate, iron, sulfate and carbonate as electron acceptors. Appl Microbiol Biotechnol 43:929–936Google Scholar
  95. Kitts CL, Cunningham DP, Unkefer PJ (1994) Isolation of three hexahydro-1,3,5-trinitro-1,3,5-triazine degrading species of the family Enterobacteriaceae from nitramine explosive-contaminated soil. Appl Environ Microbiol 60:4608–4711Google Scholar
  96. Kolhatkar R, Kuder T, Philp P, Allen J, Wilson JT (2002) Use of compound-specific stable carbon isotope analyses to demonstrate anaerobic biodegradation of MTBE in groundwater at a gasoline release site. Environ Sci Technol 36:5139–5146Google Scholar
  97. Krieger J, Roseboom W, Albracht SP, Spormann AM (2001) A stable organic free radical in anaerobic benzylsuccinate synthase of Azoarcus sp. strain T. J Biol Chem 276:12924–12927Google Scholar
  98. Kube M, Heider J, Amann J, Hufnagel P, Kuhner S, Beck A, Reinhardt R, Rabus R (2004) Genes involved in the anaerobic degradation of toluene in a denitrifying bacterium, strain EbN1. Arch Microbiol 181:182–194CrossRefPubMedGoogle Scholar
  99. Langenhoff A (2003) In-situ bioremediation of pesticides. (http://www.mep.tno.nl/Informatiebladen_eng/304e.pdf)
  100. Leahy JG, Colwell RR (1990) Microbial degradation of hydrocarbons in the environment. Microbiol Rev 54:305–315PubMedGoogle Scholar
  101. Lenke H, Warrelmann J, Daun G, Hund K, Sieglen U, Knackmuss H-J (1998) Biological treatment of TNT-contaminated soil. 2. Biologically induced immobilization of the contaminants and full-scale application. Environ Sci Technol 32:1964–1971Google Scholar
  102. Leutwein C, Heider J (1999) Anaerobic toluene-catabolic pathway in denitrifying Thauera aromatica: activation and beta-oxidation of the first intermediate, (R)-(+)-benzylsuccinate. Microbiology 145:3265–3271Google Scholar
  103. Leutwein C, Heider J (2002) (R)-Benzylsuccinyl-CoA dehydrogenase of Thauera aromatica, an enzyme of the anaerobic toluene catabolic pathway. Arch Microbiol 178:517–524Google Scholar
  104. Leuthner B, Leutwein C, Schulz H, Horth P, Haehnel W, Schiltz E, Schagger H, Heider J (1998) Biochemical and genetic characterization of benzylsuccinate synthase from Thauera aromatica: a new glycyl radical enzyme catalysing the first step in anaerobic toluene metabolism. Mol Microbiol 28:615–628Google Scholar
  105. Lovley DR, Baedecker MJ, Lonergan DJ, Cozzarelli IM, Phillips EJP, Siegel DI (1989) Oxidation of aromatic contaminants coupled to microbial iron reduction. Nature 339:297–299Google Scholar
  106. Madsen T, Boyd HB, Nylén D, Pedersen AR, Petersen GI, Simonsen F (2001). Environmental and health assessment of substances in household detergents and cosmetic detergent products. Environmental Project No. 615. http://www.mst.dk/udgiv/publications/2001
  107. Magnuson JK, Stern RV, Gossett JM, Zinder SH, Burris DR (1998) Reductive dechlorination of tetrachloroethene to ethene by a two-component enzyme pathway. Appl Environ Microbiol 64:1270–1275Google Scholar
  108. Magnuson JK, Romine MF, Burris DR, Kingsley MT (2000) Trichloroethene reductive dehalogenase from Dehalococcoides ethenogenes: Sequence of tceA and substrate range characterization. Appl Environ Microbiol 66:5141–5147Google Scholar
  109. Major DW, Hodgins WW, Butler BJ (1991) Field and laboratory evidence of in situ biotransformation of tetrachloroethene to ethene and ethane at a chemical transfer facility in North Toronto. In: Hinchee RE, Olfenbuttel (eds) On site bioremediation: processes for xenobiotic and hydrocarbon treatment. Butterworth-Heinemann, Stoneham, Mass. pp 141–171Google Scholar
  110. Marvin-Sikkema FD, de Bont JA (1994) Degradation of nitroaromatic compounds by microorganisms. Appl Microbiol Biotechnol 42:499–507Google Scholar
  111. Master ER, Lai VW-M, Kuipers B, Cullen WR, Mohn WW (2002) Sequential anaerobic-aerobic treatment of soil contaminated with weathered Aroclor 1260. Environ Sci Technol 36:100–103Google Scholar
  112. Matsumura F, Boush GM (1971) DDT metabolized by microorganisms from Lake Michigan. Nature 230:325–326Google Scholar
  113. Maymo-Gatell X, Chien Y, Gossett JM, Zinder SH (1997) Isolation of a bacterium that reductively dechlorinates tetrachloroethene to ethene. Science 276:1568–1571CrossRefPubMedGoogle Scholar
  114. Maymo-Gatell X, Nijenhuis I, Zinder SH (2001) Reductive dechlorination of cis-1,2-dichloroethene and vinyl chloride by “Dehalococcoides ethenogenes”. Environ Sci Technol 35:516–521Google Scholar
  115. McCarty PL (1997) Breathing with chlorinated solvents. Science 276:1521–1522CrossRefPubMedGoogle Scholar
  116. McCarty PL, Smith DP (1986) Anaerobic wastewater treatment. Environ Sci Technol 20:1200–1206Google Scholar
  117. McCarty PL, Wilson JT (1992) Natural anaerobic treatment of a TCE plume St. Joseph, Michigan, NPL site. In: United States Environmental Protection Agency (ed) Bioremediation of hazardous wastes. EPA /600/R-92/126. US EPA, Washington, D.C., pp 57–50Google Scholar
  118. McCormick NG, Cornell JH, Kaplan AM (1981) Biodegradation of hexahydro-1,3,5-trinitro-1,3,5-trazine. Appl Environ Microbiol 42:817–823Google Scholar
  119. McCormick NG, Feeherry FE, Levinson HS (1976) Microbial transformation of 2,4,6-TNT and other nitroaromatic compounds. Appl Environ Microbiol 31:949–958Google Scholar
  120. Meckenstock RU, Annweiler E, Michaelis W, Richnow HH, Schink B (2000) Anaerobic naphthalene degradation by a sulfate-reducing enrichment culture. Appl Environ Microbiol 66:2743–2747Google Scholar
  121. Mihelcic JR, Luthy RG (1988) Microbial-degradation of acenaphthene and naphthalene under denitrification conditions in soil-water systems. Appl Environ Microbiol 54:1188–1198Google Scholar
  122. Mikesell MD, Boyd S (1985) Reductive dechlorination of the pesticides 2,4-D and 2,4,5-T, and pentachlorophenol in anaerobic sludges. J Environ Qual 14:337–340Google Scholar
  123. Mikesell MD, Boyd SA (1986) Complete reductive dechlorination and mineralization of pentachlorophenol by anaerobic microorganisms. Appl Environ Microbiol 52:861–865Google Scholar
  124. Mogensen AS, Dolfing J, Haagensen F, Ahring BK (2003a) Potential for anaerobic conversion of xenobiotics. Adv Biochem Eng Biotechnol 82:69–134Google Scholar
  125. Mogensen AS, Haagensen F, Ahring BK (2003b) Anaerobic degradation of linear alkylbenzene sulfonate. Environ Toxicol Chem 22:706–711Google Scholar
  126. Morgan P, Watkinson RJ (1989) Microbiological methods for the clean up of soil and groundwater contaminated with halogenated organic compounds. FEMS Microbiol Rev 63:277–300Google Scholar
  127. Neumann A, Wohlfarth G, Diekert G (1996) Purification and characterization of tetrachloroethene reductive dehalogenase from Dehalospirillum multivorans. J Biol Chem 271:16515–16519Google Scholar
  128. Newcombe D, Crowley DE (1999) Bioremediation of atrazine-contaminated soil by repeated applications of atrazine-degrading bacteria. Appl Microbiol Biotechnol 51:877–882Google Scholar
  129. Nicholson DK, Woods SL, Istok JD, Peek DC (1992) Reductive dechlorination of chlorophenols by a pentachlorophenol-acclimated methanogenic consortium. Appl Environ Microbiol 58:2280–2286Google Scholar
  130. Ohtsubo Y, Kudo T, Tsuda M, Nagata Y (2004) Strategies for bioremediation of polychlorinated biphenyls. Appl Microbiol Biotechnol 65:250–258Google Scholar
  131. Padda RS, Wang CY, Hughes JB, Bennett GN (2000) Mutagenicity of trinitrotoluene and its metabolites formed during anaerobic degradation by Clostridium acetobutylicum ATCC 824. Environ Toxicol Chem 19:2871–2875Google Scholar
  132. Padda RS, Wang C, Hughes JB, Bennett GN (2003) Mutagenicity of nitroaromatic explosives during anaerobic transformation by Clostridium acetobutylicum. Environ Toxicol Chem 22:2293–2297Google Scholar
  133. Pagano JJ, Scrudato RJ, Roberts RN, Bemis JC (1995) Reductive dechlorination of PCB-contaminated sediments in an anaerobic bioreactor system. Environ Sci Technol 29:2584–2589Google Scholar
  134. Peres CM, Agathos SN (2000) Biodegradation of nitroaromatic pollutants: from pathways to remediation. Biotechnol Annu Rev 6:197–220Google Scholar
  135. Pignatello JJ, Johnson LK, Martinson MM, Carlson RE, Crawford RL (1985) Response of the microflora in outdoor experimental streams to pentachlorophenol: compartmental contributions. Appl Environ Microbiol 50:127–132Google Scholar
  136. Preuss A, Fimpel J, Diekert G (1993) Anaerobic transformation of 2,4,6-trinitrotoluene (TNT). Arch Microbiol 159:345–353Google Scholar
  137. Prince RC (1993) Petroleum spill bioremediation in marine environments. Crit Rev Microbiol 19:217–242Google Scholar
  138. Quensen JF III, Tiedje JM, Boyd SA (1988) Reductive dechlorination of polychlorinated biphenyls by anaerobic microorganisms from sediments. Science 242:752–754Google Scholar
  139. Quensen JF III, Mueller SA, Jain MK, Tiedje JM (1998) Reductive dechlorination of DDE to DDMU in marine sediment microcosms. Science 280:722–724Google Scholar
  140. Quensen JF III , Tiedje JM, Jain MK, Mueller SA (2001) Factors controlling the rate of DDE dechlorination to DDMU in Palos Verdes margin sediments under anaerobic conditions. Environ Sci Technol 35:286–291Google Scholar
  141. Rabus R, Widdel F (1995) Anaerobic degradation of ethylbenzene and other aromatic hydrocarbons by new denitrifying bacteria. Arch Microbiol 163:96–103PubMedGoogle Scholar
  142. Rabus R, Wilkes H, Behrends A, Armstroff A, Fischer T, Pierik AJ, Widdel F (2001) Anaerobic initial reaction of n-alkanes in a denitrifying bacterium: evidence for (1-methylpentyl)succicate as initial product and for involvement of an organic radical in n-hexane metabolism. J Bacteriol 183:1707–1715Google Scholar
  143. Raymond RL (1974) Reclamation of hydrocarbon contaminated ground water. US Patent 3 846 290, 5 November 1974Google Scholar
  144. Renner R (1998) “Natural” remediation of DDT, PCBs debated. Environ Sci Technol 32:360–363AGoogle Scholar
  145. Ribarova I, Topalova J, Ivanov I, Kozuharov D, Dimkov R, Cheng C (2002) Anaerobic sequencing batch reactor as initiating stage in complete pentachlorophenol biodegradation. Water Sci Technol 46:565–569Google Scholar
  146. Rittmann BE, McCarty PL (2001) Environmental biotechnology: principles and applications. McGraw-Hill, New YorkGoogle Scholar
  147. Roberts DJ, Kaake RH, Funk SB, Crawford DL, Crawford RL (1993) Anaerobic remediation of dinoseb from contaminated soil. An on-site demonstration. Appl Biochem Biotechnol 39–40:781–789Google Scholar
  148. Rockne KJ, Strand SE (1998) Biodegradation of bicyclic and polycyclic aromatic hydrocarbons in anaerobic enrichments. Environ Sci Technol 32:3962–3967Google Scholar
  149. Rockne KJ, Chee-Sanford JC, Sanford RA, Hedlund BP, Staley JT, Strand SE (2000) Anaerobic naphthalene degradation by microbial pure culture under nitrate-reducing conditions. Appl Environ Microbiol 66:1595–1601Google Scholar
  150. Rooney-Varga JN, Anderson RT, Fraga JL, Ringelberg D, Loveley DR (1999) Microbial communities associated with anaerobic benzene degradation in a petroleum-contaminated aquifer. Appl Environ Microbiol 65:3056–3063PubMedGoogle Scholar
  151. Rothermich MM, Hayes LA, Lovley DR (2002) Anaerobic, sulfate-dependent degradation of polycyclic aromatic hydrocarbons in petroleum-contaminated harbor sediment. Environ Sci Technol 36:4811–4817Google Scholar
  152. 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 372:455–458Google Scholar
  153. Ruppe S, Neumann A, Vetter W (2003) Anaerobic transformation of compounds of technical toxaphene. I. Regiospecific reaction of chlorobornanes with geminal chlorine atoms. Environ Toxicol Chem 22:2614–2621Google Scholar
  154. Ruppe S, Neumann A, Vetter W (2004) Anaerobic transformation of compounds of technical toxaphene. II. Fate of compounds lacking geminal chlorine atoms. Environ Toxicol Chem 23:591–598Google Scholar
  155. Salminen JM, Tuomi PM, Suortti A-M, Jørgensen KS (2004) Potential for aerobic and anaerobic biodegradation of petroleum hydrocarbons in boreal subsurface. Biodegradation 15:29–39CrossRefPubMedGoogle Scholar
  156. Schink B (2002) Anaerobic digestion: concepts, limits and perspectives. Water Sci Technol 45:1–8Google Scholar
  157. Semprini L, Hopkins GD, McCarty PL, Roberts PV (1992) In situ biotransformation of carbon tetrachloride and other halogenated compounds resulting from biostimulation under anoxic conditions. Environ Sci Technol 26:2454–2461Google Scholar
  158. Sethunathan N (1973) Microbial degradation of insecticides in flooded soil and in anaerobic cultures. Residue Rev 47:143–165Google Scholar
  159. Seybold CA, Mersie W, McNamee C (2001) Anaerobic degradation of atrazine and metolachlor and metabolite formation in wetland soil and water microcosms. J Environ Qual 30:1271–1277Google Scholar
  160. Shelton DR, Tiedje JM (1984) Isolation and partial characterization of bacteria in an anaerobic consortium that mineralizes 3-chlorobenzoic acid. Appl Environ Microbiol 48:840–848Google Scholar
  161. Sheremata TW, Hawari J (2000) Cyclodextrins for desorption and solubilization of 2,4,6-trinitrotoluene and its metabolites from soil. Environ Sci Technol 36:3462–3468Google Scholar
  162. Shimazu M, Mulchandani A, Chen W (2001) Simultaneous degradation of organophosphorus pesticides and p-nitrophenol by a genetically engineered Moraxell sp. with surface-expressed organophosphorus hydrolase. Biotechnol Bioeng 76:318–324Google Scholar
  163. So CM, Young LY (1999a) Initial reactions in anaerobic alkane degradation by a sulfate reducer, strain AK-01. Appl Environ Microbiol 65:5532–5540Google Scholar
  164. So CM, Young LY (1999b) Isolation and characterization of a sulfate-reducing bacterium that anaerobically degrades alkanes. Appl Environ Microbiol 65:2969–2976Google Scholar
  165. So CM, Phelps CD, Young LY (2003) Anaerobic transformation of alkanes to fatty acids by a sulfate-reducing bacterium, strain Hxd3. Appl Environ Microbiol 69:3892–3900Google Scholar
  166. Somsamak P, Cowan RM, Haggblom MM (2001) Anaerobic biotransformation of fuel oxygenates under sulfate-reducing conditions. FEMS Microbiol Ecol 37:259–264Google Scholar
  167. Song B, Palleroni NJ, Haggblom MM (2000) Isolation and characterization of diverse halobenzoate-degrading denitrifying bacteria from soils and sediments. Appl Environ Microbiol 66:3446–3453Google Scholar
  168. Song B, Palleroni NJ, Kerkhof LJ, Haggblom MM (2001) Characterization of halobenzoate-degrading, denitrifying Azoarcus and Thauera isolates and description of Thauera chlorobenzoica sp. nov. Int J Syst Evol Microbiol 51:589–602Google Scholar
  169. Spormann AM, Widdel F (2000) Metabolism of alkylbenzenes, alkanes, and other hydrocarbons in anaerobic bacteria. Biodegradation 11:85–105CrossRefPubMedGoogle Scholar
  170. Steber J, Wierich P (1987) The anaerobic degradation of detergent range fatty alcohol ethoxylates. Studies with 14C-labbelled model surfactant. Water Res 21:661–667Google Scholar
  171. Steinbach A, Seifert R, Annweiler E, Michaelis W (2004) Hydrogen and carbon isotope fractionation during anaerobic biodegradation of aromatic hydrocarbons-a field study. Environ Sci Technol 38:609–616Google Scholar
  172. Stocking AJ, Deeb RA, Flores AE, Stringfellow W, Talley J, Brownell R, Kavanaugh MC (2000) Bioremediation of MTBE: a review from a practical perspective. Biodegradation 11:187–201Google Scholar
  173. Strong LC, McTavish H, Sadowsky MJ, Wackett LP (2000) Field-scale remediation of atrazine-contaminated soil using recombinant Escherichia coli expressing atrazine chlorohydrolase. Environ Microbiol 2:91–98Google Scholar
  174. Sullivan ER, Zhang X, Phelps C, Young LY (2001) Anaerobic mineralization of stable-isotope-labeled 2-methylnaphthalene. Appl Environ Microbiol 67:4353–4357Google Scholar
  175. Sung Y, Ritalahti KM, Sanford RA, Urbance JW, Flynn SJ, Tiedje JM, Löffler FE (2003) Characterization of two tetrachloroethene-reducing, acetate-oxidizing anaerobic bacteria and their description as Desulfuromonas michiganesis sp. nov. Appl Environ Microbiol 69:2964–2974Google Scholar
  176. Swisher RD (1987) Surfactant biodegradation, 2nd edn. Dekker, New York, N.Y.Google Scholar
  177. Tadros MG, Crawford A, Mateo-Sullivan A, Zhang C, Hughes JB (2000) Toxic effects of hydroxylamino intermediates on algae Selenastrum capricornutum. Bull Environ Contam Toxicol 64:579–585Google Scholar
  178. Tartakovsky B, Levesque M, Dumortier R, Beaudet R, Guiot SR (1999) Biodegradation of pentachlorophenol in a continuous anaerobic reactor augmented with Desulfitobacterium frappieri PCP-1. Appl Environ Microbiol 65:4357–4362Google Scholar
  179. Ternan NG, McGrath JW, McMullan G, Quinn JP (1998) Organophosphonates: occurrence, synthesis and biodegradation by microorganisms. World J Microbiol Biotechnol 14:635–647Google Scholar
  180. Terzenbach DP, Blaut M (1994) Transformation of tetrachloroethylene to trichloroethylene by homoacetogenic bacteria. FEMS Microbiol Lett 123:213–218Google Scholar
  181. Tiedje JM, Quensen JF III, Chee-Sanford J, Schimel JP, Boyd SA (1993) Microbial reductive dechlorination of PCBs. Biodegradation 4:231–240PubMedGoogle Scholar
  182. Vargas C, Song B, Camps M, Haggblom MM (2000) Anaerobic degradation of fluorinated aromatic compounds. Appl Microbiol Biotechnol 53:342–347Google Scholar
  183. Vargas C, Fennell DE, Häggblom MM (2001) Anaerobic reductive dechlorination of chlorinated dioxins in estuarine sediments. Appl Microbiol Biotechnol 57:786–790Google Scholar
  184. Wackett LP, Sadosky MJ, Martinez B, Shapir N (2002) Biodegradation of atrazine and related s-triazine compounds: from enzymes to field studies. Appl Microbiol Biotechnol 58:39–45CrossRefPubMedGoogle Scholar
  185. Wagener S, Schink B (1988) Fermentative degradation of nonionic surfactants and polyethylene glycol by enrichment cultures and by pure cultures of homoacetogenic and propionate-forming bacteria. Appl Environ Microbiol 54:561–565Google Scholar
  186. Wedemeyer G (1966) Dechlorination of DDT by Aerobacter aerogenes. Science 152:647Google Scholar
  187. Widdel F, Rabus R (2001) Anaerobic biodegradation of saturated and aromatic hydrocarbons. Curr Opin Biotechnol 12:259–276Google Scholar
  188. Wiegel J, Zhang X, Wu Q (1999) Anaerobic dehalogenation of hydroxylated polychlorinated biphenyls by Desulfitobacterium dehalogenans. Appl Environ Microbiol 65:2217–2221Google Scholar
  189. Wilkes H, Rabus R, Fischer T, Armstroff A, Behrends A, Widdel F (2002) Anaerobic degradation of n-hexane in a denitrifying bacterium: further degradation of the initial intermediate (1-methylphentyl)succinate via C-skeleton rearrangement. Arch Microbiol 177:235–243Google Scholar
  190. Williams PP (1977) Metabolism of synthetic organic pesticides by anaerobic microorganisms. Residue Rev 66:63–135Google Scholar
  191. Woods SL, Ferguson JF, Benjamin MM (1989) Characterization of chlorophenol and chloromethoxybenzene biodegradation during anaerobic treatment. Environ Sci Technol 23:62–68Google Scholar
  192. Wu Q, Bedard DL, Wiegel J (1997) Temperature determines pattern of anaerobic microbial dechlorination of Aroclor 1260 primed by 2,3,4,6-tetrachlorobiphenyl in Woods Pond sediments. Appl Environ Microbiol 63:4818–4825Google Scholar
  193. Wu Q, Sowers KR, May HD (1998) Microbial reductive dechlorination of Aroclor 1260 in anaerobic slurries of estuarine sediments. Appl Environ Microbiol 64:1052–1058Google Scholar
  194. Wu Q, Sowers KR, May HD (2000) Establishment of a polychlorinated biphenyl-dechlorinating microbial consortium, specific for doubly flanked chlorines, in a defined, sediment-free medium. Appl Environ Microbiol 66:49–53Google Scholar
  195. Wu Q, Milliken CE, Meier GP, Watts JE, Sowers KR, May HD (2002a) Dechlorination of chlorobenzenes by a culture containing bacterium DF-1, a PCB dechlorinating microorganism. Environ Sci Technol 36:3290–3294CrossRefPubMedGoogle Scholar
  196. Wu Q, Watts JE, Sowers KR, May HD (2002b) Identification of a bacterium that specifically catalyzes the reductive dechlorination of polychlorinated biphenyls with doubly flanked chlorines. Appl Environ Microbiol 68:807–812Google Scholar
  197. Xue SK, Iskandar IK, Selim HM (1995) Adsorption-desorption of 2,4,6-trinitrotoluene and hexahydro-1,3,5-trinitro-1,3,5-triazine in soils. Soil Sci 160:317–327Google Scholar
  198. Young DM, Unkefer PJ, Ogden KL (1997) Biotransformation of hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) by a prospective consortium and its most effective isolate Serratia marcescens. Biotechnol Bioeng 53:515–522Google Scholar
  199. Zengler K, Richnow HH, Rosselló-Mora R, Michaelis W, Widdel F (1999) Methane formation from long-chain alkanes by anaerobic microorganisms. Nature 401:266–269Google Scholar
  200. Zhang C, Hughes JB (2003) Biodegradation pathways of hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) by Clostridium acetobutylicum cell-free extract. Chemosphere 50:665–671Google Scholar
  201. Zhang C, Hughes JB, Nishino SF, Spain J (2000a) Slurry-phase biological treatment of 2,4-dinitrotoluene and 2,6-dinitrotoluene: Role of bioaugmentation and effects of high dinitrotoluene concentrations. Environ Sci Technol 34:2810–2816Google Scholar
  202. Zhang X, Young LY (1997) Carboxylation as an initial reaction in the anaerobic metabolism of naphthalene and phenanthrene by sulfidogenic consortia. Appl Environ Microbiol 63:4759–4764Google Scholar
  203. Zhang X, Sullivan ER, Young LY (2000b) Evidence for aromatic ring reduction in the biodegradation pathway of carboxylated naphthalene by a sulfate-reducing consortium. Biodegradation 11:117–124Google Scholar
  204. Zhao J-S, Halasz A, Paquet L, Beaulieu C, Hawari J (2002) Biotransformation of hexahydro-1,3,5-trnitro-1,3,5-triazine and its mononitroso derivative hexahydro-1-nitroso-3,5-dinitro-1,3,5-triazine by Klebsiella pneumoniae strain SCZ-1 isolated from an anaerobic sludge. Appl Environ Microbiol 68:5336–5341Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Department of Environmental SciencesUniversity of Houston-Clear LakeHoustonUSA
  2. 2.Department of Biochemistry and Cell BiologyRice UniversityHoustonUSA

Personalised recommendations