Advertisement

Biodegradation of the Explosives TNT, RDX and HMX

  • Anat Bernstein
  • Zeev Ronen
Chapter
Part of the Environmental Science and Engineering book series (ESE)

Abstract

In the early twentieth century, more than 60 highly explosive compounds were developed and synthesized for military and civilian use. Of these, the most widely used explosives in the world are probably hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX), 2,4,6-trinitrotoluene (TNT) and octahydro-1,3,5,7-tetranitro-1,3,5,7-tetrazocine (HMX).

Keywords

Nitro Group Ring Cleavage Sequential Reduction Aerobic Denitration Rhodococcus Strain 
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

Acknowledgments

The work of A. Bernstein was supported by a generous contribution from Vera Barcza, Toronto, Canada Rosinger-Barcza Family Fund In support of Young Researchers at the Zuckerberg Institute for Water Research. This work was also supported in part by a grant 167/2008 from Israel Science Foundation.

References

  1. Achtnich C, Sieglen U, Knackmuss H-J, Lenke H (1999) Irreversible binding of biologically reduced 2,4,6-trinitrotoluene to soil. Environ Toxicol Chem 18:2416–2423Google Scholar
  2. Adrian NR, Arnett CM (2004) Anaerobic biodegradation of hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) by Acetobacterium malicum strain HAAP-1 isolated from a methanogenic mixed culture. Curr Microbiol 48:332–340Google Scholar
  3. Adrian NR, Arnett CM (2007) Anaerobic biotransformation of explosives in aquifer slurries amended with ethanol and propylene glycol. Chemosphere 66:1849–1856Google Scholar
  4. Adrian NR, Arnett CM, Hickey RF (2003) Stimulating the anaerobic biodegradation of explosives by the addition of hydrogen or electron donors that produce hydrogen. Water Res 37:3499–3507Google Scholar
  5. Allard A-S, Neilson AH (1997) Bioremediation of organic waste sites: a critical review of microbiological aspects. Intl Biodeter Biodegrad 39:253–285Google Scholar
  6. Alvarez MA, Kitts CL, Botsford JL, Unkefer PJ (1995) Pseudomonas aeruginosa strain MA01 aerobically metabolizes the aminodinitrotoluenes produced by 2,4,6-trinitrotoluene nitro group reduction. Can J Microbiol 41:984–991Google Scholar
  7. Angermaier L, Simon H (1983) On nitroaryl reductase activities in several Clostridia. Hoppe-Seylers Z Physiol Chem 364:1653–1663Google Scholar
  8. Arnett CM, Adrian NR (2009) Cosubstrate independent mineralization of hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) by a Desulfovibrio species under anaerobic conditions. Biodegradation 20:15–26Google Scholar
  9. ATSDR (1996a) 2,4,6-Trinitrotoluene (TNT) Fact Sheet. Agency for toxic substances and disease registry (ATSDR). Available from: http://www.atsdr.cdc.gov/toxfaqs/tfacts81.pdf
  10. ATSDR (1996b) RDX Fact Sheet. Agency for toxic substances and disease registry (ATSDR). Available from: http://www.atsdr.cdc.gov/toxfaqs/tfacts78.pdf
  11. ATSDR (1997) HMX Fact Sheet. Agency for toxic substances and disease registry (ATSDR). Available from: http://www.atsdr.cdc.gov/toxfaqs/tfacts98.pdf
  12. Behrend C, Heesche-Wagner K (1999) Formation of hydride-Meisenheimer complexes of picric acid (2,4,6-trinitrophenol) and 2,4-dinitrophenol during mineralization of picric acid by Nocardioides sp. strain CB22–2. Appl Environ Microbiol 65:1372–1377Google Scholar
  13. Beller HR, Tiemeier K (2002) Use of liquid chromatography/tandem mass spectrometry to detect distinctive indicators of in situ RDX transformation in contaminated groundwater. Environ Sci Technol 36:2060–2066Google Scholar
  14. Beller HR, Madrid V, Hudson GB, McNab WW, Carlsen T (2004) Biogeochemistry and natural attenuation of nitrate in groundwater at an explosives test facility. Appl Geochem 19:1483–1494Google Scholar
  15. Bernstein A, Ronen Z, Adar E, Nativ R, Lowag H, Stichler W, Meckenstock RU (2008) Compound-specific isotope analysis of RDX and stable isotope fractionation during aerobic and anaerobic biodegradation. Environ Sci Technol 42:7772–7777Google Scholar
  16. Bernstein A, Adar E, Ronen Z, Lowag H, Stichler W, Meckenstock RU (2010) Quantifying RDX biodegradation in groundwater using ?15N isotope analysis. J Contam Hydrol 111:25–35Google Scholar
  17. Bernstein A, Adar E, Nejidat A, Ronen Z (2011) Isolation and characterization of RDX-degrading Rhodococcus species from a contaminated aquifer. Biodegradation 22:997–1005Google Scholar
  18. Best EPH, Sprecher SL, Larson SL, Fredrickson HL, Bader DF (1999) Environmental behavior of explosives in groundwater from the Milan Army Ammunition Plant in aquatic and wetland plant treatments. Uptake and fate of TNT and RDX in plants. Chemosphere 39:2057–2072Google Scholar
  19. Bhushan B, Paquet L, Halasz A, Spain JC, Hawari J (2003a) Mechanism of xanthine oxidase catalyzed biotransformation of HMX under anaerobic conditions. Biochem Biophys Res Commun 306:509–515Google Scholar
  20. Bhushan B, Trott S, Spain JC, Halasz A, Paquet L, Hawari J (2003b) Biotransformation of hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) by a rabbit liver cytochrome P450: insight into the mechanism of RDX biodegradation by Rhodococcus sp. strain DN22. Appl Environ Microbiol 69:1347–1351Google Scholar
  21. Bhushan B, Halasz A, Thiboutot S, Ampleman G, Hawari J (2004) Chemotaxis-mediated biodegradation of cyclic nitramine explosives RDX, HMX, and CL-20 by Clostridium sp. EDB2. Biochem Biophys Res Commun 316:816–821Google Scholar
  22. Binks PR, Nicklin S, Bruce NC (1995) Degradation of hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) by Stenotrophomonas maltophilia PB1. Appl Environ Microbiol 61:1318–1322Google Scholar
  23. Blehert DS, Fox BG, Chambliss GH (1999) Cloning and sequence analysis of two Pseudomonas flavoprotein xenobiotic reductases. J Bacteriol 181:6254–6263Google Scholar
  24. Bockelmann A, Zamfirescu D, Ptak T, Grathwhol P, Teutsch G (2003) Quantification of mass fluxes and natural attenuation rates at an industrial site with a limited monitoring network: a case study. J Contam Hydrol 60:97–121Google Scholar
  25. Boopathy R (1994) Transformation of nitroaromatic compounds by a methanogenic bacterium, Methanococcus sp (strain B). Arch Microbiol 162:167–172Google Scholar
  26. Boopathy R (2000) Bioremediation of explosives contaminated soil. Intl Biodeter Biodegrad 46:29–36Google Scholar
  27. Boopathy R (2001) Enhanced biodegradation of cyclotetramethylenetetranitramine (HMX) under mixed electron-acceptor condition. Biores Technol 76:241–244Google Scholar
  28. 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
  29. Boopathy R, Kulpa CF (1994) Biotransformation of 2,4,6-trinitrotoluene (TNT) by a Methanococcus sp (strain B) isolated from a lake sediment. Can J Microbiol 40:273–278Google Scholar
  30. Boopathy R, Manning JF (1996) Characterization of partial anaerobic metabolic pathway for 2,4,6-trinitrotoluene degradation by a sulfate-reducing bacterial consortium. Can J Microbiol 42:1203–1208Google Scholar
  31. Boopathy R, Kulpa CF, Wilson M (1993) Metabolism of 2,4,6-trinitrotoluene (TNT) by Desulfovibrio sp (B strain). Appl Microbiol Biotechnol 39:270–275Google Scholar
  32. Boopathy R, Manning J, Kulpa CF (1997) Optimization of environmental factors for the biological treatment of trinitrotoluene-contaminated soil. Arch Environ Contam Toxicol 32:94–98Google Scholar
  33. Borch T, Inskeep WP, Harwood JA, Gerlach R (2005) Impact of ferrihydrite and anthraquinone-2,6-disulfonate on the reductive transformation of 2,4,6-trinitrotoluene by a gram-positive fermenting bacterium. Environ Sci Technol 39:7126–7133Google Scholar
  34. Bordeleau G, Savard MM, Martel R, Ampleman G, Thiboutot S (2008) Determination of the origin of groundwater nitrate at an air weapons range using the dual isotope approach. J Contam Hydrol 98:97–105Google Scholar
  35. Brenner A, Ronen Z, Harel Y, Abeliovich A (2000) Degradation of RDX during biological treatment of munitions waste. Water Environ Res 72:469–475Google Scholar
  36. Charles PT, Gauger PR, Patterson CH Jr, Kusterbeck AW (2000) On-site immunoanalysis of nitrate and nitroaromatic compounds in groundwater. Environ Sci Technol 34:4641–4650Google Scholar
  37. Cho Y-S, Lee B-U, Oh K-H (2008) Simultaneous degradation of nitroaromatic compounds TNT, RDX, atrazine, and simazine by Pseudomonas putida HK-6 in bench-scale bioreactors. J Chem Technol Biotechnol 83:1211–1217Google Scholar
  38. Clark B, Boopathy R (2007) Evaluation of bioremediation methods for the treatment of soil contaminated with explosives in Louisiana Army Ammunition Plant, Minden, Louisiana. J Hazard Mater 143:643–648Google Scholar
  39. Claus H, Bausinger T, Lehmler I, Perret N, Fels G, Dehner U, Preuß J, König H (2007) Transformation of 2,4,6-trinitrotoluene (TNT) by Raoultella terrigena. Earth Environ Sci 18:27–35Google Scholar
  40. Coleman NV, Nelson DR, Duxbury T (1998) Aerobic biodegradation of hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) as a nitrogen source by a Rhodococcus sp., strain DN22. Soil Biol Biochem 30:1159–1167Google Scholar
  41. Coleman NV, Spain JC, Duxbury T (2002) Evidence that RDX biodegradation by Rhodococcus strain DN22 is plasmid-borne and involves a cytochrome p-450. J Appl Microbiol 93:463–472Google Scholar
  42. Cooper PW, Kurowski SR (1997) Chemistry of explosives. In: Introduction to the Technology of Explosives. Wiley-VCH Inc, New York, pp 1–38Google Scholar
  43. Crocker FH, Indest KJ, Fredrickson HL (2006) Biodegradation of the cyclic nitramine explosives RDX, HMX, and CL-20. Appl Microbiol Biotechnol 73:274–290Google Scholar
  44. Danielson PB (2002) The cytochrome P450 superfamily: biochemistry, evolution and drug metabolism in humans. Curr Drug Metab 37:561–597Google Scholar
  45. Darrach MR, Chutjian A, Plett GA (1998) Trace explosives signatures from World War II unexploded undersea ordnance. Environ Sci Technol 32:1354–1358Google Scholar
  46. 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
  47. Diegor EJM, Abrajano T, Stehmeier L, Patel T, Winsor L (1999) In: Proceedings of the 19th international meeting on organic geochemistry, Istanbul, Turkey, pp 29Google Scholar
  48. DiGnazio FJ, Krothe NC, Baedke SJ, Spalding RF (1998) ?15N of nitrate derived from explosive sources in karst aquifer beneath the ammunition burning ground. J Hydrol 206:164–175Google Scholar
  49. Drzyzga O, Gorontzy T, Schmidt A, Blotevogel KH (1995) Toxicity of explosives and related compounds to the luminescent bacterium Vibrio fischeri NRRL-B-11177. Arch Environ Contam Toxicol 28:229–235Google Scholar
  50. Drzyzga O, Bruns-Nagel D, Gorontzy T, Blotevogel K-H, von Löw E (1999) Anaerobic incorporation of the radiolabeled explosive TNT and metabolites into the organic soil matrix of contaminated soil after different treatment procedures. Chemosphere 38:2081–2095Google Scholar
  51. Duque E, Ha?dour A, Godoy F, Ramos J-L (1993) Construction of a Pseudomonas hybrid strain that mineralizes 2,4,6-trinitrotoluene. J Bacteriol 175:2278–2283Google Scholar
  52. Ederer MM, Lewis TA, Crawford RL (1997) 2,4,6-Trinitrotoluene (TNT) transformation by Clostridia isolated from a munition-fed bioreactor: comparison with non-adapted bacteria. J Ind Microbiol Biotechnol 18:82–88Google Scholar
  53. Esteve-Núñez A, Ramos JL (1998) Metabolism of 2,4,6-trinitrotoluene by Pseudomonas sp. JLR11. Environ Sci Technol 32:3802–3808Google Scholar
  54. Esteve-Nuñez A, Lucchesi G, Philipp B, Schink B, Ramos JL (2000) Respiration of 2,4,6-trinitrotoluene by Pseudomonas sp. strain JLR11. J Bacteriol 182:1352–1355Google Scholar
  55. Esteve-Núñez A, Caballero A, Ramos JL (2001) Biological degradation of 2,4,6trinitrotoluene. Microbiol Mol Biol Rev 65:335–352Google Scholar
  56. Eyers L, Stenuit L, Agathos SN (2008) Denitration of 2,4,6-trinitrotoluene by Pseudomonas aeruginosa ESA-5 in the presence of ferrihydrite. Appl Microbiol Biotechnol 79:489–497Google Scholar
  57. Fiorella PD, Spain JC (1997) Transformation of 2,4,6-trinitrotoluene by Pseudomonas pseudoalcaligenes JS52. Appl Environ Microbiol 63:2007–2015Google Scholar
  58. Fournier D, Halasz A, Spain J, Fiurasek P, Hawari J (2002) Determination of key metabolites during biodegradation of hexahydro-1,3,5-trinitro-1,3,5-triazine with Rhodococcus sp. strain DN22. Appl Environ Microbiol 68:166–172Google Scholar
  59. Fournier D, Halasz A, Thiboutot S, Ampleman G, Manno D, Hawari J (2004) Biodegradation of octahydro-1,3,5,7-tetranitro-1,3,5,7-tetrazocine (HMX) by Phanerochaete chrysosporium: new insight into the degradation pathway. Environ Sci Technol 38:4130–4133Google Scholar
  60. Freedman DL, Sutherland KW (1998) Biodegradation of hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) under nitrate-reducing conditions. Water Sci Technol 38:33–40Google Scholar
  61. French CE, Nicklin S, Bruce NC (1998) Aerobic degradation of 2,4,6-trinitrotoluene by Enterobacter cloacae PB2 and by pentaerythritol tetranitrate reductase. Appl Environ Microbiol 64:2864–2868Google Scholar
  62. Fuchs JS, Oneto ML, Casabé NB, Gómez Segura O, Tarulla R, Vaccarezza M, Sánchez-Rivas C, Kesten EM, Wood EJ (2001) Ecotoxicological characterization of a disposal lagoon from a munition plant. Bull Environ Contam Toxicol 67:696–703Google Scholar
  63. Fuller ME, Manning JF (1997) Aerobic gram-positive and gram-negative bacteria exhibit differential sensitivity to and transformation of 2,4,6-trinitrotoluene (TNT). Curr Microbiol 35:77–83Google Scholar
  64. Fuller M, McClay K, Hawari J, Paquet L, Malone T, Fox B, Steffan R (2009) Transformation of RDX and other energetic compounds by xenobiotic reductases XenA and XenB. Appl Microbiol Biotechnol 84:535–544Google Scholar
  65. Fuller ME, Perreault N, Hawari J (2010) Microaerophilic degradation of hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) by three Rhodococcus strains. Lett Appl Microbiol 51:313–318Google Scholar
  66. Funk SB, Roberts DJ, Crawford DL, Crawford RL (1993) Initial-phase optimization for bioremediation of munition compound-contaminated soils. Appl Environ Microbiol 59:2171–2177Google Scholar
  67. Gelman F, Kotlyar A, Chiguala D, Ronen Z (2011) Precise and accurate compound-specific carbon and nitrogen isotope analysis of RDX by GC-IRMS. Intl J Environ Anal Chem (in press)Google Scholar
  68. George SE, Huggins-Clark G, Brooks LR (2001) Use of a Salmonella microsuspension bioassay to detect the mutagenicity of munitions compounds at low concentrations. Mutation Res 490:45–56Google Scholar
  69. Gilcrease CP, Murphy VG (1995) Bioconversion of 2,4-diamino-6-nitrotoluene to a novel metabolite under anoxic and aerobic conditions. Appl Environ Microbiol 61:4209–4214Google Scholar
  70. Groom CA, Beaudet S, Halasz A, Paquet L, Hawari J (2001) Detection of the cyclic nitramine explosives hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) and octahydro-1,3,5,7-tetranitro-1,3,5,7-tetrazine (HMX) and their degradation products in soil environments. J Chromatogr A 909:53–60Google Scholar
  71. Haïdour A, Ramos JL (1996) Identification of products resulting from the biological reduction of 2,4,6-trinitrotoluene, 2,4-dinitrotoluene and 2,6-dinitrotoluene by Pseudomonas sp. Environ Sci Technol 30:2365–2370Google Scholar
  72. Halasz A, Spain J, Paquet L, Beaulieu C, Hawari J (2002) Insights into the formation and degradation mechanisms of methylenedinitramine during the incubation of RDX with anaerobic sludge. Environ Sci Technol 36:633–638Google Scholar
  73. Halasz A, Manno D, Strand SE, Bruce NC, Hawari J (2010) Biodegradation of RDX and MNX with Rhodococcus sp. strain DN22: new insights into the degradation pathway. Environ Sci Technol 44:9330–9336Google Scholar
  74. Hartenbach A, Hofstetter TB, Berg M, Bolotin J, Schwarzenbach RP (2006) Using nitrogen isotope fractionation to assess abiotic reduction of nitroaromatic compounds. Environ Sci Technol 40:7710–7716Google Scholar
  75. Hawari J, Halasz A, Paquet L, Zhou E, Spencer B, Ampleman G, Thiboutot S (1998) Characterization of metabolites in the biotransformacion of 2,4,6-trinitrotoluene with anaerobic sludge: role of triaminotoluene. Appl Environ Microbiol 64:2200–2206Google Scholar
  76. Hawari J, Halasz A, Beaudet S, Paquet L, Ampleman G, Thiboutot S (1999) Biotransformation of 2,4,6-trinitrotoluene with Phanerochaete chrysosporium in agitated cultures at pH 4.5. Appl Environ Microbiol 65:2977–2986Google Scholar
  77. Hawari J, Beaudet S, Halasz A, Thiboutot S, Ampleman G (2000a) Microbial degradation of explosives: biotransformation versus mineralization. Appl Microbiol Biotechnol 54:605–618Google Scholar
  78. Hawari J, Halasz A, Sheremata T, Beaudet S, Groom C, Paquet L, Rhofir C, Ampleman G, Thiboutot S (2000b) Characterization of metabolites during biodegradation of hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) with municipal anaerobic sludge. Appl Environ Microbiol 66:2652–2657Google Scholar
  79. Hawari J, Halasz A, Beaudet S, Paquet L, Ampleman G, Thiboutot S (2001) Biotransformation routes of octahydro-1,3,5,7-tetranitro-1,3,5,7-tetrazocine by municipal anaerobic sludge. Environ Sci Technol 35:70–75Google Scholar
  80. Hlavica P (2009) Assembly of non-natural electron transfer conduits in the cytochrome P450 system: a critical assessment and update of artificial redox constructs amenable to exploitation in biotechnological areas. Biotechnol Adv 27:103–121Google Scholar
  81. Hoffsommer JC, Kubose DA, Glover DJ (1977) Kinetic isotope effects and intermediate formation for the aqueous alkaline homogeneous hydrolysis of 1,3,5-triaza-1,3,5-trinitrocyclohexane (RDX). J Phys Chem 81:380–385Google Scholar
  82. Hofstetter TB, Neumann A, Arnold WA, Bolotin J, Cramer CJ, Schwarzenbach RP (2008) Substituent effects on nitrogen isotope fractionation during abiotic reduction of nitroaromatic compounds. Environ Sci Technol 42:1997–2003Google Scholar
  83. 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
  84. Hughes JB, Wang C, Yesland K, Richardson A, Bhadra R, Bennet G, Rudolph F (1998) Bamberger rearrangement during TNT metabolism by Clostridium acetobutylicum. Environ Sci Technol 32:494–500Google Scholar
  85. Hunkeler D, Chollet N, Pittet X, Aravena R, Cherry JA, Parker BL (2004) Effect of source variability and transport processes on carbon isotope ratio of TCE and PCE in two sandy aquifers. J Contam Hydrol 74:265–282Google Scholar
  86. Indest KJ, Crocker FH, Athow R (2007) A TaqMan polymerase chain reaction method for monitoring RDX-degrading bacteria based on the xplA functional gene. J Microbiol Methods 68:267–274Google Scholar
  87. Indest KJ, Jung CM, Chen H-P, Hancock D, Florizone C, Eltis LD, Crocker FH (2010) Functional characterization of pGKT2, a 182-kilobase plasmid containing the xplAB genes, which are involved in the degradation of hexahydro-1,3,5-trinitro-1,3,5-triazine by Gordonia sp. strain KTR9. Appl Environ Microbiol 76:6329–6337Google Scholar
  88. Jackson RJ, Rylott EL, Fournier D, Hawari J, Bruce NC (2007) Exploring the biochemical properties and remediation applications of the unusual explosive-degrading P450 system XplA/B. Proc Natl Acad Sci U S A 104:16822–16827Google Scholar
  89. Kalafut T, Wales ME, Rastogi VK, Naumova RP, Zaripova SK, Wild JR (1998) Biotransformation patterns of 2,4,6-trinitrotoluene by aerobic bacteria. Curr Microbiol 36:45–54Google Scholar
  90. Khan TA, Bhadra R, Hughes J (1997) Anaerobic transformation of 2,4,6-TNT and related nitroaromatic compounds by Clostridium acetobutylicum. J Ind Microbiol Biotechnol 18:198–203Google Scholar
  91. Kim HY, Song HG (2000) Comparison of 2,4,6-trinitrotoluene degradation by seven strains of white rot fungi. Curr Microbiol 41:317–320Google Scholar
  92. Kim H-Y, Bennett GN, Song H-G (2002) Degradation of 2,4,6-trinitrotoluene by Klebsiella sp isolated from activated sludge. Biotechnol Lett 24:2023–2028Google Scholar
  93. 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
  94. Kitts CL, Green CE, Otley RA, Alvarez MA, Unkefer PJ (2000) Type 1 nitroreductases in soil enterobacteria reduce TNT (2,4,6-trinitrotoluene) and RDX (hexahydro-1,3,5-trinitro-1,3,5-triazine). Can J Microbiol 26:278–282Google Scholar
  95. Kuder T, Wilson JT, Kaiser P, Kolhatkar R, Philp P, Allen J (2005) Enrichment of stable carbon and hydrogen isotopes during anaerobic biodegradation of MTBE: microcosm and field evidence. Environ Sci Technol 39:213–220Google Scholar
  96. Kwon MJ, Finneran KT (2008) Biotransformation products and mineralization potential for hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) in abiotic versus biological degradation pathways with anthraquinone-2,6-disulfonate (AQDS) and Geobacter metallireducens. Biodegradation 19:705–715Google Scholar
  97. Lachance B, Robidoux PY, Hawari J, Ampleman G, Thiboutot S, Sunahara GI (1999) Cytotoxic and genotoxic effects of energetic compounds on bacterial and mammalian cells in vitro. Mutat Res 444:25–39Google Scholar
  98. Lenke H, Knackmuss H-J (1992) Initial hydrogenation during catabolism of picric acid by Rhodococcus erythropolis HL 24–2. Appl Environ Microbiol 58:2933–2937Google Scholar
  99. Lewin U, Efer J, Engewald W (1996) High-performance liquid chromatographic analysis with electrochemical detection for residues of explosives in water samples around a former ammunition plant. J Chromatogr A 730:161–167Google Scholar
  100. Lewis TA, Goszczynski S, Crawford RL, Korus RA, Admassu W (1996) Products of anaerobic 2,4,6-trinitrotoluene (TNT) transformation by Clostridium bifermentans. Appl Environ Microbiol 62:4669–4674Google Scholar
  101. Mak KS, Griebler C, Meckenstock RU, Liedl R, Peter A (2006) Combined application of conservative transport modelling and compound-specific carbon isotope analyses to assess in situ attenuation of benzene, toluene, and o-xylene. J Contam Hydrol 88:306–320Google Scholar
  102. Martel R, Robertson TJ, Doan MQ, Thiboutot S, Ampleman G, Provatas A, Jenkins T (2008) 2,4,6-Trinitrotoluene in soil and groundwater under a waste lagoon at the former explosives factory Maribyrnong (EFM), Environ Geol 53:1249–1259Google Scholar
  103. 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
  104. McCormick NG, Cornell JH, Kaplan AM (1981) Biodegradation of hexahydro-1,3,5-trinitro-1,3,5-triazine. Appl Environ Microbiol 42:817–823Google Scholar
  105. McGrath CJ (1995) Review of formulations for processes affecting the subsurface transport of explosives. Technical Report IRRP-95-2. US Army Corps of Engineers, Waterways Experiment Station, Vicksburg, MSGoogle Scholar
  106. McGuire RR, Lee CG, Velsko CA, Raber E (1995) Application of stable isotope ratios to the analysis of explosive residues. In: Proceedings of the fifth international symposium on the analysis and detection of explosives, Washington DC, Dec 4–8Google Scholar
  107. McKelvie JR, Lindstrom JE, Beller HR, Richmond SA, Sherwood Lollar B (2005) Analysis of anaerobic BTX biodegradation in a subarctic aquifer using isotopes and benzylsuccinates. J Contam Hydrol 81:167–186Google Scholar
  108. McKelvie JR, Mackay DM, de Sieyes NR, Lacrampe-Couloume G, Sherwood Lollar B (2007) Quantifying MTBE biodegradation in the Vandenberg Air Force Base ethanol release study using stable carbon isotopes. J Contam Hydrol 94:157–165Google Scholar
  109. Meckenstock RU, Morasch B, Griebler C, Richnow HH (2004) Stable isotope fractionation analysis as a tool to monitor biodegradation in contaminated aquifers. J Contam Hydrol 75:215–255Google Scholar
  110. Montpas S, Samson J, Langlois E, Lei J, Piche Y, Chêvenert R (1997) Degradation of 2,4,6-trinitrotoluene by Serratia marcescens. Biotechnol Lett 19:291–294Google Scholar
  111. Moonkoo K, Mahlon CK, Yaorong Q (2006) Molecular and stable carbon isotopic characterization of PAH contaminants at McMurdo Station, Antarctica. Marine Poll Bull 52:1585–1590Google Scholar
  112. Morley MC, Yamamoto H, Speitel GE, Clausen J (2006) Dissolution kinetics of high explosives particles in a saturated sandy soil. J Contam Hydrol 85:141–158Google Scholar
  113. Morrill PL, Lacrampe-Couloume G, Slater GF, Sleep BE, Edwards EA, McMaster ML, Major DW, Sherwood Lollar B (2005) Quantifying chlorinated ethene degradation during reductive dechlorination at Kelly AFB using stable carbon isotopes. J Contam Hydrol 76:279–293Google Scholar
  114. Naumova RP, Selivanovskaya SLU, Mingatina FA (1988) Possibilities for the deep bacterial destruction of 2,4,6-trinitrotoluene. Mikrobiologia 57:218–222Google Scholar
  115. Nejidat A, Kafka L, Tekoah Y, Ronen Z (2008) Effect of organic and inorganic nitrogenous compounds on RDX degradation and cytochrome P-450 expression in Rhodococcus strain YH1. Biodegradation 19:313–320Google Scholar
  116. Neuwoehner J, Schofer A, Erlenkaemper B, Steinbach K, Hund-Rinke K, Eisentraeger A (2007) Toxicological characterization of 2,4,6-trinitrotoluene, its transformation products, and two nitramine explosives. Environ Toxicol Chem 26:1090–1099Google Scholar
  117. Nissenbaum A (1975) The distribution of natural stable isotopes of carbon as a possible tool for the differentiation of samples of TNT. J Forensic Sci 20:455–459Google Scholar
  118. Oh B-T, Sarath G, Shea PJ (2001) TNT nitroreductase from a Pseudomonas aeruginosa strain isolated from TNT-contaminated soil. Soil Biol Biochem 33:875–881Google Scholar
  119. Oh B-T, Shea PJ, Drijber RA, Vasilyeva GK, Sarath G (2003) TNT biotransformation and detoxification by a Pseudomonas aeruginosa strain. Biodegradation 14:309–319Google Scholar
  120. Pak JW, Knoke KL, Noguera DR, Fox BG, Chambliss GH (2000) Transformation of 2,4,6-trinitrotoluene by purified xenobiotic reductase B from Pseudomonas fluorescens I-C. Appl Environ Microbiol 66:4742–4750Google Scholar
  121. Park C, Kim T-H, Kim S, Kim S-W, Lee J, Kim S-H (2003) Optimization for biodegradation of 2,4,6-trinitrotoluene (TNT) by Pseudomonas putida. J Biosci Bioeng 95:567–571Google Scholar
  122. Pasti-Grigsby MB, Lewis TA, Crawford DL, Crawford RL (1996) Transformation of 2,4,6-trinitrotoluene (TNT) by Actinomycetes isolated from TNT-contaminated and uncontaminated environments. Appl Environ Microbiol 62:1120–1123Google Scholar
  123. Pavlostathis SG, Jackson GH (1999) Biotransformation of 2,4,6-trinitrotoluene in Anabaena sp cultures. Environ Toxicol Chem 18:412–419Google Scholar
  124. Pennington JC, Brannon JM (2002) Environmental fate of explosives. Thermochim Acta 384:163–172Google Scholar
  125. Pennington JC, Brannon JM, Gunnison D, Harrelson DW, Zakikhani M, Miyares P, Jenkins TF, Clarke J, Hayes C, Ringleberg D, Perkins E, Fredrickson H (2001) Monitored natural attenuation of explosives. Soil Sediment Contam 10:45–70Google Scholar
  126. Peterson FJ, Mason RP, Horspian J, Holtzman JL (1979) Oxygen-sensitive and insensitive nitroreduction by Escherichia coli and rat hepatic microcosomes. J Biol Chem 254:4009–4014Google Scholar
  127. Phillips SA, Doyle S, Philp L, Coleman M (2003) Proceedings: network developing forensic applications of stable isotope ratio mass spectrometry conference. Sci Justice 43:153–160Google Scholar
  128. Preuss A, Fimpel J, Dickert G (1993) Anaerobic transformation of 2,4,6-trinitrotoluene (TNT). Arch Microbiol 159:345–353Google Scholar
  129. Price CB, Brannon JM, Yost SL, Hayes CA (2001) Relationship between redox potential and pH on RDX transformation in soil–water slurries. J Environ Eng 127:26–31Google Scholar
  130. Pudge IB, Daugulis AJ, Dubois C (2003) The use of Enterobacter cloacae ATCC 43560 in the development of a two-phase partitioning bioreactor for the destruction of hexahydro-1,3,5-trinitro-1,3,5-s-triazine (RDX). J Biotechnol 100:65–75Google Scholar
  131. Regan KM, Crawford RL (1994) Characterization of Clostridium bifermentans and its biotransformation of 2,4,6-trinitrotoluene (TNT) and 1,3,5-triaza-1,3,5-trinitrocyclohexane (RDX). Biotechnol Lett 16:1081–1086Google Scholar
  132. Rieger P-G, Knackmuss HJ (1995) Basic knowledge and perspectives on biodegradation of 2,4,6-trinitrotoluene and related nitroaromatic compounds in contaminated soil. In: Spain JC (ed) Biodegradation of Nitroaromatic Compounds. Plenum Press, New York, pp 1–18Google Scholar
  133. Rieger P-G, Sinnwell V, Preuss A, Franke W, Knackmuss H-J (1999) Hydride-Meisenheimer complex formation and protonation as key reactions of 2,4,6-trinitrophenol biodegradation by Rhodococcus erythropolis. J Bacteriol 181:1189–1195Google Scholar
  134. Ringelberg DB, Reynolds CM, Walsh ME, Jenkins TF (2003) RDX loss in a surface soil under saturated and well drained conditions. J Environ Qual 32:1244–1249Google Scholar
  135. Roh H, Yu C, Fuller M, Chu K-H (2009) Identification of hexahydro-1,3,5-trinitro-1,3,5-triazine-degrading microorganisms via 15N-stable isotope probing. Environ Sci Technol 43:2505–2511Google Scholar
  136. Ronen Z, Brenner A, Abeliovich A (1998) Biodegradation of RDX-contaminated wastes in a nitrogen-deficient environment. Water Sci Technol 38:219–224Google Scholar
  137. Ronen Z, Yanovich Y, Goldin R, Adar E (2008) Metabolism of the explosive hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) in a contaminated vadose zone. Chemosphere 73:1492–1498Google Scholar
  138. Rylott EL, Jackson RG, Sabbadin F, Seth-Smith HMB, Edwards J, Chong CS, Strand SE, Grogan G, Bruce NC (2011) The explosive-degrading cytochrome P450 XplA: biochemistry, structural features and prospects for bioremediation. Biochim Biophys Acta 1:230–236Google Scholar
  139. Sagi-Ben Moshe S (2011) Biodegradation and transport of explosives in sandy unsaturated zone. PhD Thesis, The Hebrew University of Jerusalem, pp 119Google Scholar
  140. Sagi-Ben Moshe S, Ronen Z, Dahan O, Weisbrod N, Groisman L, Adar E, Nativ R (2009) Sequential biodegradation of TNT, RDX and HMX in a mixture. Environ Pollut 157:2231–2238Google Scholar
  141. Sagi-Ben Moshe S, Ronen Z, Dahan O, Bernstein A, Weisbrod N, Gelman F, Adar E (2010) Isotopic evidence and quantification assessment of in situ RDX biodegradation in the deep unsaturated zone. Soil Biol Biochem 42:1253–1262Google Scholar
  142. Schmidt TC, Zwank L, Elsner M, Berg M, Meckenstock RU, Haderlein SB (2004) Compound-specific stable isotope analysis of organic contaminants in natural environments: a critical review of the state of the art, prospects, and future challenges. Anal Bioanal Chem 378:283–300Google Scholar
  143. Seth-Smith HMB, Rosser SJ, Basran A, Travis ER, Dabbs ER, Nicklin S, Bruce NC (2002) Cloning, sequencing, and characterization of the hexahydro-1,3,5-trinitro-1,3,5-triazine degradation gene cluster from Rhodococcus rhodochrous. Appl Environ Microbiol 68:4764–4771Google Scholar
  144. Seth-Smith HMB, Edwards J, Rosser SJ, Rathbone DA, Bruce NC (2008) The explosive-degrading cytochrome P450 system is highly conserved among strains of Rhodococcus spp. Appl Environ Microbiol 74:4550–4552Google Scholar
  145. Sherburne LA, Shrout JD, Alvarez PJJ (2005) Hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) degradation by Acetobacterium paludosum. Biodegradation 16:539–547Google Scholar
  146. Sheremata TW, Hawari J (2000) Mineralization of RDX by the white rot fungus Phanerochaete chrysosporium to carbon dioxide and nitrous oxide. Environ Sci Technol 34:3384–3388Google Scholar
  147. Singh R, Soni P, Kumar P, Purohit S, Singh A (2009) Biodegradation of high explosive production effluent containing RDX and HMX by denitrifying bacteria. World J Microbiol Biotechnol 25:269–275Google Scholar
  148. Soojhawon I, Lokhande PD, Kodam KM, Gawai KR (2005) Biotransformation of nitroaromatics and their effects on mixed function oxidase system. Enzyme Microb Technol 37:527–533Google Scholar
  149. Spanggord RJ, Mabey WR, Chuo T, Haynes DL, Alferness PL, Tee DS, Mill T (1982) Environmental fate studies of HMX. Phase 1, screening studies, final report. SRI International, Menlo Park, CAGoogle Scholar
  150. Speitel G, Engels T, McKinney D (2001) Biodegradation of RDX in unsaturated soil. Bioremediation J 5:1–11Google Scholar
  151. Spence MJ, Bottrell SH, Thornton SF, Richnow HH, Spence KH (2005) Hydrochemical and isotopic effects associated with petroleum fuel biodegradation pathways in a chalk aquifer. J Contam Hydrol 79:67–88Google Scholar
  152. Spiker JK, Crawford DL, Crawford RL (1992) Influence of 2,4,6-trinitrotoluene (TNT) concentration on the degradation of TNT in explosive-contaminated soils by the white rot fungus Phanerochaete chrysosporium. Appl Environ Microbiol 58:3199–3202Google Scholar
  153. Stenuit B, Eyers L, El Fantroussi S, Agathos SN (2005) Promising strategies for the mineralisation of 2,4,6-trinitrotoluene. Rev Environ Sci Biotechnol 4:39–60Google Scholar
  154. Stenuit B, Eyers L, Rozenberg R, Habib-Jiwan J-L, Agathos SN (2006) Aerobic growth of Escherichia coli with 2,4,6-trinitrotoluene (TNT) as the sole nitrogen source and evidence of TNT denitration by whole cells and cell-free extracts. Appl Environ Microbiol 72:7945–7948Google Scholar
  155. Stenuit B, Eyers L, Rozenberg R, Habib-Jiwan J-L, Matthijs S, Cornelis P, Agathos SN (2009) Denitration of 2,4,6-trinitrotoluene in aqueous solutions using small-molecular-weight catalyst(s) secreted by Pseudomonas aeruginosa ESA-5. Environ Sci Technol 43:2011–2017Google Scholar
  156. Steuckart C, Berger-Prelss E, Levsen K (1994) Determination of explosives and their biodegradation products in contaminated soil and water from former ammunition plants by automated multiple development high-performance thin-layer chromatography. Anal Chem 66:2570–2577Google Scholar
  157. Tekoah Y, Abeliovich A, Nejidat A (1999) Participation of cytochrome P450 in the biodegradation of RDX by a Rhodococcus strain. In: 2nd international symposium, biodegradation of nitroaromatic compounds and explosives, Leesburg, VA, pp 7Google Scholar
  158. Thompson KT, Crocker FH, Fredrickson HL (2005) Mineralization of the cyclic nitramine explosive hexahydro-1,3,5-trinitro-1,3,5-triazine by Gordonia and Williamsia spp. Appl Environ Microbiol 71:8265–8272Google Scholar
  159. Uchimiya M, Gorb L, Isayev O, Qasim MM, Leszczynski J (2010) One-electron standard reduction potentials of nitroaromatic and cyclic nitramine explosives. Environ Pollut 158:3048–3053Google Scholar
  160. US EPA (2006) 2006 Edition of the Drinking Water Standards and Health Advisories. Office of Water, EPA 822-R-06-013, Washington, DCGoogle Scholar
  161. Van Aken B, Yoon JM, Schnoor JL (2004) Biodegradation of nitro-substituted explosives 2,4,6-trinitrotoluene, hexahydro-1,3,5-trinitro-1,3,5-triazine, and octahydro-1,3,5, 7-tetranitro-1,3,5-tetrazocine by a phytosymbiotic Methylobacterium sp. associated with poplar tissues (Populus deltoides x nigra DN34). Appl Environ Microbiol 70:508–517Google Scholar
  162. Van Dillewijn P, Caballero A, Paz JA, González-Pérez MM, Oliva JM, Ramos JL (2007) Bioremediation of 2,4,6-trinitrotoluene under field conditions. Environ Sci Technol 41:1378–1383Google Scholar
  163. Van Dillewijn P, Wittich R-M, Caballero A, Ramos J-L (2008) Type II hydride transferases from different microorganisms yield nitrite and diarylamines from polynitroaromatic compounds. Appl Environ Microbiol 74:6820–6823Google Scholar
  164. Vanderberg LA, Perry JJ, Unkefer PJ (1995) Catabolism of 2,4,6-trinitrotoluene by Mycobacterium vaccae. Appl Microbiol Biotechnol 43:937–945Google Scholar
  165. Vorbeck C, Lenke H, Fischer P, Knackmuss H-J (1994) Identification of a hydride-Meisenheimer complex as a metabolite of 2,4,6-trinitrotoluene by a Mycobacterium strain. J Bacteriol 176:932–934Google Scholar
  166. Vorbeck C, Lenke H, Fischer P, Spain JC, Knackmuss H-J (1998) Initial reductive reactions in aerobic microbial metabolism of 2,4,6-trinitrotoluene. Appl Environ Microbiol 64:246–252Google Scholar
  167. Waisner S, Hansen L, Fredrickson H, Nestler C, Zappi M, Banerji S, Bajpai R (2002) Biodegradation of RDX within soil-water slurries using a combination of differing redox incubation conditions. J Hazard Mater B95:91–106Google Scholar
  168. Wani AH, Davis JL (2003) RDX biodegradation column study: influence of ubiquitous electron acceptors on anaerobic biotransformation of RDX. J Chem Technol Biotechnol 78:1082–1092Google Scholar
  169. Williams RE, Rathbone DA, Scrutton NS, Bruce NC (2004) Biotransformation of explosives by the old yellow enzyme family of flavoproteins. Appl Environ Microbiol 70:3566–3574Google Scholar
  170. Wilson RD, Thornton SF, Mackay DM (2004) Challenges in monitoring the natural attenuation of spatially variable plumes. Biodegradation 15:359–369Google Scholar
  171. Wingfors H, Edlund C, Hägglund L, Waleij A, Sjöström J, Karlsson R-M, Leffler P, Qvarfort U, Ahlberg M, Thiboutot S, Ampelman G, Martel R, Duvalois W, Creemers A, Van Ham N (2006) Evaluation of the Contamination by Explosives and Metals in Soils at the Älvdalen Shooting Range. Part II: Results and Discussion. NBC Defence Scientific report, FOI-R-1877-SEGoogle Scholar
  172. Wittich R-M, Haïdour A, Van Dillewijn P, Ramos J-L (2008) OYE flavoprotein reductases initiate the condensation of TNT-derived intermediates to secondary diarylamines and nitrite. Environ Sci Technol 42:734–739Google Scholar
  173. Wittich R-M, Ramos J-L, Van Dillewijn P (2009) Microorganisms and explosives: mechanisms of nitrogen release from TNT for use as an N-source for growth. Environ Sci Technol 43:2773–2776Google Scholar
  174. Won WD, Heckly RJ, Glover DJ, Hoffsommer JC (1974) Metabolic disposition of 2,4,6-trinitrotoluene. Appl Microbiol 27:513–516Google Scholar
  175. Yinon J (1990) Toxicity and metabolism of explosives. CRC Press Inc., Boca Raton, FLGoogle Scholar
  176. Yinon J, Zitrin S (1993) Modern methods and applications in analysis of explosives. Wiley, ChichesterGoogle Scholar
  177. 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
  178. 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
  179. Zhang B, Kendall RJ, Anderson TA (2006) Toxicity of the explosive metabolites hexahydro-1,3,5-trinitroso-1,3,5-triazine (TNX) and hexahydro-1-nitroso-3,5-dinitro-1,3,5-triazine (MNX) to the earthworm Eisenia fetida. Chemosphere 64:86–95Google Scholar
  180. Zhao J-S, Halasz A, Paquet L, Beaulieu C, Hawari J (2002) Biodegradation of hexahydro-1,3,5-trinitro-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
  181. Zhao J-S, Paquet L, Halasz A, Hawari J (2003a) Metabolism of hexahydro-1,3-5-trinitro-1,3,5-triazine through initial reduction to hexahydro-1-nitroso-3, 5-dinitro-1,3,5-triazine followed by denitration in Clostridium bifermentans HAW-1. Appl Microbiol Biotechnol 63:187–193Google Scholar
  182. Zhao J-S, Spain J, Hawari J (2003b) Phylogenetic and metabolic diversity of hexahydro-1,3,5-trintitro-1,3,5-triazine (RDX) transforming bacteria in strictly anaerobic mixed cultures enriched on RDX as nitrogen source. FEMS Microbiol Ecol 46:189–196Google Scholar
  183. Zhao J-S, Paquet L, Halasz A, Manno D, Hawari J (2004a) Metabolism of octahydro-1,3,5,7-tetranitro-1,3,5,7-tetrazocine by Clostridium bifermentans strain HAW-1 and several other H2-producing fermentative anaerobic bacteria. FEMS Microbiol Lett 237:65–72Google Scholar
  184. Zhao J-S, Spain J, Thiboutot S, Ampleman G, Greer C, Hawari J (2004b) Phylogeny of cyclic nitramine-degrading psychrophilic bacteria in marine sediment and their potential role in the natural attenuation of explosives. FEMS Microbiol Ecol 49:349–357Google Scholar
  185. Zhao J-S, Manno D, Beaulieu C, Paquet L, Hawari J (2005) Shewanella sediminis sp. nov., a novel Na+-requiring and hexahydro-1,3,5-trinitro-1,3,5-triazine-degrading bacterium from marine sediment. Intl J Syst Evol Microbiol 55:1511–1520Google Scholar
  186. Zhao J-S, Manno D, Leggiadro C, O’Neil D, Hawari J (2006) Shewanella halifaxensis sp nov., a novel obligately respiratory and denitrifying psychrophile. Intl J Syst Evol Microbiol 56:205–212Google Scholar
  187. Zhao J-S, Manno D, Hawari J (2007) Abundance and diversityofoctahydro-1,3,5,7-tetranitro-1,3,5,7-tetrazocine (HMX)-metabolizing bacteria in UXO-contaminated marine sediments. FEMS Microbiol Ecol 59:706–717Google Scholar
  188. Zhao J-S, Den Y, Manno D, Hawari J (2010) Shewanella spp. genomic evolution for a cold marine lifestyle and in situ explosive biodegradation. PLoS One 5:e9109Google Scholar
  189. Ziganshin AM, Gerlach R, Borch T, Naumov AV, Naumova RP (2007) Production of eight different hydride complexes and nitrite release from 2,4,6-trinitrotoluene by Yarrowia lipolytica. Appl Environ Microbiol 73:7898–7905Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg  2012

Authors and Affiliations

  1. 1.Department of Environmental Hydrology and MicrobiologyZuckerberg Institute for Water Research, Blaustein Institutes for Desert Research, Ben-Gurion University of the NegevSede BoqerIsrael

Personalised recommendations