Abstract
2,4,6-trinitrotoluene (TNT) is known to be one of the most common military explosives. In spite of its established toxicity and mutagenicity for many organisms, soils and groundwater are still being frequently contaminated at manufacturing, disposal and TNT destruction sites. The inability of natural aquatic and soil biota to use TNT as growth substrate has been recognized as the primary limitation in the application of bioremediation processes to contaminated environments. However, promising degradation pathways have been recently discovered which may lead to the mineralisation of TNT. Significant advances have been made in studying the mechanism of TNT denitration, which can be considered as the major reaction and the driving force towards beneficial biodegradation. The possibilities to favour TNT denitration are discussed based on current knowledge of the enzymology and genetics of denitration in nitroaromatic degrading organisms. The literature survey demonstrates that the only enzymes characterized so far for their denitrase activity towards TNT belong to the class I flavin-dependent β/α barrel oxidoreductases, also known as the “Old Yellow Enzyme” family. In addition, this review provides an overview of strategies and future directions towards a rational search for new catabolic activities, including metagenomic library screening, plus new possibilities to improve the activity of known catabolic enzymes acting on TNT, such as DNA shuffling.
Similar content being viewed by others
References
M-A Abril C. Michan KN Timmis JL Ramos (1989) ArticleTitleRegulator and enzyme specificities of the TOL plasmid-encoded upper pathway for degradation of aromatic hydrocarbons and expansion of the substrate range of the pathway Appl. Environ. Microbiol. 171 6782–6790
M Altamirano L Garcia-Villada M Agrelo L Sanchez-Martin L Martin-Otero A Flores-Moya M Rico V Lopez-Rodas E Costas (2004) ArticleTitleA novel approach to improve specificity of algal biosensors using wild-type and resistant mutants: An application to detect TNT Biosens. Bioelec. 19 1319–1323 Occurrence Handle10.1016/j.bios.2003.11.001
K Ask N Decologne N Asare JA Holme Y Artur H Pelczar P Camus (2004) ArticleTitleDistribution of nitroreductive activity toward nilutamide in rat Toxicol. Appl. Pharmacol. 201 1–9 Occurrence Handle10.1016/j.taap.2004.04.006 Occurrence Handle15519603
S Ayer RJ Andersen H Cun-Heng J Clardy (1984) ArticleTitlePhidolopin, a new purine derivative from the bryozoan Phidolopora pacifica J. Org. Chem. 49 3869–3870 Occurrence Handle10.1021/jo00194a053
T Barna HL Messiha C Petosa NC Bruce NS Scrutton PCE Moody (2002) ArticleTitleCrystal structure of bacterial morphinone reductase and properties of the C191A mutant enzyme J. Biol. Chem. 277 30976–30983 Occurrence Handle10.1074/jbc.M202846200 Occurrence Handle12048188
A Basran RJ Harris MJ Sutcliffe NS Scrutton (2003) ArticleTitle H-tunneling in the multiple H-transfers of the catalytic cycle of morphinone reductase and in the reductive half-reduction of the homologous pentaerythritol tetranitrate reductase J. Biol. Chem. 278 43973–43982 Occurrence Handle10.1074/jbc.M305983200 Occurrence Handle12941965
C Behrend K Heesche-Wagner (1999) ArticleTitleFormation of hydride-Meisenheimer complexes of picric acid (2,4,6-trinitrophenol) and 2,4-dinitrophenol during mineralization of picric acid by Nocardioides sp. strain CB 22–2 Appl. Environ. Microbiol. 65 1372–1377 Occurrence Handle10103224
JEM Beurskens CGC Dekker H Heuvel Particlevan den M Swart J Wolf Particlede (1994) ArticleTitleDechlorination of chlorinated benzenes by an anaerobic microbial consortium that selectively mediates the thermodynamic most favorable reactions Environ. Sci. Technol. 28 701–706 Occurrence Handle10.1021/es00053a026
PR Binks CE French S Nicklin NC Bruce (1996) ArticleTitleDegradation of pentaerythritol tetranitrate by Enterobacter cloacae PB2 Appl. Environ. Microbiol. 62 1214–1219 Occurrence Handle8919782
DS Blehert BG Fox GH Chambliss (1999) ArticleTitleCloning and sequence analysis of two Pseudomonas flavoprotein xenobiotic reductases J. Bacteriol. 181 6254–6263 Occurrence Handle10515912
DS Blehert KL Knoke BG Fox GH Chambliss (1997) ArticleTitleRegioselectivity of nitroglycerin denitration by flavoprotein nitroester reductases purified from two Pseudomonas species J. Bacteriol. 179 6912–6920 Occurrence Handle9371434
N Boon J Goris P Vos ParticleDe W Verstraete EM Top (2001) ArticleTitleGenetic diversity among 3-chloroaniline- and aniline-degrading strains of the Comamonadaceae Appl. Environ. Microbiol. 67 1107–1115 Occurrence Handle10.1128/AEM.67.3.1107-1115.2001 Occurrence Handle11229899
R Boopathy CF Kulpa (1992) ArticleTitleTrinitrotoluene (TNT) as a sole nitrogen source for a sulfate-reducing bacterium Desulfovibrio sp. (B strain) isolated from an anaerobic digester Curr. Microbiol. 25 235–241 Occurrence Handle10.1007/BF01570724 Occurrence Handle1368976
T Borch R Gerlach (2004) ArticleTitleUse of reversed-phase high-performance liquid chromatography-diode array detection for complete separation of 2,4,6-trinitrotoluene metabolites and EPA Method 8330 explosives: influence of temperature and an ion-pair reagent J. Chrom. A 1022 83–94 Occurrence Handle10.1016/j.chroma.2003.09.067
ABA Boxall CJ Sinclair K Fenner D Kolpin SJ Maund (2004) ArticleTitleWhen synthetic chemicals degrade in the environment Environ. Sci. Technol. 38 368A–375A Occurrence Handle15506178
IA Buryakov (2004) ArticleTitleExpress analysis of explosives, chemical warfare agents and drugs with multicapillary column gas chromatography and ion mobility increment spectrometry J. Chrom. B 800 75–82 Occurrence Handle10.1016/j.jchromb.2003.10.064
A Caballero A Esteve-Nuñez GJ Zylstra JL Ramos (2005) ArticleTitleAssimilation of nitrogen from nitrite and trinitrotoluene in Pseudomonas putida JLR11 J. Bacteriol. 187 396–399 Occurrence Handle10.1128/JB.187.1.396-399.2005 Occurrence Handle15601726
PT Charles LC Shriver-Lake SC Francesconi AM Churilla JG Rangasammy JCH Patterson JR Deschamps AW Kusterbeck (2004) ArticleTitleCharacterization and performance evaluation of in vivo and in vitro produced monoclonal anti-TNT antibodies for the detection of TNT J. Immunol. Methods 284 15–26 Occurrence Handle10.1016/j.jim.2003.09.010 Occurrence Handle14736413
PC Cirino FH Arnold (2002) ArticleTitleProtein engineering of oxygenases for biocatalysis Curr. Op. Chem. Biol. 6 130–135 Occurrence Handle10.1016/S1367-5931(02)00305-8
JM Conder TW La Point AT Bowen (2004) ArticleTitlePreliminary kinetics and metabolism of 2,4,6-trinitrotoluene and its reduced metabolites in an aquatic oligochaete Aquatic Toxicol. 69 199–213 Occurrence Handle10.1016/j.aquatox.2004.04.013
A Crameri S-A Raillard E Bermudez WPC Stemmer (1998) ArticleTitleDNA shuffling of a family of genes from diverse species accelerates directed evolution Nature 391 288–291 Occurrence Handle10.1038/34663 Occurrence Handle9440693
RL Crawford (1995) ArticleTitleThe microbiology and treatment of nitroaromatic compounds Curr. Op. Biotechnol. 6 329–336 Occurrence Handle10.1016/0958-1669(95)80055-7
M Dai SD Copley (2004) ArticleTitleGenome shuffling improves degradation of the anthropogenic pesticide pentachlorophenol by Sphingobium chlorophenolicum ATCC 39723 Appl. Environ. Microbiol. 70 2391–2397 Occurrence Handle10.1128/AEM.70.4.2391-2397.2004 Occurrence Handle15066836
G Daun H Lenke M Reuss H-J Knackmuss (1998) ArticleTitleBiological treatment of TNT-contaminated soil. 1. Anaerobic cometabolic reduction and interaction of TNT and metabolites with soil components Environ. Sci. Technol. 32 1956–1963 Occurrence Handle10.1021/es970949u
JK Davis GC Paoli Z He LJ Nadeau CC Somerville JC Spain (2000) ArticleTitleSequence analysis and initial characterization of two isozymes of hydroxylaminobenzene mutase from Pseudomonas pseudoalcaligenes JS45 Appl. Environ. Microbiol. 66 2965–2971 Occurrence Handle10.1128/AEM.66.7.2965-2971.2000 Occurrence Handle10877793
TL Davis (1943) The Chemistry of Powder and Explosives John Wiley & Sons, Inc. New York
SG Dodard J Powlowski GI Sunahara (2004) ArticleTitleBiotransformation of 2,4,6-trinitrotoluene (TNT) by enchytraeids (Enchytraeus albidus) in vivo and in vitro Environ. Poll. 131 263–273 Occurrence Handle10.1016/j.envpol.2004.02.018
B Donlon E Razo-Flores JA Field G Lettinga (1995) ArticleTitleToxicity of N-substitued aromatics to acetoclastic methanogenic activity in granular sludge Appl. Environ. Microbiol. 61 3889–3893 Occurrence Handle8526501
M Dua A Singh N Sethunathan AK Johri (2002) ArticleTitleBiotechnology and bioremediation: successes and limitations Appl. Microbiol. Biotechnol. 59 143–152 Occurrence Handle10.1007/s00253-002-1024-6 Occurrence Handle12111139
E Duque A Haidour F Godoy JL Ramos (1993) ArticleTitleConstruction of a Pseudomonas hybrid strain that mineralizes 2,4,6-trinitrotoluene J. Bacteriol. 175 2278–2283 Occurrence Handle8468288
S Ebert P-G Rieger H-J Knackmuss (1999) ArticleTitleFunction of coenzyme F420 in aerobic catabolism of 2,4,6-trinitrophenol and 2,4-dinitrophenol by Nocardioides simplex FJ2–1A J. Bacteriol. 181 2669–2674
S El Fantroussi H Naveau SN Agathos (1998) ArticleTitleAnaerobic dechlorinating bacteria Biotechnol. Progr. 14 167–188 Occurrence Handle10.1021/bp980011k
J Eriksson S Krankki A Shchukarev U Skyllberg (2004) ArticleTitleBinding of 2,4,6-trinitrotoluene, aniline, and nitrobenzene to dissolved and particulate soil organic matter Environ. Sci. Technol. 38 3074–3080 Occurrence Handle10.1021/es035015m Occurrence Handle15224738
J Eriksson U Skyllberg (2001) ArticleTitleBinding of 2,4,6-trinitrotoluene and its degradation products in a soil organic matter two-phase system J. Environ. Qual. 30 2053–2061 Occurrence Handle11790013
A Esteve-Nuñez A Caballero JL Ramos (2001) ArticleTitleBiological degradation of 2,4,6-trinitrotoluene Microbiol. Mol. Biol. Rev. 65 335–352 Occurrence Handle10.1128/MMBR.65.3.335-352.2001 Occurrence Handle11527999
A Esteve-Nuñez G Lucchesi B Philipp B Schink JL Ramos (2000) ArticleTitleRespiration of 2,4,6-trinitrotoluene by Pseudomonas sp. strain JLR11 J. Bacteriol. 182 1352–1355 Occurrence Handle10.1128/JB.182.5.1352-1355.2000 Occurrence Handle10671458
A Esteve-Nuñez JL Ramos (1998) ArticleTitleMetabolism of 2,4,6-trinitrotoluene by Pseudomonas sp JLR11 Environ. Sci. Technol. 32 3802–3808 Occurrence Handle10.1021/es9803308
L Eyers I George L Schuler B Stenuit SN Agathos S El Fantroussi (2004a) ArticleTitleEnvironmental genomics: exploring the unmined richness of microbes to degrade xenobiotics Appl. Biochem. Microbiol. 66 123–130 Occurrence Handle10.1007/s00253-004-1703-6
Eyers L, Stenuit B, El Fantroussi S & Agathos SN (2004b) Microbial characterization of TNT-contaminated soils and anerobic TNT degradation: high and unusual denitration activity, W. Verstraete, Proceedings of the European Symposium on Environmental Biotechnology, ESEB 2004 (pp 51–54), Taylor and Francis Group plc, London, UK.
P Fauser M Thomsen (2002) ArticleTitleSensitivity analysis of calculated exposure concentrations and dissipation of DEHP in a topsoil compartment: the influence of the third phase effect and dissolved organic matter (DOM) Sci. Total Environ. 296 89–103 Occurrence Handle10.1016/S0048-9697(02)00053-0 Occurrence Handle12398329
S Fetzner (1998) ArticleTitleBacterial dehalogenation Appl. Microbiol. Biotechnol. 50 633–657 Occurrence Handle10.1007/s002530051346 Occurrence Handle9891928
PD Fiorella JC Spain (1997) ArticleTitleTransformation of 2,4,6-trinitrotoluene by Pseudomonas pseudoalcaligenes JS52 Appl. Environ. Microbiol. 63 2007–2015
TB Fitzpatrick S Auweter K Kitzing T Clausen N Amrhein P Macheroux (2004) ArticleTitleStructural and functional impairment of an Old Yellow Enzyme homologue upon affinity tag incorporation Prot. Exp. Purif. 36 280–291 Occurrence Handle10.1016/j.pep.2004.04.012
CE French S Nicklin NC Bruce (1998) ArticleTitleAerobic degradation of 2,4,6-trinitrotoluene by Enterobacter cloacae PB2 and by pentaerythritol tetranitrate reductase Appl. Environ. Microbiol. 64 2864–2868 Occurrence Handle9687442
ME Fuller JF Manning (1997) ArticleTitleAerobic Gram-positive and Gram-negative bacteria exhibit differential sensitivity to and transformation of 2,4,6-trinitrotoluene (TNT) Curr. Microbiol. 35 77–83 Occurrence Handle10.1007/s002849900216 Occurrence Handle9216880
ME Fuller JF Manning (2004) ArticleTitleMicrobiological changes during bioremediation of explosives-contaminated soils in laboratory and pilot-scale bioslurry reactors Bioresource Technol. 91 123–133 Occurrence Handle10.1016/S0960-8524(03)00180-9
SB Funk DJ Roberts DL Crawford RL Crawford (1993) ArticleTitleInitial-phase optimization for bioremediation of munition compound-contaminated soils Appl. Environ. Microbiol. 59 2171–2177 Occurrence Handle8357251
PC Gilcrease VG Murphy (1995) ArticleTitleBioconversion of 2,4-diamino-6-nitrotoluene to a novel metabolite under anoxic and aerobic conditions Appl. Environ. Microbiol. 61 4209–4214 Occurrence Handle8534088
N Gilles (2004) ArticleTitleGreen explosives: collateral damage Nature 427 580–581 Occurrence Handle10.1038/427580a Occurrence Handle14961090
S Goux N Shapir S El Fantroussi S Lelong SN Agathos L Pussemier (2003) ArticleTitleLong-term maintenance of rapid atrazine degradation in soils inoculated with atrazine degraders Water, Air Soil Pollut. Focus 3 131–142
J-P Grivet A-M Delort J-C Portais (2003) ArticleTitleNMR and microbiology: from physiology to metabolomics Biochimie 85 823–840 Occurrence Handle10.1016/j.biochi.2003.08.004 Occurrence Handle14652172
PE Groenewegen P Breeuwer JM Helvoort Particlevan AA Langenhoff FP Vries Particlede JA Bont Particlede (1992) ArticleTitleNovel degradative pathway of 4-nitrobenzoate in Comamonas acidovorans NBA-10 J. Gen. Microbiol. 138 1599–1605 Occurrence Handle1527502
A Haïdour JL Ramos (1996) ArticleTitleIdentification 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 2365–2370 Occurrence Handle10.1021/es950824u
BE Haigler JC Spain (1993) ArticleTitleBiodegradation of 4-nitrotoluene by Pseudomonas sp. strain 4NT Appl. Environ. Microbiol. 59 2239–2243 Occurrence Handle8357257
BE Haigler WC Suen JC Spain (1996) ArticleTitlePurification and sequende analysis of 4-methyl-5-nitrocatechol oxygenase from Burkholderia sp. strain DNT J. Bacteriol. 178 6019–6024 Occurrence Handle8830701
BE Haigler WH Wallace JC Spain (1994) ArticleTitleBiodegradation of 2-nitrotoluene by Pseudomonas sp. strain JS42 Appl. Environ. Microbiol. 60 3466–3469 Occurrence Handle7944378
M Hashimoto K Hattori (1966) ArticleTitleOxypyrrolnitrin: a metabolite of Pseudomonas Chem. Pharm. Bull. 14 1314–1316 Occurrence Handle5979179
J Hawari S Beaudet A Halasz S Thiboutot G Ampleman (2000) ArticleTitleMicrobial degradation of explosives: biotransformation versus mineralization Appl. Microbiol. Biotechnol. 54 605–618 Occurrence Handle10.1007/s002530000445 Occurrence Handle11131384
J Hawari A Halasz L Paquet B Spencer G Ampleman S Thiboutot (1998) ArticleTitleCharacterization of metabolites in the biotransformation of 2,4,6-trinitrotoluene with anaerobic sludge: role of triaminotoluene Appl. Environ. Microbiol. 64 2200–2206 Occurrence Handle9603835
J He C Hertweck (2003) ArticleTitleIteration as programmed event during polyketide assembly; molecular analysis of the aureothin biosynthesis gene cluster Chem. Biol. 10 1225–1232 Occurrence Handle10.1016/j.chembiol.2003.11.009 Occurrence Handle14700630
Z He JC Spain (1997) ArticleTitleStudies of the catabolic pathway of degradation of nitrobenzene by Pseudomonas pseudoalcaligenes JS45: removal of the amino group from 2-aminomuconic semialdehyde Appl. Environ. Microbiol. 63 4839–4843 Occurrence Handle9471964
G Heiss KW Hofmann N Trachtmann DM Walters P Rouvière H-J Knackmuss (2002) ArticleTitlenpd gene functions of Rhodococcus (opacus) erythropolis HL PM-1 in the initial steps of 2,4,6-trinitrophenol degradation Microbiology 148 799–806 Occurrence Handle11882715
G Heiss H-J Knackmuss (2002) ArticleTitleBioelimination of nitroaromatic compounds: immobilization versus mineralization Curr. Op. Biotechnol. 5 282–287
G Heiss N Trachtmann Y Abe M Takeo H-J Knackmuss (2003) ArticleTitleHomologous npdGI genes in 2,4-dinitrophenol- and 4-nitrophenol-degrading Rhodococcus spp Appl. Environ. Microbiol. 69 2748–2754 Occurrence Handle10.1128/AEM.69.5.2748-2754.2003 Occurrence Handle12732545
KW Hofmann H-J Knackmuss G Heiss (2004) ArticleTitleNitrite elimination and hydrolytic ring cleavage in 2,4,6-trinitrophenol (picric acid) degradation Appl. Environ. Microbiol. 70 2854–2860 Occurrence Handle10.1128/AEM.70.5.2854-2860.2004 Occurrence Handle15128543
J-S Hsu Y-B Yang C-H Deng C-L Wei S-H Liaw Y-C Tsai (2004) ArticleTitleFamily shuffling of expandase genes to enhance substrate specificity for penicillin G Appl. Environ. Microbiol. 70 6257–6263 Occurrence Handle10.1128/AEM.70.10.6257-6263.2004 Occurrence Handle15466573
S Huang PA Lindahl C Wang GN Bennett FB Rudolph JB Hughes (2000) ArticleTitle2,4,6-trinitrotoluene reduction by carbon monoxide dehydrogenase from Clostridium thermoaceticum Appl. Environ. Microbiol. 66 1474–1478 Occurrence Handle10.1128/AEM.66.4.1474-1478.2000 Occurrence Handle10742229
JB Hughes C Wang K Yesland A Richardson R Bhadra G Bennett F Rudolph (1998) ArticleTitleBamberger rearrangement during TNT metabolism by Clostridium acetobutylicum Environ. Sci. Technol. 32 494–500 Occurrence Handle10.1021/es970612s
RK Jain JH Dreisbach JC Spain (1994) ArticleTitleBiodegradation of p-nitrophenol via 1,2,4-benzenetriol by an Arthrobacter sp Appl. Environ. Microbiol. 60 3030–3032 Occurrence Handle8085840
JM Joern P Meinhold FH Arnold (2002) ArticleTitleAnalysis of shuffled gene libraries J. Mol. Biol. 316 643–656 Occurrence Handle10.1006/jmbi.2001.5349 Occurrence Handle11866523
GR Johnson RK Jain JC Spain (2002) ArticleTitleOrigins of the 2,4-dinitrotoluene pathway J. Bacteriol. 184 4219–4232 Occurrence Handle10.1128/JB.184.15.4219-4232.2002 Occurrence Handle12107140
GR Johnson BF Smets JC Spain (2001) ArticleTitleOxidative transformation of aminodinitrotoluene isomers by multicomponent dioxygenases Appl. Environ. Microbiol. 67 5460–5466 Occurrence Handle10.1128/AEM.67.12.5460-5466.2001 Occurrence Handle11722893
GR Johnson JC Spain (2003) ArticleTitleEvolution of catabolic pathways for synthetic compounds: bacterial pathways for degradation of 2,4-dinitrotoluene and nitrobenzene Appl. Microbiol. Biotechnol. 62 110–123 Occurrence Handle10.1007/s00253-003-1341-4 Occurrence Handle12750857
LR Johnson R Davenport H Balbach DJ Schaeffer (1994) ArticleTitlePhototoxicology 3. Comparative toxicity of trinitrotoluene and aminodinitrotoluenes to Daphnia magna, Dugesia dorotocephala, and sheep erythrocytes Ecotoxicol. Environ. Saf. 27 34–49 Occurrence Handle10.1006/eesa.1994.1005 Occurrence Handle7525203
CM Jung DA Newcombe DL Crawford RL Crawford (2004) ArticleTitleDetection and decontamination of residual energetics from ordnance and explosive scrap Biodegradation 15 41–48 Occurrence Handle10.1023/B:BIOD.0000009961.03463.a6 Occurrence Handle14971856
T Kalafut ME Wales VK Rastogi RP Naumova SK Zaripova JR Wild (1998) ArticleTitleBiotransformation patterns of 2,4,6-trinitrotoluene by aerobic bacteria Curr. Microbiol. 36 45–54 Occurrence Handle10.1007/s002849900278 Occurrence Handle9405746
DL Kaplan AM Kaplan (1982) ArticleTitleMutagenicity of 2,4,6-trinitrotoluene-surfactant complexes Bull. Environ. Contam. Toxicol. 28 33–38 Occurrence Handle10.1007/BF01608409 Occurrence Handle7039734
M Kataoka A Kotaka R Thiwthong M Wada S Nakamori S Shimizu (2004) ArticleTitleCloning and overexpression of the old yellow enzyme gene of Candida macedoniensis, and its application to the production of a chiral compound J. Biotechnol. 114 1–9 Occurrence Handle10.1016/j.jbiotec.2004.04.033 Occurrence Handle15464593
H Khan T Barna RJ Harris NC Bruce I Barsukov AW Munro PCE Moody NS Scrutton (2004) ArticleTitleAtomic resolution structures and solution behaviour of enzyme-substrate complexes of Enterobacter cloacae PB2 pentaerythritol tetranitrate reductase J. Biol. Chem. 279 30563–30572 Occurrence Handle10.1074/jbc.M403541200 Occurrence Handle15128738
H Khan RJ Harris T Barna DH Craig NC Bruce AW Munro PCE Moody NS Scrutton (2002) ArticleTitleKinetic and structural basis of reactivity of pentaerythritol tetranitrate reductase with NADPH, 2-cyclohexenone, nitroesters, and nitroaromatic explosives J. Biol. Chem. 277 21906–21912 Occurrence Handle10.1074/jbc.M200637200 Occurrence Handle11923299
M Kikuchi K Ohnishi S Harayama (2000) ArticleTitleAn effective family shuffling method using single-stranded DNA Gene 243 133–137 Occurrence Handle10.1016/S0378-1119(99)00547-8 Occurrence Handle10675621
H-Y Kim G Bennett H-G Song (2002) ArticleTitleDegradation of 2,4,6-trinitrotoluene by Klebsiella sp. isolated from activated sludge Biotechnol. Lett. 24 2023–2028 Occurrence Handle10.1023/A:1021127201608
J Kim K Sung MY Corapcioglu MC Drew (2004) ArticleTitleSolute transport and extraction by a single root in unsaturated soils: model development and experiment Environ. Poll. 131 61–70 Occurrence Handle10.1016/j.envpol.2004.02.026
J Klausen SP Tröber SB Haderlein RP Schwarzenbach (1995) ArticleTitleReduction of substituted nitrobenzenes by Fe(II) in aqueous mineral suspensions Environ. Sci. Technol. 29 2396–2404
H Knicker (2003) ArticleTitleIncorporation of 15N-TNT transformation products into humifying plant organic matter as revealed by one- and two-dimensional solid state NMR spectroscopy Sci. Tot. Environ. 308 211–220 Occurrence Handle10.1016/S0048-9697(02)00610-1
H Knicker C Achtnich H Lenke (2001) ArticleTitleSolid-state nitrogen-15 nuclear magnetic resonance analysis of biologically reduced 2,4,6-trinitrotoluene in a soil slurry remediation J. Environ. Qual. 30 403–410 Occurrence Handle11285900
RM Kohli V Massey (1998) ArticleTitleThe oxidative half-reaction of Old Yellow Enzyme. The role of tyrosine 196 J. Biol. Chem. 273 32763–32770 Occurrence Handle10.1074/jbc.273.49.32763 Occurrence Handle9830020
Y Kumagai M Kikushima Y Nakai N Shimojo M Kunimoto (2004) ArticleTitleNeuronal nitric oxide synthase (NNOS) catalyzes one-electron reduction of 2,4,6-trinitrotoluene, resulting in decreased nitric oxide production and increased nNOS gene expression: implication for oxidative stress Free Radical Biol. Med. 37 350–357 Occurrence Handle10.1016/j.freeradbiomed.2004.04.023
BM Kurinenko GY Yakovleva NA Denivarova YV Abreimova (2003) ArticleTitleSpecific toxic effects of 2,4,6-trinitrotoluene on Bacillus subtilis SK1 Appl. Biochem. Microbiol. 39 275–278 Occurrence Handle10.1023/A:1023527611310
JW Kury RD Breithaupt CM Tarver (1999) ArticleTitleDetonation waves in trinitrotoluene Shock Waves 9 227–237 Occurrence Handle10.1007/s001930050160
B Lachance AY Renoux M Sarrazin J Hawari GI Sunahara (2004) ArticleTitleToxicity and bioaccumulation of reduced TNT metabolites in the earthworm Eisenia andrei exposed to amended forest soil Chemosphere 55 1339–1348 Occurrence Handle10.1016/j.chemosphere.2003.11.049 Occurrence Handle15081777
H Lenke C Achtnich H-J Knackmuss (2000) Perspectives of bioelimination of polynitroaromatic compounds JC Spain JB Hughes H-J Knackmuss (Eds) Biodegradation of Nitroaromatic Compounds and Explosives Lewis Publishers New York 91–126
H Lenke H-J Knackmuss (1992) ArticleTitleInitial hydrogenation during catabolism of picric acid by Rhodococcus erythropolis HL 24–2 Appl. Environ. Microbiol. 58 2933–2937 Occurrence Handle1444408
H Lenke DH Pieper C Bruhn H-J Knackmuss (1992) ArticleTitleDegradation of 2,4-dinitrophenol by two Rhodococcus erythropolis strains, HL 24–1 and HL 24–2 Appl. Environ. Microbiol. 58 2928–2932 Occurrence Handle1444407
DJ Lessner GR Johnson RE Parales JC Spain DT Gibson (2002) ArticleTitleMolecular characterization and substrate specificity of nitrobenzene dioxygenase from Comamonas sp. strain JS765 Appl. Environ. Microbiol. 68 634–641 Occurrence Handle10.1128/AEM.68.2.634-641.2002 Occurrence Handle11823201
TA Lewis DA Newcombe RL Crawford (2004) ArticleTitleBioremediation of soils contaminated with explosives J. Environ. Manag. 70 291–307 Occurrence Handle10.1016/j.jenvman.2003.12.005
H Li BJ Teppen CT Johnston SA Boyd (2004) ArticleTitleThermodynamics of nitroaromatic compound adsorption from water by smectite clay Environ. Sci. Technol. 38 5433–5442 Occurrence Handle10.1021/es035054y Occurrence Handle15543748
FE Löffler JM Tiedje RA Sanford (1999) ArticleTitleFraction of electrons consumed in electron acceptor reduction and hydrogen thresholds as indicators of halorespiratory physiology Appl. Environ. Microbiol. 65 4049–4056 Occurrence Handle10473415
JC Lynch JM Brannon K Hatfield JJ Delfino (2003) ArticleTitleAn exploratory approach to modeling explosive compound persistence and flux using dissolution kinetics J. Cont. Hydrol. 66 147–159 Occurrence Handle10.1016/S0169-7722(03)00030-5
JL Martin SD Comfort PJ Shea TA Kokjohn RA Drijber (1997) ArticleTitleDenitration of 2,4,6-trinitrotoluene (TNT) by Pseudomonas savastanoi Can. J. Microbiol. 43 447–455 Occurrence Handle9198535
B Martinez J Tomkins LP Wackett R Wing MJ Sadowsky (2001) ArticleTitleComplete nucleotide sequence and organization of the atrazine catabolic plasmid pADP-1 from Pseudomonas sp. strain ADP J. Bacteriol. 183 5684–5697 Occurrence Handle10.1128/JB.183.19.5684-5697.2001 Occurrence Handle11544232
FD Marvin-Sikkema JAM Bont Particlede (1994) ArticleTitleDegradation of nitroaromatic compounds by microorganisms Appl. Microbiol. Biotechnol. 42 499–507 Occurrence Handle10.1007/s002530050285 Occurrence Handle7765729
Y Meah BJ Brown S Chakraborty V Massey (2001) ArticleTitleOld yellow enzyme: reduction of nitrate esters, glycerin trinitrate, and propylene 1,2-dinitrate Proc. Natl. Acad. Sci. USA 98 8560–8565 Occurrence Handle10.1073/pnas.151249098 Occurrence Handle11438708
AA Meharg GR Dennis JWG Caimey (1997) ArticleTitleBiotransformation of 2,4,6-trinitrotoluene (TNT) by ectomycorrhizal basidiomycetes Chemosphere 35 513–521 Occurrence Handle10.1016/S0045-6535(97)00116-1
K Miura Y Tomioka H Suzuki M Yonoezawa T Hishinuma M Mizugaki (1997) ArticleTitleMolecular cloning of the nemA gene encoding N-ethylmaleimide reductase from Escherichia coli Biol. Pharm. Bull. 20 110–112 Occurrence Handle9013822
L Nadeau J Spain (1995) ArticleTitleBacterial degradation of m-nitrobenzoic acid Appl. Environ. Microbiol. 61 840–843 Occurrence Handle7574625
RP Naumova SLU Selivanovskaya FA Mingatina (1988) ArticleTitlePossibilities for the deep bacterial destruction of 2,4,6-trinitrotoluene Mikrobiologiya 57 218–222
YS Niino S Chakraborty BJ Brown V Massey (1995) ArticleTitleA new old yellow enzyme of Saccharomyces cerevisiae J. Biol. Chem. 270 1983–1991 Occurrence Handle10.1074/jbc.270.5.1983 Occurrence Handle7836424
SF Nishino GC Paoli JC Spain (2000a) ArticleTitleAerobic degradation of dinitrotoluenes and pathway for bacterial degradation of 2,6-dinitrotoluene Appl. Environ. Microbiol. 66 2139–2147 Occurrence Handle10.1128/AEM.66.5.2139-2147.2000
SF Nishino JC Spain Z He (2000b) Strategies for aerobic degradation of nitroaromatic compounds by bacteria: process discovery to field application JC Spain JB Hughes H-J Knackmuss (Eds) Biodegradation of Nitroaromatic Compounds and Explosives Lewis Publishers New York 7–62
T Ohmori S Hagiwara A Ueda Y Minoda K Yamada (1978) ArticleTitleProduction of pyoluteorin and its derivatives from n-paraffin by Pseudomonas aeruginosa S10B2 Agric. Biol. Chem. 42 2031–2036
JW Pak KL Knoke DR Noguera BG Fox GH Chambliss (2000) ArticleTitleTransformation of 2,4,6-trinitrotoluene by purified xenobiotic reductase B from Pseudomonas fluorescens I-C Appl. Environ. Microbiol. 66 4742–4750 Occurrence Handle10.1128/AEM.66.11.4742-4750.2000 Occurrence Handle11055918
N Patel V Cardoza E Christensen B Rekapalli M Ayalew JCN Stewart (2004) ArticleTitleDifferential gene expression of Chlamydomonas reinhardtii in response to 2,4,6-trinitrotoluene (TNT) using microarray analysis Plant Science 167 1109–1122 Occurrence Handle10.1016/j.plantsci.2004.06.013
CM Peres SN Agathos (2000) ArticleTitleBiodegradation of nitroaromatic pollutants: from pathways to remediation Biotechnol. Ann. Rev. 6 197–220 Occurrence Handlefull_text||10.1016/S1387-2656(00)06023-3
CM Peres R Russ H Lenke SN Agathos (2001) ArticleTitleBiodegradation of 4-nitrobenzoate, 4-aminobenzoate and their mixtures: new strains, unusual metabolites and insights into pathway regulation FEMS Microbiol. Ecol. 37 151–159 Occurrence Handle10.1016/S0168-6496(01)00156-8
FJ Peterson RP Mason J Hovsepian JL Holtzman (1979) ArticleTitleOxygen-sensitive and -insensitive nitroreduction by Escherichia coli and rat hepatic microsomes J. Biol. Chem. 254 4009–4014 Occurrence Handle374406
DH Pieper W Reineke (2000) ArticleTitleEngineering bacteria for bioremediation Curr. Op. Biotechnol. 11 262–270 Occurrence Handle10.1016/S0958-1669(00)00094-X
JT Popesku A Singh J-S Zhao J Hawari OP Ward (2003) ArticleTitleHigh TNT-transforming activity by a mixed culture acclimated and maintained on crude-oil-containing media Can. J. Microbiol. 49 362–366 Occurrence Handle10.1139/w03-049 Occurrence Handle12897831
JT Popesku A Singh J-S Zhao J Hawari OP Ward (2004) ArticleTitleMetabolite production during transformation of 2,4,6-trinitrotoluene (TNT) by a mixed culture acclimated and maintained on crude oil-containing media Appl. Microbiol. Biotechnol. 65 739–746 Occurrence Handle10.1007/s00253-004-1625-3 Occurrence Handle15133643
V Purohit AK Basu (2000) ArticleTitleMutagenicity of nitroaromatic compounds Chem. Res. Toxicol. 13 673–692 Occurrence Handle10.1021/tx000002x Occurrence Handle10956054
JL Ramos M Mar Gonzalez-Perez A Caballero P Van Dillewijn (2005) ArticleTitleBioremediation of polynitrated aromatic compounds: Plants and microbes put fight Curr. Opin. Biotechnol. 16 275–281 Occurrence Handle10.1016/j.copbio.2005.03.010 Occurrence Handle15961028
W Rhys-Williams SC Taylor PA Williams (1993) ArticleTitleA novel pathway for the catabolism of 4-nitrotoluene by Pseudomonas J. Gen. Microbiol. 139 1967–1972 Occurrence Handle8245826
RG Riefler BF Smets (2000) ArticleTitleEnzymatic reduction of 2,4,6-trinitrotoluene and related nitroarenes: kinetics linked to one-electron redox potentials Environ. Sci. Technol. 34 3900–3906 Occurrence Handle10.1021/es991422f
P-G Rieger H-J Knackmuss (1995) Basic knowledge and perspectives on biodegradation of 2,4,6-trinitrotoluene and related nitroaromatic compounds in contaminated soil JC Spain (Eds) Biodegradation of Nitroaromatic Compounds Plenum Press New York 1–18
P-G Rieger H Meier M Gerle U Vogt T Groth H-J Knackmuss (2002) ArticleTitleXenobiotics in the environment: present and future strategies to obviate the problem of biological persistence J. Biotechnol. 94 101–123 Occurrence Handle10.1016/S0168-1656(01)00422-9 Occurrence Handle11792455
P-G Rieger V Sinnwell A Preub W Francke H-J Knackmuss (1999) ArticleTitleHydride-Meisenheimer complex formation and protonation as key reactions of 2,4,6-trinitrophenol biodegradation by Rhodococcus erythropolis J. Bacteriol. 181 1189–1195 Occurrence Handle9973345
BK Robertson PK Jjemba (2005) ArticleTitleEnhanced bioavailability of sorbed 2,4,6-trinitrotoluene (TNT) by a bacterial consortium Chemosphere 58 263–270 Occurrence Handle10.1016/j.chemosphere.2004.08.080 Occurrence Handle15581929
PY Robidoux P Gong M Sarrazin G Bardai L Paquet J Hawari C Dubois GI Sunahara (2004) ArticleTitleToxicity assessment of contaminated soils from an antitank firing range Ecotoxicol. Environ. Saf. 58 300–313 Occurrence Handle10.1016/j.ecoenv.2003.11.004 Occurrence Handle15223256
RA Sanford JR Cole FE Loffler JM Tiedje (1996) ArticleTitleCharacterization of Desulfitobacterium chlororespirans sp. nov., which grows by coupling the oxidation of lactate to the reductive dechlorination of 3-chloro-4-hydroxybenzoate Appl. Environ. Microbiol. 62 3800–3808 Occurrence Handle8837437
J Sarlauskas A Nemeikaite-Ceniene Z Anusevicius L Miseviciene MM Julvez M Medina C Gomez-Moreno N Cenas (2004) ArticleTitleFlavoenzyme-catalyzed redox cycling of hydroxylamino- and amino metabolites of 2,4,6-trinitrotoluene: implications for their cytotoxicity Arch. Biochem. Biophys. 425 184–192 Occurrence Handle10.1016/j.abb.2004.02.043 Occurrence Handle15111126
M Schaefer (2004) ArticleTitleAssessing 2,4,6-trinitrotoluene (TNT)-contaminated soil using three different earthworm test methods Ecotoxicol. Environ. Saf. 57 74–80 Occurrence Handle10.1016/j.ecoenv.2003.08.005 Occurrence Handle14659369
A Schenzle H Lenke P Fischer PA Williams H-J Knackmuss (1997) ArticleTitleCatabolism of 3-nitrophenol by Ralstonia eutropha JMP 134 Appl. Environ. Microbiol. 63 1421–1427
A Schenzle H Lenke JC Spain H-J Knackmuss (1999) ArticleTitleChemoselective nitro group reduction and reductive dechlorination initiate degradation of 2-chloro-5-nitrophenol by Ralstonia eutropha JMP134 Appl. Environ. Microbiol. 65 2317–2323 Occurrence Handle10347008
PD Schloss J Handelsman (2003) ArticleTitleBiotechnological prospects from metagenomics Cur. Op. Biotechnol. 14 303–310 Occurrence Handle10.1016/S0958-1669(03)00067-3
JL Seffernick LP Wackett (2001) ArticleTitleRapid evolution of bacterial catabolic enzymes: a case study with atrazine chlorohydrolase Biochemistry 40 12747–12753 Occurrence Handle10.1021/bi011293r Occurrence Handle11669610
MD Shelley RL Autenrieth JR Wild BE Dale (1996) ArticleTitleThermodynamic analysis of trinitrotoluene biodegradation and mineralization pathways Biotechnol. Bioeng. 50 198–205 Occurrence Handle10.1002/(SICI)1097-0290(19960720)51:2<198::AID-BIT9>3.0.CO;2-E
CF Shen JA Hawari G Ampleman S Thiboutot SR Guiot (2000) ArticleTitleOrigin of p-cresol in the anaerobic degradation of trinitrotoluene Can. J. Microbiol. 46 119–124 Occurrence Handle10.1139/cjm-46-2-119 Occurrence Handle10721479
TW Sheremata J Hawari (2000) ArticleTitleCyclodextrins for desorption and solubilization of 2,4,6-trinitrotoluene and its metabolites from soils Environ. Sci. Technol. 34 3462–3468 Occurrence Handle10.1021/es9910659
JR Snape NA Walkley AP Morby S Nicklin GF White (1997) ArticleTitlePurification, properties, and sequence of glycerol trinitrate reductase from Agrobacterium radiobacter J. Bacteriol. 179 7796–7802 Occurrence Handle9401040
Z Snellinx A Nepovim S Taghavi J Vangronsveld T Vanek D Vander Lelie (2002) ArticleTitleBiological remediation of explosives and related nitroaromatic compounds Environ. Sci. Pollut. Res. 9 48–61
JC Spain (2000) Introduction JC Spain JB Hughes H Knackmuss (Eds) Biodegradation of Nitroaromatic Compounds and Explosives Lewis Publishers New York 1–6
RJ Spanggord JC Spain SF Nishino KE Mortelmans (1991) ArticleTitleBiodegradation of 2,4-dinitrotoluene by a Pseudomonas sp Appl. Environ. Microbiol. 57 3200–3205 Occurrence Handle1781682
T Spiess F Desiere P Fischer JC Spain H-J Knackmuss H Lenke (1998) ArticleTitleA new 4-nitrotoluene degradation pathway in a Mycobacterium strain Appl. Environ. Microbiol. 64 446–452 Occurrence Handle9464378
WC Suen BE Haigler JC Spain (1996) ArticleTitle2,4-dinitrotoluene dioxygenase from Burkholderia sp. strain DNT: similarity to naphthalene dioxygenase J. Bacteriol. 178 4926–4934 Occurrence Handle8759857
WC Suen JC Spain (1993) ArticleTitleCloning and characterization of Pseudomonas sp. strain DNT genes for 2,4-dinitrotoluene degradation J. Bacteriol. 175 1831–1837 Occurrence Handle8449889
W-C Suen N Zhang L Xiao V Madison A Zaks (2004) ArticleTitleImproved activity and thermostability of Candida antarctica lipase B by DNA family shuffling Prot. Eng. Design Select 17 133–140 Occurrence Handle10.1093/protein/gzh017
GI Sunahara S Dodard M Sarrazin L Paquet G Ampleman S Thiboutot J Hawari AY Renoux (1998) ArticleTitleDevelopment of a soil extraction procedure for ecotoxicity characterization of energetic compounds Ecotoxicol. Environ. Saf. 39 185–194 Occurrence Handle10.1006/eesa.1997.1624 Occurrence Handle9570909
S Taylor A Hewitt J Lever C Hayes L Perovich P Thorne C Daghlian (2004) ArticleTitleTNT particle size distributions from detonated 155-mm howitzer rounds Chemosphere 55 357–367 Occurrence Handle10.1016/j.chemosphere.2003.11.031 Occurrence Handle14987934
KA Thorn JC Pennington C Hayes (2002) ArticleTitle15NMR investigation of the reduction and binding of TNT in an aerobic bench scale reactor simulating windrow composting Environ. Sci. Technol. 36 3797–3805 Occurrence Handle10.1021/es011382r Occurrence Handle12322753
KN Timmis DH Pieper (1999) ArticleTitleBacteria designed for bioremediation Trends Biotechnol. 17 201–204 Occurrence Handle10.1016/S0167-7799(98)01295-5
V Torsvik L Ovreas (2002) ArticleTitleMicrobial diversity and function in soil: from genes to ecosystems Curr. Op. Microbiol. 5 240–245 Occurrence Handle10.1016/S1369-5274(02)00324-7
T Urbanski (1964) Chemistry and Technology of Explosives Pergamon Press Oxford, UK
JM Tront JB Hughes (2005) ArticleTitleOxidative microbial degradation of 2,4,6-trinitrotoluene via 3-methyl-4,6-dinitrocatechol Environ. Sci. Technol 39 4540–4549 Occurrence Handle10.1021/es048014i Occurrence Handle16047791
B Aken ParticleVan SN Agathos (2001) ArticleTitleBiodegradation of nitro-substituted explosives by white-rot fungi: a mechanistic approach Adv. Appl. Microbiol. 48 1–77 Occurrence Handle11677677
B Van Aken JM Yoon JL Schnoor (2004) ArticleTitleBiodegradation 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 × nigra DN34) Appl. Environ. Microbiol. 70 508–517 Occurrence Handle10.1128/AEM.70.1.508-517.2004 Occurrence Handle14711682
LA Vanderberg JJ Perry PJ Unkefer (1995) ArticleTitleCatabolism of 2,4,6-trinitrotoluene by Mycobacterium vaccae Appl. Microbiol. Biotechnol. 43 937–945 Occurrence Handle10.1007/s002530050508 Occurrence Handle7576561
S Vats C Stuttard LC Vining (1987) ArticleTitleTransductional analysis of chloramphenicol biosynthesis genes in Streptomyces venezuelae J. Bacteriol. 169 3809–3813 Occurrence Handle3475271
C Vorbeck H Lenke P Fischer H-J Knackmuss (1994) ArticleTitleIdentification of a hydride-Meisenheimer complex as a metabolite of 2,4,6-trinitrotoluene by a Mycobacterium strain J. Bacteriol. 176 932–934 Occurrence Handle8300548
C Vorbeck H Lenke P Fischer JC Spain H-J Knackmuss (1998) ArticleTitleInitial reductive reaction in aerobic microbial metabolism of 2,4,6-trinitrotoluene Appl. Environ. Microbiol. 64 246–252
OP Ward A Singh JD Hamme ParticleVan (2003) ArticleTitleAccelerated biodegradation of petroleum waste J. Ind. Microbiol. Biotechnol. 30 260–270 Occurrence Handle10.1007/s10295-003-0042-4 Occurrence Handle12687495
JM Weiss AJ Mckay C Derito C Watanabe KA Thorn EL Madsen (2004a) ArticleTitleDevelopment and application of pyrolysis gas chromatography/mass spectrometry for the analysis of bound trinitrotoluene residues in soil Environ. Sci. Technol. 38 2167–2174 Occurrence Handle10.1021/es034911v
M Weiss R Geyer T Gunther M Kaestner (2004b) ArticleTitleFate and stability of 14C-labeled 2,4,6-trinitrotoluene in contaminated soil following microbial bioremediation processes Environ. Toxicol. Chem. 23 2049–2060 Occurrence Handle10.1897/03-143
M Weiss R Geyer R Russow HH Richnow M Kastner (2004c) ArticleTitleFate and metabolism of [15N]2,4,6-trinitrotoluene in soil Environ. Toxicol. Chem. 23 1852–1860 Occurrence Handle10.1897/03-414
RE Williams NC Bruce (2002) ArticleTitle‘New uses for an Old Enzyme’ – the Old Yellow Enzyme family of flavoenzymes Microbiology 148 1607–1614 Occurrence Handle12055282
RE Williams DA Rathbone NS Scrutton NC Bruce (2004) ArticleTitleBiotransformation of explosives by the old yellow enzyme family of flavoproteins Appl. Environ. Microbiol. 70 3566–3574 Occurrence Handle10.1128/AEM.70.6.3566-3574.2004 Occurrence Handle15184158
AV Yabannavar G Zylstra (1995) ArticleTitleCloning and characterization of the genes for p-nitrobenzoate degradation from Pseudomonas pickettii YH105 Appl. Environ. Microbiol. 61 4284–4290 Occurrence Handle8534095
J Ye A Singh OP Ward (2004) ArticleTitleBiodegradation of nitroaromatics and other nitrogen-containing xenobiotics World J. Microbiol. Biotechnol. 20 117–135 Occurrence Handle10.1023/B:WIBI.0000021720.03712.12
J Zeyer HP Kocher KN Timmis (1986) ArticleTitleInfluence of para-substituents on the oxidative metabolism of o-nitrophenols by Pseudomonas putida B2 Appl. Environ. Microbiol. 52 334–339 Occurrence Handle3752997
Y-X Zhang K Perry VA Vinci K. Powell WPC Stemmer SB del Cardayré (2002) ArticleTitleGenome shuffling leads to rapid phenotypic improvement in bacteria Nature 415 644–646 Occurrence Handle10.1038/415644a Occurrence Handle11832946
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Stenuit, B., Eyers, L., Fantroussi, S.E. et al. Promising Strategies for the Mineralisation of 2,4,6-trinitrotoluene. Rev Environ Sci Biotechnol 4, 39–60 (2005). https://doi.org/10.1007/s11157-005-5515-7
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s11157-005-5515-7