Abstract
The review covers the strategies for the biodegradation of a dangerous pollutant of the environment, an explosive 2,4,6-trinitrotoluene. The characteristics of the metabolism of this compound in microorganisms under aerobic and anaerobic conditions and the main enzymes involved in the transformation are described. The main class of enzymes involved in the destruction of trinitrotoluene are nitroreductases; oxidases, hydrogenases, and peroxidases may also be involved in degradation. Several approaches to the biodegradation of trinitrotoluene in the environment have been singled out and discussed: bioaugmentation of the biomass of TNT-destructor strains and consortia of microorganisms that degrade this compound; stimulation of the autochthonous microflora of polluted natural environments via the introduction of additional substrates for microorganism growth and electron donors for the reduction of trinitrotoluene; pollutant biodegradation by immobilized cells of microorganisms in bioreactors and biofilters; phytoremediation and the application of preventive measures consisting of the introduction of spores and lyophilisates of bacteria with biodegradation activity in a mixture containing nitroaromatic compounds.
Similar content being viewed by others
REFERENCES
Ju, K.-S. and Parales, R.E., Nitroaromatic compounds, from synthesis to biodegradation, Microbiol. Mol. Biol. Rev., 2010, vol. 74, no. 2, pp. 250–272. doi 10.1128/MMBR.00006-10
Mercimek, H.A., Dincer, S., Guzeldag, G., et al., Degradation of 2,4,6-trinitrotoluene by P. aeruginosa and characterization of some metabolites, Braz. J. Microbiol., 2015, vol. 46, no. 1, pp. 103–111. doi 10.1590/S1517-838246120140026
Kalderis, D., Hawthorne, S.B., Clifford, A.A., and Gidarakos, E., Interaction of soil, water and TNT during degradation of TNT on contaminated soil using subcritical water, J. Hazard. Mater., 2008, vol. 159, pp. 329–334. doi 10.1016/j.jhazmat.2008.02.041
Fu, D., Zhang, Y., Lv, F., et al., Removal of organic materials from TNT red water by Bamboo Charcoal adsorption, Chem. Eng. J., 2012, vols. 193–194, pp. 39–49. doi 10.1016/j.cej.2012.03.039
Muter, O., Potapova, K., Limane, B., et al., The role of nutrients in the biodegradation of 2,4,6-trinitrotoluene in liquid and soil, J. Environ. Manage., 2012, vol. 98, pp. 51–55. doi 10.1016/j.jenvman.2011.12.010
Claus, H., Microbial degradation of 2,4,6-trinitrotoluene in vitro and in natural environments, in Biological Remediation of Explosive Residues, Environmental Science and Engineering, Singh, S.N., Ed., Switzerland: Springer International Publishing, 2014, pp. 15–38. doi 10.1007/978-3-319-01083-0_2
Kao, C.-M., Lin, B.-H., Chen, S.-C., et al., Biodegradation of trinitrotoluene (TNT) by indigenous microorganisms from TNT contaminated soil, and their application in TNT bioremediation, Bioremed. J., 2016, vol. 20, no. 3, pp. 165–173. doi 10.1080/10889868.2016.1148007
Stenuit, B.A. and Agathos, S.N., Microbial 2,4,6-trinitrotoluene degradation: could we learn from (bio)chemistry for bioremediation and vice versa?, Appl. Microbiol. Biotechnol., 2010, vol. 88, pp. 1043–1064. doi 10.1007/ s00253-010-2830-x
Gallagher, E.M., Young, L.Y., McGuinness, L.M., and Kerkhof, L.J., Detection of 2,4,6-trinitrotoluene-utilizing anaerobic bacteria by 15N and 13C incorporation, Appl. Environ. Microbiol., 2010, vol. 76, no. 5, pp. 1695–1698. doi 10.1128/AEM.02274-09
Montgomery, M.T., Coffin, R.B., Boyd, T.J., et al., 2,4,6-Trinitrotoluene mineralization and bacterial production rates of natural microbial assemblages from coastal sediments, Environ. Pollut., 2011, vol. 159, pp. 3673–3680. doi 10.1016/j.envpol.2011.07.018
Erkelens, M., Adetutu, E.M., Taha, M., et al., Sustainable remediation—the application of bioremediated soil for use in the degradation of TNT chips, J. Environ. Manage., 2012, vol. 110, pp. 69–76. doi 10.1016/j.jenvman.2012.05.022
Kulkarni, M. and Chaudhari, A., Microbial remediation of nitro-aromatic compounds: an overview, J. Environ. Manage., 2007, vol. 85, pp. 496–512. doi 10.1016/j.jenvman.2007.06.009
Innemanova, P., Velebova, R., Filipova, A., et al., Anaerobic in situ biodegradation of TNT using whey as an electron donor: a case study, New Biotechnol., 2015, vol. 32, no. 6, pp. 701–709. doi 10.1016/j.nbt.2015.03.014
Adrian, N.R. and Arnett, C.M., Anaerobic biotransformation of explosives in aquifer slurries amended with ethanol and propylene glycol, Chemosphere, 2007, vol. 66, pp. 1849–1856. doi 10.1016/j.chemosphere.2006.08.042
Sheu, Y.T., Lien, P.J., Chen, C.C., et al., Bioremediation of 2,4,6-trinitrotoluene-contaminated groundwater using unique bacterial strains: microcosm and mechanism studies, Int. J. Environ. Sci. Technol., 2016, vol. 13, pp. 1357–1366. doi 10.1007/s13762-016-0976-5
Chatterjee, S., Deb, U., Datta, S., et al., Common explosives (TNT, RDX, HMX) and their fate in the environment: emphasizing bioremediation, Chemosphere, 2017, vol. 184, pp. 438–451. doi 10.1016/j.chemosphere.2017.06.008
Glick, B.R., Using soil bacteria to facilitate phytoremediation, Biotech. Adv., 2010, vol. 28, pp. 367–374. doi 10.1016/j.biotechadv.2010.02.001
Das, P., Datta, R., Makris, K.C., and Sarkar, D., Vetiver grass is capable of removing TNT from soil in the presence of urea, Environ. Pollut., 2010, vol. 158, pp. 1980–1983. doi 10.1016/j.envpol.2009.12.011
Das, P., Sarkar, D., Makris, K.C., and Datta, R., Urea-facilitated uptake and nitroreductase-mediated transformation of 2,4,6-trinitrotoluene in soil using vetiver grass, J. Environ. Chem. Eng., 2015, vol. 3, no. 1, pp. 445–452. doi 10.1016/j.jece.2015.01.008
Kiiskila, J.D., Das, P., Sarkar, D., and Datta, R., Phytoremediation of explosive-contaminated soils, Curr. Pollut. Rep., 2015, vol. 1, pp. 23–34. doi 10.1007/s40726-015-0003-3
Afzal, M., Khan, Q.M., and Sessitsch, A., Endophytic bacteria: prospects and applications for the phytoremediation of organic pollutants, Chemosphere, 2014, vol. 117, pp. 232–242. doi 10.1016/j.chemosphere.2014.06.078
Hannink, N.K., Subramanian, M., Rosser, S.J., et al., Enhanced transformation of TNT by tobacco plants expressing a bacterial nitroreductase, Int. J. Phytorem., 2007, vol. 9, pp. 385–401. doi 10.1080/ 15226510701603916
Kurumata, M., Takahashi, M., Sakamoto, A., et al., Tolerance to, and uptake and degradation of 2,4,6-trinitrotoluene (TNT) are enhanced by the expression of a bacterial nitroreductase gene in Arabidopsis thaliana, Z. Naturforsch. C, 2005, vol. 60, nos. 3—4, pp. 272–278. doi 10.1515/znc-2005-3-412
van Dillewijn, P., Couselo, J.L., Corredoira, E., et al., Bioremediation of 2,4,6-trinitrotoluene by bacterial nitroreductase expressing transgenic aspen, Environ. Sci. Technol., 2008, vol. 42, no. 19, pp. 7405–7410. doi 10.1021/es801231w
French, C.E., Rosser, S.J., Davies, G.J., et al., Biodegradation of explosives by transgenic plants expressing pentaerythritol tetranitrate reductase, Nat. Biotechnol., 1999, vol. 17, pp. 491–494. doi 10.1038/8673
Zhu, B., Peng, R.H., Fu, X.Y., et al., Enhanced transformation of TNT by Arabidopsis plants expressing an old yellow enzyme, Plos One, 2012, vol. 7, no. 7. e39 861. doi 10.1371/journal.pone.0039861
Panz, K. and Miksch, K., Phytoremediation of explosives (TNT, RDX, HMX) by wild-type and transgenic plants, J. Environ. Manage., 2012, vol. 113, pp. 85–92. doi 10.1016/j.jenvman.2012.08.016
Makris, K.C., Sarkar, D., and Datta, R., Coupling indigenous biostimulation and phytoremediation for the restoration of 2,4,6-trinitrotoluene-contaminated sites, J. Environ. Monit., 2010, vol. 12, pp. 399–403. doi 10.1039/b908162c
Ullah, H., Shah, A.A., Hasan, F., and Hameed, A., Biodegradation of trinitrotoluene by immobilized Bacillus sp. YRE1, Pak. J. Bot., 2010, vol. 42, no. 5, pp. 3357–3367.
Solyanikova, I.P., Robota, I.V., Mazur, D.M., et al., Application of Bacillus sp. strain VT-8 for decontamination of TNT polluted sites, Microbiology, 2014, vol. 83, no. 5, pp. 577–584. doi 10.1134/S0026261714050257
Lin, H., Chen, Z., Megharaj, M., and Naidu, R., Biodegradation of TNT using Bacillus mycoides immobilized in PVA–sodium alginate—kaolin, Appl. Clay Sci., 2013, vol. 83-84, pp. 336–342. doi 10.1016/j.clay.2013.08.004
Wang, Z., Ye, Z., Zhang, M., and Bai, X., Degradation of 2,4,6-trinitrotoluene (TNT) by immobilized microorganism-biological filter, Process Biochem., 2010, vol. 45, pp. 993–1001. doi 10.1016/j.procbio.2010.03.006
Zhang, M., Liu, G.-H., Song, K., et al., Biological treatment of 2,4,6-trinitrotoluene (TNT) red water by immobilized anaerobic–aerobic microbial filters, Chem. Eng. J., 2015, vol. 259, pp. 876–884. doi 10.1016/j.cej.2014.08.041
Nyanhongo, G.S., Aichernig, N., Ortner, M., et al., Incorporation of 2,4,6-trinitrotoluene (TNT) transforming bacteria into explosive formulations, J. Hazard. Mater., 2009, vol. 165, pp. 285–290. doi 10.1016/j.jhazmat.2008.09.107
Mercimek, H.A., Dincer, S., Guzeldag, G., et al., Aerobic biodegradation of 2,4,6-trinitrotoluene (TNT) by Bacillus cereus isolated from contaminated soil, Microb. Ecol., 2013, vol. 66, pp. 512–521. doi 10.1007/s00248-013-0248-6
Bai, J., Yang, J., Liu, P., and Yang, Q., Transformation pathway of 2,4,6-trinitrotoluene by Escherichia coli nitroreductases and improvement of activity using structure-based mutagenesis, Process Biochem., 2015, vol. 50, pp. 705–711. doi 10.1016/j.procbio.2015.01.029
Smets, B.F., Yin, H., and Esteve-Nunez, A., TNT biotransformation: when chemistry confronts mineralization, Appl. Microbiol. Biotechnol., 2007, vol. 76, pp. 267–277. doi 10.1007/s00253-007-1008-7
Rylott, E.L., Lorenz, A., and Bruce, N.C., Biodegradation and biotransformation of explosives, Curr. Opin. Biotechnol., 2011, vol. 22, pp. 434–440. doi 10.1016/ j.copbio.2010.10.014
Keenan, B.G. and Wood, T.K., Orthric Rieske dioxygenases for degrading mixtures of 2,4-dinitrotoluene/naphthalene and 2-amino-4,6-dinitrotoluene/4-amino-2,6-dinitrotoluene, Appl. Microbiol. Biotechnol., 2006, vol. 73, pp. 827–838. doi 10.1007/s00253-006-0538-8
Nyanhongo, G.S., Schroeder, M., Steiner, W., and Gubitz, G.M., Biodegradation of 2,4,6-trinitrotoluene (TNT): an enzymatic perspective, Biocatal. Biotransform., 2005, vol. 23, no.2, pp. 53–69. doi 10.1080/10242420500090169
Esteve-Nunez, A., Caballero, A., and Ramos, J.L., Biological degradation of 2,4,6-trinitrotoluene, Microbiol. Mol. Biol. Rev., 2001, vol. 65, no. 3, pp. 335–352. doi 10.1128/MMBR.65.3.335–352.2001
Solyanikova, I.P., Baskunov, B.P., Baboshin, M.A., et al., Detoxification of high concentrations of trinitrotoluene by bacteria, App. Biochem. Microbiol., 2012, vol. 48, no. 1, pp. 21–27.
Gumuscu, B. and Tekinay, T., Effective biodegradation of 2,4,6-trinitrotoluene using a novel bacterial strain isolated from TNT-contaminated soil, Int. Biodeterior. Biodegrad., 2013, vol. 85, pp. 35–41. doi 10.1016/j.ibiod.2013.06.007
Lee, B.-U., Park, S.-C., Cho, Y.-S., et al., Expression and characterization of the TNT nitroreductase of Pseudomonas sp. HK-6 in Escherichia coli, Curr. Microbiol., 2008, vol. 56, pp. 386–390. doi 10.1007/s00284-007-9093-5
Hong, Y. and Gu, J.-D., Bacterial anaerobic respiration and electron transfer relevant to the biotransformation of pollutants, Int. Biodeterior. Biodegrad., 2009, vol. 63, pp. 973–980. doi 10.1016/j.ibiod.2009.08.001
Huang, J., Ning, G., Li, F., and Sheng, G.D., Biotransformation of 2,4-dinitrotoluene by obligate marine Shewanella marisflavi EP1 under anaerobic conditions, Bioresour. Technol., 2015, vol. 180, pp. 200–206. doi 10.1016/j.biortech.2014.12.108
Bhattacharya, J., Dev, S., and Das, B., Low Cost Wastewater Bioremediation Technology, Chapter 2: Nutrients for the Selective Growth of Specific Bacteria, Elsevier, 2018, pp. 43–75
Meier, M.J., Paterson, E.S., and Lambert, I.B., Use of substrate-induced gene expression in metagenomic analysis of an aromatic hydrocarbon-contaminated soil, Appl. Environ. Microbiol., 2016, vol. 82, no. 3, pp. 897–909. doi 10.1128/AEM.03306-15
Park, C., Kim, T.-H., Kim, S., et al., Enhanced biodegradation of 2,4,6-trinitrotoluene (TNT) with various supplemental energy sources, J. Microbiol. Biotechnol., 2002, vol. 12, no. 4, pp. 695—698.
Liang, S.-H., Hsu, D.-W., Lin, C.-Y., et al., Enhancement of microbial 2,4,6-trinitrotoluene transformation with increased toxicity by exogenous nutrient amendment, Ecotoxicol. Environ. Saf., 2017, vol. 138, pp. 39–46. doi 10.1016/j.ecoenv.2016.12.012
Khilyas, I.V., Ziganshin, A.M., Pannier, A.J., and Gerlach, R., Effect of ferrihydrite on 2,4,6-trinitrotoluene biotransformation by an aerobic yeast, Biodegradtion, 2013, vol. 24, no. 5, pp. 631–644. doi 10.1007/s10532-012-9611-4
Soojhawon, I., Lokhande, P.D., Kodam, K.M., and Gawai, K.R., Biotransformation of nitroaromatics and their effects on mixed function oxidase system, Enzyme Microb. Technol., 2005, vol. 37, no. 5, pp. 527–533. doi 10.1016/j.enzmictec.2005.03.011
Lin, H.-Y., Yu, C.-P., and Chen, Z.-L., Aerobic and anaerobic biodegradation of TNT by newly isolated Bacillus mycoides, Ecol. Eng., 2013, vol. 52, pp. 270–277. doi 10.1016/j.ecoleng.2012.11.004
Bernstein, A. and Ronen, Z., Biodegradation of the explosives TNT, RDX and HMX in microbial degradation of xenobiotics, in Environmental Science and Engineering, Singh, S.N., Ed., Berlin: Springer, 2012, pp. 135–176.
Zaripov, S.A., Naumov, A.V., Abdrakhmanova, J.F., et al., Models of 2,4,6-trinitrotoluene (TNT) initial conversion by yeasts, FEMS Microbiol. Lett., 2002, vol. 217, pp. 213–217. doi 10.1111/j.1574-6968.2002.tb11477.x
Ziganshin, A.M., Gerlakh, R., Naumenko, E.A., and Naumova, R.P., Aerobic Degradation of 2,4,6-trinitrotoluene by the YEAST STRAIN Geotrichum candidum AN-Z4, Microbiology (Moscow), 2010, vol. 79, no. 2, pp. 178–183.
Anasonye, F., Winquist, E., Rasanen, M., et al., Bioremediation of TNT contaminated soil with fungi under laboratory and pilot scale conditions, Int. Biodeterior. Biodegrad., 2015, vol. 105, pp. 7–12. doi 10.1016/j.ibiod.2015.08.003
Ziganshin, A.M., Naumova, R.P., Pannier, A.J., and Gerlach, R., Influence of pH on 2,4,6-trinitrotoluene degradation by Yarrowia lipolytica, Chemosphere, 2010, vol. 79, pp. 426–433. doi 10.1016/j.chemosphere.2010.01.051
Gallagher, E.M., Anaerobic degradation of 2,4,6- trinitrotoluene (TNT): molecular analysis of active degraders and metabolic pathways, Ph.D. Thesis, New Brunswick, New Jersey, 2010.
Fleischmann, T.J., Walker, K.C., Spain, J.C., et al., Anaerobic transformation of 2,4,6-TNT by bovine ruminal microbes, Biochem. Biophys. Res. Commun., 2004, vol. 314, pp. 957–963. doi 10.1016/j.bbrc.2003.12.193
ACKNOWLEDGMENTS
The work was supported by Russian Foundation for Basic Research and Perm Region (project no. 16-44-590359).
Author information
Authors and Affiliations
Corresponding author
Additional information
Translated by A. Ostyak
Abbreviations: TNT—trinitrotoluene; UV—ultraviolet radiation; COD—chemical oxygen consumption; SIGEX—substrate-induced gene expression.
Rights and permissions
About this article
Cite this article
Maksimova, Y.G., Maksimov, A.Y. & Demakov, V.A. Biotechnological Approaches to the Bioremediation of an Environment Polluted with Trinitrotoluene. Appl Biochem Microbiol 54, 767–779 (2018). https://doi.org/10.1134/S0003683818080045
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0003683818080045