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http://dx.doi.org/10.4014/jmb.1203.04002

Microbial Degradation and Toxicity of Hexahydro-1,3,5-Trinitro-1,3,5-Triazine  

Khan, Muhammad Imran (Department of Civil and Environmental Engineering, College of Engineering, Yonsei University)
Lee, Jaejin (Department of Civil and Environmental Engineering, College of Engineering, Yonsei University)
Park, Joonhong (Department of Civil and Environmental Engineering, College of Engineering, Yonsei University)
Publication Information
Journal of Microbiology and Biotechnology / v.22, no.10, 2012 , pp. 1311-1323 More about this Journal
Abstract
In the present work, current knowledge on the potential fate, microbial degradation, and toxicity of hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) was thoroughly reviewed, focusing on the toxicological assessment of a variety of potential RDX degradation pathways in bacteria and fungi. The present review on microbial degradation pathways and toxicities of degradation intermediates suggests that, among aerobic RDX degradation pathways, the one via denitration may be preferred in a toxicological perspective, and that among anaerobic pathways, those forming 4-nitro-2,4-diazabutanal (NDAB) via ring cleavage of 1-nitroso-3,5-dinitro-1,3,5-triazinane (MNX) may be toxicologically advantageous owing to its potential mineralization under partial or complete anoxic conditions. These findings provide important information on RDX-degrading microbial pathways, toxicologically most suitable to be stimulated in contaminated fields.
Keywords
RDX; microbial degradation; intermediate toxicity; biodegradation pathway; bioremediation;
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1 Crouse, L. C. B., M. W. Michie, M. A. Major, M. S. Johnson, R. B. Lee, and H. I. Paulus. 2006. Subchronic oral toxicity of RDX in rats. In: Toxicology Study No. 85-XC-5131-03. Protocol No. 5131-38-02-12-01. U.S. Army Center for Health Promotion and Preventive Medicine, Aberdeen Providing Ground, MD.
2 Davies, J. O., D. M. Roberts, A. Hittarage, and N. A. Buckley. 2007. Oral C-4 plastic explosive in humans - a case series. Clin. Toxicol. (Phila.) 45: 454-457.   DOI   ScienceOn
3 Department of Defense (DoD) (US). 2010. Emerging Chemical and Material Risks. Available at https://www.denix.osd.mil/portal/page/portal/CMRMD/ECMR.
4 EPA. 2009. 2009 Edition of the Drinking Water Standards and Health Advisories. Available at http://water.epa.gov/action/advisories/drinking/upload/dwstandards2009.pdf .
5 Fournier, D., A. Halasz, J. Spain, P. Fiurasek, and J. Hawari. 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: 166-172.   DOI   ScienceOn
6 Fournier, D., A. Halasz, J. Spain, R. J. Spanggord, J. C. Bottaro, and J. Hawari. 2004. Biodegradation of the hexahydro-1,3,5-trinitro-1,3,5-triazine ring cleavage product 4-nitro-2,4-diazabutanal by Phanerochaete chrysosporium. Appl. Environ. Microbiol. 70: 1123-1128.   DOI   ScienceOn
7 Fournier, D., S. Trott, J. Hawari, and J. Spain. 2005. Metabolism of the aliphatic nitramine 4-nitro-2,4-diazabutanal by Methylobacterium sp. strain JS178. Appl. Environ. Microbiol. 71: 4199-4202.   DOI   ScienceOn
8 Adrian, N. R. and C. M. Arnett. 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: 332-340.   DOI   ScienceOn
9 Zhao, J. S., L. Paquet, A. Halasz, and J. Hawari. 2003. 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: 187-193.   DOI   ScienceOn
10 Sunahara, G. I., S. Dodard, M. Sarrazin, L. Paquet, G. Ampleman, S. Thiboutot, J. Hawari, and A. Y. Renoux. 1998. Development of a soil extraction procedure for ecotoxicity characterization of energetic compounds. Ecotoxicol. Environ. Saf. 39: 185-194.   DOI   ScienceOn
11 Thompson, K. T., F. H. Crocker, and H. L. Fredrickson. 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: 8265-8272.   DOI   ScienceOn
12 Vila, M., S. Mehier, S. Lorber-Pascal, and F. Laurent. 2007. Phytotoxicity to and uptake of RDX by rice. Environ. Pollut. 145: 813-817.   DOI   ScienceOn
13 Weisse, R. 2008. The bioremediation of 2,4,6-trinitrotoluene by three classes of organisms. Basic Biotechnol. eJournal 4: 66-71.
14 Williams, L. R., K. Wong, A. Stewart, C. Suciu, S. Gaikwad, N. Wu, et al. 2012. Behavioral and physiological effects of RDX on adult zebrafish. Compar. Biochem. Physiol. C 155: 33-38.
15 Zhang, B. H., S. B. Cox, S. T. McMurry, A. Jackson, G. P. Cobb, and T. A. Anderson. 2008. Effect of two major N-nitroso hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) metabolites on earthworm reproductive success. Environ. Pollut. 153: 658-667.   DOI   ScienceOn
16 Woody, R. C., G. L. Kearns, M. A. Brewster, C. P. Turley, G. B. Shapr, and R. S. Lake. 1986. The neurotoxicity of cyclotrimethylenetrinitramine (RDX) in a child: A clinical and pharmacokinetic evaluation. Clin. Toxicol. 24: 305-319.   DOI
17 Zhang, B. H., C. M. Freitag, J. E. Canas, Q. Q. Cheng, and T. A. Anderson. 2006. Effects of hexahydro-1,3,5-trinitro-1,3,5- triazine (RDX) metabolites on cricket (Acheta domesticus) survival and reproductive success. Environ. Pollut. 144: 540-544.   DOI   ScienceOn
18 Zhang, B. H., R. J. Kendall, and T. A. Anderson. 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: 86-95.   DOI   ScienceOn
19 Zhang, B. and X. Pan. 2009. RDX induces aberrant expression of microRNAs in mouse brain and liver. Environ. Health Perspect. 117: 231-240.
20 Zhang, C. L. and J. B. Hughes. 2003. Biodegradation pathways of hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) by Clostridium acetobutylicum cell-free extract. Chemosphere 50: 665-671.   DOI   ScienceOn
21 Zhao, J. S., A. Halasz, L. Paquet, C. Beaulieu, and J. Hawari. 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: 5336-5341.   DOI   ScienceOn
22 Rylott, E. L. and N. C. Bruce. 2009. Plants disarm soil: Engineering plants for the phytoremediation of explosives. Trends Biotechnol. 27: 73-81.   DOI   ScienceOn
23 Zhao, J. S., D. Manno, and J. Hawari. 2008. Regulation of hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) metabolism in Shewanella halifaxensis HAW-EB4 by terminal electron acceptors and involvement of c-type cytochrome. Soc. Gen. Microbiol. 154: 1026-1037.
24 Roh, H., C. P. Yu, M. E. Fuller, and K. H. Chu. 2009. Identification of hexahydro-1,3,5-trinitro-1,3,5-triazine-degrading microorganisms via 15N stable isotope probing. Environ. Sci. Technol. 43: 2505-2511.   DOI   ScienceOn
25 Rylott, E. L., A. Lorenz, and N. C. Bruce. 2010. Biodegradation and biotransformation of explosives. Curr. Opin. Biotechnol. 22: 17.
26 Rylott, E. L., R. G. Jackson, F. Sabbadin, H. M. B. Seth-Smith, J. Edwards, C. S. Chong, et al. 2011. The explosive-degrading cytochrome P450 XplA: Biochemistry, structural features and prospects for bioremediation. Biochem. Biophys. Acta 1814: 230-236.   DOI   ScienceOn
27 Sagi-Ben Moshe, S., Z. Ronen, O. Dahan, N. Weisbrod, L. Groisman, E. Adar, and R. Nativ. 2009. Sequential biodegradation of TNT, RDX and HMX in a mixture. Environ. Pollut. 157: 2231-2238.   DOI   ScienceOn
28 Seth-Smith, H. M. B., J. Edwards, S. J. Rosser, D. A. Rathbone, and N. C. Bruce. 2008. The explosive-degrading cytochrome P450 system is highly conserved among strains of Rhodococcus spp. Appl. Environ. Microbiol. 74: 4550-4552.   DOI   ScienceOn
29 Sheremata, T. W. and J. Hawari. 2000. Mineralization of RDX by the white rot fungus Phanerochaete chrysosporium to carbon dioxide and nitrous oxide. Environ. Sci. Technol. 34: 3384-3388.   DOI   ScienceOn
30 Simini, M., R. T. Checkai, R. G. Kuperman, C. T. Phillips, J. E. Kolakowski, C. W. Kurnas, and G. I. Sunahara. 2003. Reproduction and survival of Eisenia fetida in a sandy loam soil amended with the nitro-heterocyclic explosives RDX and HMX. Pedobiologia 47: 657-662.
31 Smith, J. N., J. Liu, M. A. Espino, and G. P. Cobb. 2007. Age dependent acute oral toxicity of hexahydro-1,3,5-trinitro-1,3,5- triazine (RDX) and two anaerobic N-nitroso metabolites in deer mice (Peromyscus maniculatus). Chemosphere 67: 2267-2273.   DOI   ScienceOn
32 Smith, J. N., M. A. Espino, J. Liu, N. A. Romero, S. B. Cox, and G. P. Cobb. 2009. Multigenerational effects in deer mice (Peromyscus maniculatus) exposed to hexahydro-1,3,5-trinitroso-1,3,5-triazine (TNX). Chemosphere 75: 910-914.   DOI   ScienceOn
33 Smith, J. N., X. Pan, A. Gentles, E. E. Smith, S. B. Cox, and G. P. Cobb. 2006. Reproductive effects of hexahydro-1,3,5-trinitroso-1,3,5-triazine in deer mice (Peromyscus maniculatus) during a controlled exposure study. Environ. Toxicol. Chem. 25: 446-451.   DOI   ScienceOn
34 Spanggord, R. J., T. Mill, T. W. Chou, W. H. Mabey, J. H. Smith, and S. Lee. 1980. Environmental fate studies on certain munition waste water constituents: Part 2. SRI Report LSU- 7934. SRI International, Menlo Park, CA.
35 Stahl, J. D., B. V. Aken, M. D. Cameron, and S. D. Aust. 2001. Hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) biodegradation in liquid and solid-state matrices by Phanerochaete chrysosporium. Bioremed. J. 5: 13-25.   DOI   ScienceOn
36 Meyer, S. A., A. J. Marchand, J. L. Hight, G. H. Roberts, L. B. Escalon, L. S. Inouye, and D. K. MacMillan. 2005. Up-anddown procedure (UDP) determinations of acute oral toxicity of nitroso degradation products of hexahydro-1,3,5-trinitro-1,3,5- triazine (RDX). J. Appl. Toxicol. 25: 427-434.   DOI   ScienceOn
37 Nejidat, A., L. Kafka, Y. Tekoah, and Z. Ronen. 2008. Effect of organic and inorganic nitrogenous compounds on RDX degradation and cytochrome P450 expression in Rhodococcus strain YH1. Biodegradation 19: 313-320.   DOI   ScienceOn
38 Monteil-Rivera, F., L. Paquet, R. Giroux, and J. Hawari. 2008. Contribution of hydrolysis in the abiotic attenuation of RDX and HMX in coastal waters. J. Environ. Qual. 37: 858-864.   DOI   ScienceOn
39 Monteil-Rivra, F., L. Paquet, A. Halasz, M. T. Montgomery, and J. Hawari. 2005. Reduction of octahydro-1,3,5,7-tetranitro-1,3,5,7-tetrazocine by zerovalent iron: Product distribution. Environ. Sci. Technol. 39: 9725-9731.   DOI   ScienceOn
40 Mukhi, S., X. P. Pan, G. P. Cobb, and R. Patino. 2005. Toxicity of hexahydro-1,3,5-trinitro-1,3,5-triazine to larval zebrafish (Danio rerio). Chemosphere 61: 178-185.   DOI   ScienceOn
41 Occupational Safety and Health Administration (OSHA). 2010. Cyclonite (RDX). http://www.osha.gov/dts/chemicalsampling/data/CH_231075.html
42 Pak, J. W., K. L. Knoke, D. R. Noguera, B. G. Fox, and G. H. Chambliss. 2000. Transformation of 2,4,6-trinitrotoluence by purified xenobiotics reductase B from Pseudomonas fluorescens I-C. Appl. Environ. Micobiol. 66: 4742-4750.   DOI   ScienceOn
43 Pan, X., B. Zhang, J. Smith, M. San Francisco, T. Anderson, and G. Cobb. 2007. N-Nitroso compounds produced in deer mouse (Peromyscus maniculatus) GI tracts following hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) exposure. Chemosphere 67: 1164-1170.   DOI   ScienceOn
44 Park, J., S. D. Comfort, P. J. Shea, and T. A. Machacek. 2004. Remediating munitions-contaminated soil with zerovalent iron and cationic surfactants. J. Environ. Qual. 33: 1305-1313.   DOI   ScienceOn
45 Rocheleau, S., B. Lachance, R. G. Kuperman, J. Hawari, S. Thiboutot, G. Ampleman, and G. I. Sunahara. 2008. Toxicity and uptake of cyclic nitramine explosives in ryegrass Lolium perenne. Environ. Pollut. 156: 199-206.   DOI   ScienceOn
46 Perreault, N. N., F. H. Crocker, K. J. Indest, and J. Hawari. 2012. Involvement of cytochrome c CymA in the anaerobic metabolism of RDX by Shewanella oneidensis MR-1. Can. J. Microbiol. 58: 124-131.   DOI   ScienceOn
47 Quinn Jr., M. J., M. A. Bazar, C. A. McFarland, E. J. Perkins, K. A. Gust, and M. S. Johnson. 2009. Sublethal effects of subacute exposure to RDX (1,3,5-trinitro-1,3,5-triazine) in the northern bobwhite (Colinus virginianus). Environ. Toxicol. Chem. 28: 1266-1270.   DOI   ScienceOn
48 Robidoux, P. Y., C. Svendsen, J. Caumartin, J. Hawari, G. Ampleman, S. Thiboutot, J. M. Weeks, and G. I. Sunahara. 2000. Chronic toxicity of energetic compounds in soil determined using the earthworm (Eisenia andrei) reproduction test. Environ. Toxicol. Chem. 19: 1764-1773
49 Iwai, S., B. Chai, W. J. Sul, J. R. Cole, S. A. Hashsham, and J. M. Tiedje. 2010. Gene-targeted-metagenomics reveals extensive diversity of aromatic dioxygenase genes in the environment. ISME J. 4: 279-285.   DOI   ScienceOn
50 Jackson, R. G., E. L. Rylott, D. Fournier, J. Hawari, and N. C. Bruce. 2007. Exploring the biochemical properties and remediation applications of the unusual explosive-degrading P450 system XplA/B. Proc. Natl. Acad. Sci. USA 104: 16822-16827.   DOI   ScienceOn
51 Johnson, M. S., M. J. Quinn Jr., M. A. Bazar, K. A. Gust, B. L. Escalon, and E. J. Perkins. 2007. Subacute toxicity of oral 2,6- dinitrotoluene and 1,3,5-trinitro-1,3,5-triazine (RDX) exposure to the northern bobwhite (Colinus virginianus). Environ. Toxicol. Chem. 26: 1481-1487.   DOI   ScienceOn
52 Kitts, C. L., D. P. Cunningham, and P. J. Unkefer. 1994. Isolation of 3 hexahydro-1,3,5-trinitro-1,3,5-triazine-degrading species of the family Enterobacteriaceae from nitramine explosivecontaminated soil. Appl. Environ. Microbiol. 60: 4608-4611.
53 Juhasz, A. L. and R. Naidu. 2007. Explosives: Fate, dynamics, and ecological impact in terrestrial and marine environments. Rev. Environ. Contam. Toxicol. 191: 163-215.
54 Kalderis, D., A. L. Juhasz, R. Boopathy, and S. Comfort. 2011. Soils contaminated with explosives: Environmental fate and evaluation of state-of the-art remediation processes (IUPAC Technical Report). Pure Appl. Chem. 83: 1407-1484.   DOI   ScienceOn
55 Kitts, C. L., C. E. Green, R. A. Otley, M. A. Alvarez, and P. J. Unkefer. 2000. Type I nitroreductases in soil enterobacteria reduce TNT (2,4,6-trinitrotoluene) and RDX (hexahydro-1,3,5- trinitro-1,3,5-triazine). Can. J. Microbiol. 46: 278-282.   DOI   ScienceOn
56 Kwon, M. J. and K. T. Finneran. 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: 705-715.   DOI   ScienceOn
57 Kwon, M. J. and K. T. Finneran. 2009. Hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) reduction is concurrently mediated by direct electron transfer from hydroquinones and resulting biogenic Fe(II) formed during electron shuttle amended biodegradation. Environ. Eng. Sci. 26: 961-971.   DOI   ScienceOn
58 Lee, S. Y. and B. W. Brodman. 2004. Biodegradation of 1,3,5-trinitro-1,3,5-triazine (RDX). J. Environ. Sci. Health A 39: 61-75.   DOI   ScienceOn
59 Lotufo, G. R., A. B. Gibson, and J. L. Yoo. 2010. Toxicity and bioconcentration evaluation of RDX and HMX using sheepshead minnows in water exposures. Ecotoxicol. Environ. Saf. 73: 1653-1657.   DOI   ScienceOn
60 Lee, T. K., J. J. Lee, W. J. Sul, S. Iwai, B. Chai, J. M. Tiedje, and J. H. Park. 2011. Novel biphenyl-oxidizing bacteria and dioxygenase genes from a Korean tidal mudflat. Appl. Environ. Microbiol. 77: 3888-3891.   DOI   ScienceOn
61 McFarland, C. A., M. J. Quinn Jr., M. A. Bazar, L. G. Talent, and M. S. Johnson. 2009. Toxic effects of oral hexahydro-1,3,5-trinitro-1,3,5-triazine in the western fence lizard (Sceloporus occidentalis). Environ. Toxicol. 28: 1043-1050.   DOI   ScienceOn
62 Fuller, M. E., K. McClay, J. Hawari, L. Paquet, T. E. Malone, B. G. Fox, and R. J. Steffan. 2009. Transformation of RDX and other energetic compounds by xenobiotic reductases XenA and XenB. Appl. Microbiol. Biotechnol. 84: 535-544.   DOI   ScienceOn
63 Fuller, M. E., N. Perreault, and J. Hawari. 2010. Microaerophilic degradation of hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) by three Rhodococcus strains. Letter Appl. Microbiol. 51: 313-318.   DOI   ScienceOn
64 Gallagher, E. M., L. Y. Young, L. M. McGuinness, and L. J. Kerkhof. 2010. Detection of 2,4,6-trinitrotoluene-utilizing anaerobic bacteria by 15N and 13C incorporation. Appl. Environ. Microbiol. 76: 1695-1698.   DOI   ScienceOn
65 George, S. E., G. Huggins-Clark, and L. R. Brooks. 2001. Use of a Salmonella microsuspension bioassay to detect the mutagenicity of munitions compounds at low concentrations. Mut. Res. 490: 45-56.   DOI   ScienceOn
66 Glover, D. J. and J. C. Hoffsommer. 1979. Photolysis of RDX. Identification and reactions of products. Technical Report NSWC TR-79-349. Naval Surface Weapons Centre, Silver Spring, MD.
67 Halasz, A., N. C. Bruce, and J. Hawari. 2010. Biodegradation of RDX and MNX with Rhodococcus sp. strain DN22: New insights into the degradation pathway. Environ. Sci. Technol. 44: 9330-9336.   DOI   ScienceOn
68 Gregory, K. B., P. Larese-Casanova, G. F. Parkin, and M. M. Scherer. 2004. Abiotic transformation of hexahydro-1,3,5-trinitro-1,3,5-triazine by fell bound to magnetite. Environ. Sci. Technol. 38: 1408-1414.   DOI   ScienceOn
69 Gust, K. A., M. S. Wilbanks, X. Guan, M. Piroozni, T. Habib, L. Yoo, et al. 2011. Investigations of transcript expression in fathead minnow (Pimephales promelas) brain tissue reveal toxicological impacts of RDX exposure. Aqua. Toxicol. 101: 135-145.   DOI   ScienceOn
70 Halasz, A. and J. Hawari. 2011. Degradation Routes of RDX in various redox systems. ACS Symp. Ser. 1071: 441-462.
71 Harris, G. 2011. Government says 2 common materials pose risk of cancer. New York Times. Retrieved 2011-06-11.
72 Hawari, J., A. Halasz, T. Sheremata, S. Beaudet, C. Groom, L. Paquet, et al. 2000. Characterization of metabolites during biodegradation of hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) with municipal anaerobic sludge. Appl. Environ. Microbiol. 66: 2652-2657.   DOI   ScienceOn
73 Hawari, J., S. Beaudet, A. Halasz, S. Thiboutot, and G. Ampleman. 2000. Microbial degradation of explosive; biotransformation versus mineralization. Appl. Microbiol. Biotechnol. 54: 605-618.   DOI   ScienceOn
74 Hazen, T. C., R. Chakraborty, I. R. Gregory, J. P. Bowman, L. Jimenez, D. Zhang, et al. 2009. Use of gene probes to access the impact and effectiveness of aerobic in situ bioremediation of TCE and PCE. Arch. Microbiol. 191: 221-232.   DOI   ScienceOn
75 Best, E. P. H., K. N. Geter, H. E. Tatem, and B. K. Lane. 2006. Effects, transfer, and fate of RDX from aged soil in plants and worms. Chemosphere 62: 616-625.   DOI   ScienceOn
76 Indest, K. J., C. M. Jung, H. P. Chen, D. Hancock, C. Florizone, L. D. Eltis, and F. H. Crocker. 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: 6329-6337.   DOI   ScienceOn
77 Agency for Toxic Substances and Disease Registry (ATSDR). 2010. Division of Toxicology and Environmental Medicine/Applied Toxicology Branch 1600 Clifton Road NE Mailstop F-62 Atlanta, Georgia 30333 (http://www.atsdr.cdc.gov).
78 Bayman, P., S. D. Ritchey, and J. W. Bennett. 1995. Fungal interactions with the explosive RDX (hydroxylamino-dinitroso- 1,3,5-triazine). J. Ind. Microbiol. 15: 418-423.   DOI   ScienceOn
79 Bhatt, M., J. S. Zhao, A. Halasz, and J. Hawari. 2006. Biodegradation of hexahydro-1,3,5-trinitro-1,3,5-triazine by novel fungi isolated from unexploded ordnance contaminated marine sediment. J. Ind. Microbiol. Biotechnol. 33: 850-858.   DOI   ScienceOn
80 Bhushan, B., A. Halasz, J. Spain, S. Thiboutot, G. Ampleman, and J. Hawari. 2002. Biotransformation of hexahydro-1,3,5-trinitro-1,3,5-triazine catalyzed by a NAD(P)H: Nitrate oxidoreductase from Aspergillus niger. Environ. Sci. Technol. 36: 3104-3108.   DOI   ScienceOn
81 Bhushan, B., A. Halasz, S. Thiboutot, G. Ampleman, and J. Hawari. 2004. Chemotaxis-mediated biodegradation of cyclic nitramine explosives RDX, HMX, and CL-20 by Clostridium sp. EDB2. Biochem. Biophys. Res. Commun. 316: 816-821.   DOI   ScienceOn