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

Applied and Environmental Microbiology

Volumn 76, Issue 19, 2010, Pages 6329-6337

  Indest, Karl J ^a   Jung, Carina M ^a   Chen, Hao Ping ^b   Hancock, Dawn ^a   Florizone, Christine ^b   Eltis, Lindsay D ^a   Crocker, Fiona H ^a  

^a U S ARMY ENGINEER RESEARCH AND DEVELOPMENT CENTER   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; BACTERIAL CELLS; CYTOCHROME P450; CYTOCHROMES P450; FUNCTIONAL CHARACTERIZATION; FUSION PROTEINS; GORDONIA SP; INORGANIC NITROGEN; NITRAMINES; NITROGEN METABOLISM; NITROGEN SOURCES; QUANTITATIVE REAL TIME PCR; RDX DEGRADATION; RHODOCOCCUS; SYNTHASES; TRANSCRIPT LEVEL; UP-REGULATION;

AMINO ACIDS; AMMONIUM COMPOUNDS; ENCODING (SYMBOLS); ESCHERICHIA COLI; EXPLOSIVES; GENES; MICROBIOLOGY; NITROGEN;

DEGRADATION;

BACTERIAL DNA; BACTERIAL PROTEIN; CYCLONITE; NITRATE; NITRITE; QUATERNARY AMMONIUM DERIVATIVE; RECOMBINANT PROTEIN; TRIAZINE DERIVATIVE;

AMINO ACID; AMMONIUM; BACTERIUM; CYTOCHROME; DEGRADATION; DICOTYLEDON; EXPLOSIVE; GENE; GROWTH RATE; METABOLISM; MICROBIAL COMMUNITY; NITRITE; NITROGEN; PLASMID; POLYMERASE CHAIN REACTION; PROTEIN; REAL TIME; TRANSFORMATION;

ARTICLE; BACTERIAL GENE; BIOTRANSFORMATION; CHEMISTRY; DNA SEQUENCE; ESCHERICHIA COLI; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GRAM POSITIVE BACTERIUM; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PLASMID; SEQUENCE HOMOLOGY;

BACTERIAL PROTEINS; BIOTRANSFORMATION; DNA, BACTERIAL; ESCHERICHIA COLI; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENES, BACTERIAL; GRAM-POSITIVE BACTERIA; METABOLIC NETWORKS AND PATHWAYS; MOLECULAR SEQUENCE DATA; NITRATES; NITRITES; PLASMIDS; QUATERNARY AMMONIUM COMPOUNDS; RECOMBINANT PROTEINS; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; TRIAZINES;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; GORDONIA SP.; RHODOCOCCUS; RHODOCOCCUS JOSTII;

EID: 78049247494     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01217-10     Document Type: Article

References (56)

1. 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.
2. Adrian, N. R., C. M. Arnett, and R. F. Hickey. 2003. Stimulating the anaerobic biodegradation of explosives by the addition of hydrogen or electron donors that produce hydrogen. Water Res. 37:3499-3507.
3. Andeer, P. F., D. A. Stahl, N. C. Bruce, and S. E. Strand. 2009. Lateral transfer of genes for hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) degradation. Appl. Environ. Microbiol. 75:3258-3262.
4. Arenskotter, M., D. Broker, and A. Steinbüchel. 2004. Biology of the metabolically diverse genus Gordonia. Appl. Environ. Microbiol. 70:3195-3204.
5. Aziz, R. K., D. Bartels, A. A. Best, M. DeJongh, T. Disz, R. A. Edwards, K. Formsma, S. Gerdes, E. M. Glass, M. Kubal, F. Meyer, G. J. Olsen, R. Olson, A. L. Osterman, R. A. Overbeek, L. K. McNeil, D. Paarmann, T. Paczian, B. Parrello, G. D. Pusch, C. Reich, R. Stevens, O. Vassieva, V. Vonstein, A. Wilke, and O. Zagnitko. 2008. The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75.
6. Balkwill, D. L., and W. C. Ghiorse. 1985. Characterization of subsurface bacteria associated with two shallow aquifers in Oklahoma. Appl. Environ. Microbiol. 50:580-588.
7. Bauchop, T., and S. R. Elsden. 1960. The growth of micro-organisms in relation to their energy supply. J. Gen. Microbiol. 23:457-469.
8. Behrens, S., M. F. Azizian, P. J. McMurdie, A. Sabalowsky, M. E. Dolan, L. Semprini, and A. M. Spormann. 2008. Monitoring abundance and expression of "Dehalococcoides" species chloroethene-reductive dehalogenases in a tetrachloroethene-dechlorinating flow column. Appl. Environ. Microbiol. 74:5695-5703.
9. Beller, H. R. 2002. Anaerobic biotransformation of RDX (hexahydro-1,3,5- trinitro-1,3,5-triazine) by aquifer bacteria using hydrogen as the sole electron donor. Water Res. 36:2533-2540.
10. Bhushan, B., S. Trott, J. C. Spain, A. Halasz, L. Paquet, and J. Hawari. 2003. 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. 69:1347-1351.
11. Boopathy, R., M. Gurgas, J. Ullian, and J. F. Manning. 1998. Metabolism of explosive compounds by sulfate-reducing bacteria. Curr. Microbiol. 37:127-131.
12. Bradley, P. M., and R. S. Dinicola. 2005. RDX (hexahydro-1,3,5-trinitro- 1,3,5-triazine) biodegradation in aquifer sediments under manganese-reducing conditions. Bioremediat. J. 9:1-8.
13. Broker, D., M. Arenskotter, A. Legatzki, D. H. Nies, and A. Steinbüchel. 2004. Characterization of the 101-kilobase-pair megaplasmid pKB1, isolated from the rubber-degrading bacterium Gordonia westfalica Kb1. J. Bacteriol. 186:212-225.
14. Bryant, C., and M. DeLuca. 1991. Purification and characterization of an oxygen-insensitive NAD(P)H nitroreductase from Enterobacter cloacae. J. Biol. Chem. 266:4119-4125.
15. Clausen, J., J. Robb, D. Curry, and N. Korte. 2004. A case study of contaminants on military ranges: Camp Edwards, Massachusetts, U.S.A. Environ. Pollut. 129:13-21.
16. Coleman, N. V., D. R. Nelson, and T. Duxbury. 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. 30:1159-1167.
17. Crocker, F. H., K. J. Indest, and H. L. Fredrickson. 2006. Biodegradation of the cyclic nitramine explosives RDX, HMX, and CL-20. Appl. Microbiol. Biotechnol. 73:274-290.
18. Crocker, F. H., K. T. Thompson, J. E. Szecsody, and H. L. Fredrickson. 2005. Biotic and abiotic degradation of CL-20 and RDX in soils. J. Environ. Qual. 34:2208-2216.
19. Davis, J. L., A. H. Wani, B. R. O'Neal, and L. D. Hansen. 2004. RDX biodegradation column study: comparison of electron donors for biologically induced reductive transformation in groundwater. J. Hazard. Mater. 112:45-54.
20. Donovan, C., A. Schwaiger, R. Kramer, and M. Bramkamp. 2010. Subcellular localization and characterization of the ParAB system from Corynebacterium glutamicum. J. Bacteriol. 192:3441-3451.
21. 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.
22. Freedman, D. L., and K. W. Sutherland. 1998. Biodegradation of hexahydro- 1,3,5-trinitro-1,3,5-triazine (RDX) under nitrate-reducing conditions. Water Sci. Technol. 38:33-40.
23. 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.
24. Hawari, J., A. Halasz, T. Sheremata, S. Beaudet, C. Groom, L. Paquet, C. Rhofir, G. Ampleman, and S. Thiboutot. 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.
25. Indest, K. J., F. H. Crocker, and R. Athow. 2007. A TaqMan polymerase chain reaction method for monitoring RDX-degrading bacteria based on the xplA functional gene. J. Microbiol. Methods 68:267-274.
26. T). Stand. Genomic Sci. 2:1.2010.
27. 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. U. S. A. 104:16822-16827.
28. Jenkins, T. F., M. E. Walsh, P. G. Thorne, P. H. Miyares, T. A. Ranney, C. L. Grant, and J. R. Esparza. 1998. Site characterization for explosives contamination at a military firing range impact area. U.S. Army Cold Regions Research and Engineering Laboratory. Special report 98-9. U.S. Army Cold Regions Research and Engineering Laboratory, Hanover, NH.
29. Kim, Y. H., I. Kang, H. Bergeron, P. C. Lau, K. H. Engesser, and S. J. Kim. 2006. Physiological, biochemical, and genetic characterization of an alicyclic amine-degrading Mycobacterium sp. strain THO100 isolated from a morpholinecontaining culture of activated sewage sludge. Arch. Microbiol. 186:425-434.
30. 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.
31. Langille, M. G., W. W. Hsiao, and F. S. Brinkman. 2008. Evaluation of genomic island predictors using a comparative genomics approach. BMC Bioinformatics 9:329.
32. Lee, P. K., T. W. Macbeth, K. S. Sorenson, Jr., R. A. Deeb, and L. Alvarez- Cohen. 2008. Quantifying genes and transcripts to assess the in situ physiology of "Dehalococcoides" spp. in a trichloroethene-contaminated groundwater site. Appl. Environ. Microbiol. 74:2728-2739.
33. Maniatis, T., J. Sambrook, and E. F. Fritsch. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
34. McLeod, M. P., R. L. Warren, W. W. Hsiao, N. Araki, M. Myhre, C. Fernandes, D. Miyazawa, W. Wong, A. L. Lillquist, D. Wang, M. Dosanjh, H. Hara, A. Petrescu, R. D. Morin, G. Yang, J. M. Stott, J. E. Schein, H. Shin, D. Smailus, A. S. Siddiqui, M. A. Marra, S. J. Jones, R. Holt, F. S. Brinkman, K. Miyauchi, M. Fukuda, J. E. Davies, W. W. Mohn, and L. D. Eltis. 2006. The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse. Proc. Natl. Acad. Sci. U. S. A. 103:15582-15587.
35. Nakashima, N., and T. Tamura. 2004. Isolation and characterization of a rolling-circle-type plasmid from Rhodococcus erythropolis and application of the plasmid to multiple-recombinant-protein expression. Appl. Environ. Microbiol. 70:5557-5568. (Pubitemid 39279634)
36. Nejidat, A., L. Kafka, Y. Tekoah, and Z. Ronen. 2008. Effect of organic and inorganic nitrogenous compounds on RDX degradation and cytochrome P-450 expression in Rhodococcus strain YH1. Biodegradation 19:313-320.
37. Park, J. W., and D. E. Crowley. 2006. Dynamic changes in nahAc gene copy numbers during degradation of naphthalene in PAH-contaminated soils. Appl. Microbiol. Biotechnol. 72:1322-1329.
38. Pennington, J. C., T. F. Jenkins, S. Thiboutot, G. Ampleman, J. Clausen, A. D. Hewitt, J. Lewis, M. E. Walsh, T. A. Ranney, B. Silverblatt, A. Marois, A. Gagnon, P. Brousseau, J. E. Zufelt, K. Poe, M. Bouchard, R. Martel, D. D. Walker, C. A. Ramsey, C. A. Hayes, S. L. Yost, K. L. Bjella, L. Trepanier, T. E. Berry, D. J. Lambert, P. Dubé, and N. M. Perron. 2005. Distribution and fate of energetics on DoD test and training ranges: report 5. U.S. Army Engineer Research and Development Center. ERDC TR-05-2. U.S. Army Engineer Research and Development Center, Vicksburg, MS.
39. Poupin, P., V. Ducrocq, S. Hallier-Soulier, and N. Truffaut. 1999. Cloning and characterization of the genes encoding a cytochrome P450 (PipA) involved in piperidine and pyrrolidine utilization and its regulatory protein (PipR) in Mycobacterium smegmatis mc2155. J. Bacteriol. 181:3419-3426.
40. Ramakers, C. J., R. H. Uijter, R. H. Eprez, and A. F. Oorman. 2003. Assumption- free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339:62-66.
41. 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 15Nstable isotope probing. Environ. Sci. Technol. 43:2505-2511.
42. Rylott, E. L., R. G. Jackson, J. Edwards, G. L. Womack, H. M. Seth-Smith, D. A. Rathbone, S. E. Strand, and N. C. Bruce. 2006. An explosive-degrading cytochrome P450 activity and its targeted application for the phytoremediation of RDX. Nat. Biotechnol. 24:216-219.
43. Sabbadin, F., R. Jackson, K. Haider, G. Tampi, J. P. Turkenburg, S. Hart, N. C. Bruce, and G. Grogan. 2009. The 1.5-A structure of XplA-heme, an unusual cytochrome P450 heme domain that catalyzes reductive biotransformation of royal demolition explosive. J. Biol. Chem. 284:28467-28475.
44. Schafer, A., A. Tauch, W. Jager, J. Kalinowski, G. Thierbach, and A. Puhler. 1994. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145:69-73.
45. Seth-Smith, H. M., 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.
46. Seth-Smith, H. M., S. J. Rosser, A. Basran, E. R. Travis, E. R. Dabbs, S. Nicklin, and N. C. Bruce. 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. 68:4764-4771.
47. Seto, M., K. Kimbara, M. Shimura, T. Hatta, M. Fukuda, and K. Yano. 1995. A novel transformation of polychlorinated biphenyls by Rhodococcus sp. strain RHA1. Appl. Environ. Microbiol. 61:3353-3358.
48. Sherburne, L. A., J. D. Shrout, and P. J. Alvarez. 2005. Hexahydro-1,3,5- trinitro-1,3,5-triazine (RDX) degradation by Acetobacterium paludosum. Biodegradation 16:539-547.
49. Sheremata, T. W., A. Halasz, L. Paquet, S. Thiboutot, G. Ampleman, and J. Hawari. 2001. The fate of the cyclic nitramine explosive RDX in natural soil. Environ. Sci. Technol. 35:1037-1040.
50. Shrout, J. D., P. Larese-Casanova, M. M. Scherer, and P. J. Alvarez. 2005. Sustained and complete hexahydro-1,3,5-trinitro-1,3,5-triazine (RDX) degradation in zero-valent iron simulated barriers under different microbial conditions. Environ. Technol. 26:1115-1126.
51. Sielaff, B., and J. R. Andreesen. 2005. Analysis of the nearly identical morpholine monooxygenase-encoding mor genes from different Mycobacterium strains and characterization of the specific NADH:ferredoxin oxidoreductase of this cytochrome P450 system. Microbiology 151:2593-2603.
52. 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.
53. van der Geize, R., G. I. Hessels, R. van Gerwen, P. van der Meijden, and L. Dijkhuizen. 2001. Unmarked gene deletion mutagenesis of kstD, encoding 3-ketosteroid delta1-dehydrogenase, in Rhodococcus erythropolis SQ1 using sacB as counter-selectable marker. FEMS Microbiol. Lett. 205:197-202.
54. Vindal, V., K. Suma, and A. Ranjan. 2007. GntR family of regulators in Mycobacterium smegmatis: a sequence and structure based characterization. BMC Genomics 8:289.
55. Walsh, M. E., C. M. Collins, C. H. Racine, T. F. Jenkins, A. B. Gelvin, and T. A. Ranney. 2010. Sampling for explosive residues at Fort Greely, Alaska: reconnaissance visit July 2000. U.S. Army Cold Regions Research and Engineering Laboratory. ERDC/CRREL TR-01-15. U.S. Army Cold Regions Research and Engineering Laboratory, Hanover, NH.
56. Zhao, J. S., J. Spain, S. Thiboutot, G. Ampleman, C. Greer, and J. Hawari. 2004. Phylogeny of cyclic nitramine-degrading psychrophilic bacteria in marine sediment and their potential role in the natural attenuation of explosives. FEMS Microbiol. Ecol. 49:349-357.