engineered for complete toluene degradation facilitates Cr(VI) reduction Free

Abstract

Toluene and other fuel hydrocarbons are commonly found in association with radionuclides at numerous US Department of Energy sites, frequently occurring together with Cr(VI) and other heavy metals. In this study, the extremely radiation-resistant bacterium , which naturally reduces Cr(VI) to the less mobile and less toxic Cr(III), was engineered for complete toluene degradation by cloned expression of and genes of . The recombinant Tod/Xyl strain showed incorporation of carbon from C-labelled toluene into cellular macromolecules and carbon dioxide, in the absence or presence of chronic ionizing radiation. The engineered bacteria were able to oxidize toluene under both minimal and complex nutrient conditions, and recombinant cells reduced Cr(VI) in sediment microcosms. As such, the Tod/Xyl strain could provide a model for examining the reduction of metals coupled to organic contaminant oxidation in aerobic radionuclide-contaminated sediments.

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2006-08-01
2024-03-29
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References

  1. Aemprapa S, William P. A. 1998; Implications of the xylQ gene of TOL plasmid pWW102 for the evolution of aromatic catabolic pathways. Microbiology 144:1387–1396 [CrossRef]
    [Google Scholar]
  2. Albarran G, Schuler R. H. 2002; Micellar electrophoretic capillary chromatographic analysis of the products produced in the radiolytic oxidation of toluene and phenol. Radiat Phys Chem 63:661–663 [CrossRef]
    [Google Scholar]
  3. Balkwill D. L, Reeves R. H, Drake G. R, Reeves J. Y, Crocker F. H, Baldwin-King M, Boone D. R. 1997; Phylogenetic characterization of bacteria in the subsurface microbial culture collection. FEMS Microbiol Rev 20:201–216 [CrossRef]
    [Google Scholar]
  4. Brim H, McFarlan S. C, Fredrickson J. K, Minton K. W, Zhai M, Wackett L. P, Daly M. J. 2000; Engineering Deinococcus radiodurans for metal remediation in radioactive mixed waste environments. Nat Biotechnol 18:85–90 [CrossRef]
    [Google Scholar]
  5. Brim H, Venkateswaran A, Kostandarithes H. M, Fredrickson J. K, Daly M. J. 2003; Engineering Deinococcus geothermalis for bioremediation of high-temperature radioactive waste environments. Appl Environ Microbiol 69:4575–4582 [CrossRef]
    [Google Scholar]
  6. Collinsworth W. L, Chapman P. J, Dagley S. 1973; Stereospecific enzymes in the degradation of aromatic compounds by Pseudomonas putida . J Bacteriol 113:922–931
    [Google Scholar]
  7. Costura R. K, Alvarez P. J. 2000; Expression and longevity of toluene dioxygenase in Pseudomonas putida F1 grown at different dissolved oxygen concentrations. Water Res 34:3014–3018 [CrossRef]
    [Google Scholar]
  8. Dagley S, Gibson D. T. 1965; The bacterial degradation of catechol. Biochem J 95:466–474
    [Google Scholar]
  9. Daly M. J. 2000; Engineering radiation-resistant bacteria for environmental biotechnology. Curr Opin Biotechnol 11:280–285 [CrossRef]
    [Google Scholar]
  10. Daly M. J, Minton K. W. 1996; An alternative pathway of recombination of chromosomal fragments precedes recA -dependent recombination in the radioresistant bacterium Deinococcus radiodurans . J Bacteriol 178:4461–4471
    [Google Scholar]
  11. Daly M. J, Gaidamakova E. K, Matrosova V. Y. 10 other authors 2004; Accumulation of Mn(II) in Deinococcus radiodurans facilitates gamma-radiation resistance. Science 306:1025–1028 [CrossRef]
    [Google Scholar]
  12. Eary L. D, Rai D. 1987; Kinetics of chromium (III) oxidation to chromium (VI) by reaction with manganese dioxide. Environ Sci Technol 21:1187–1193 [CrossRef]
    [Google Scholar]
  13. Finette B. A, Gibson D. T. 1988; Initial studies on the regulation of toluene degradation by Pseudomonas putida F1. Biocatalysis 2:29–37 [CrossRef]
    [Google Scholar]
  14. Forster-Fromme K, Jendrossek D. 2005; Malate : quinone oxidoreductase (MqoB) is required for growth on acetate and linear terpenes in Pseudomonas citronellolis . FEMS Microbiol Lett 246:25–31 [CrossRef]
    [Google Scholar]
  15. Fredrickson J. K, Brockman F. J, Bjornstad B. N. 7 other authors 1993; Microbiological characteristics of pristine and contaminated deep vadose sediments from an arid region. Geomicrobiol J 11:95–107 [CrossRef]
    [Google Scholar]
  16. Fredrickson J. K, Kostandarithes H. M, Li S. W, Plymale A. E, Daly M. J. 2000; Reduction of Fe(III), Cr(VI), U(VI), and Tc(VII) by Deinococcus radiodurans R1. Appl Environ Microbiol 66:2006–2011 [CrossRef]
    [Google Scholar]
  17. Fredrickson J. K, Zachara J. M, Balkwill D. L, Kennedy D, Li S. M, Kostandarithes H. M, Brockman F. J, Daly M, J, Romine M. F. 2004; Geomicrobiology of high-level nuclear waste-contaminated vadose sediments at the Hanford site, Washington state. Appl Environ Microbiol 70:4230–4241 [CrossRef]
    [Google Scholar]
  18. Ghosal D, Omelchenko M. V, Gaidamakova E. K. 10 other authors 2005; How radiation kills cells: survival of Deinococcus radiodurans and Shewanella oneidensis under oxidative stress. FEMS Microbiol Rev 29:361–375
    [Google Scholar]
  19. Gibson D. T, Hensley M, Yoshioka H, Marby T. J. 1970; Formation of (+)- cis -2,3-dihydroxy-1-methylcyclohexa-4,6-diene from toluene by Pseudomonas putida . Biochemistry 9:1626–1630 [CrossRef]
    [Google Scholar]
  20. Hanson R. S, Phillips J. A. 1981 Manual of Methods for General Bacteriology Washington, DC: American Society for Microbiology;
    [Google Scholar]
  21. Harayama S, Rekik M. 1990; The meta cleavage operon of TOL degradative plasmid pWW0 comprises 13 genes. Mol Gen Genet 221:113–120 [CrossRef]
    [Google Scholar]
  22. Haro M. A, de Lorenzo V. 2001; Metabolic engineering of bacteria for environmental applications: construction of Pseudomonas strains for biodegradation of 2-chlorotoluene. J Biotechnol 85:103–113 [CrossRef]
    [Google Scholar]
  23. Horn J. M, Harayama S, Timmis K. N. 1991; DNA sequence determination of the TOL plasmid (pWWO) xylGFJ genes of Pseudomonas putida : implications for the evolution of aromatic catabolism. Mol Microbiol 5:2459–2474 [CrossRef]
    [Google Scholar]
  24. Hugouvieux-Cotte-Pattat N, Kohler T, Rekik M, Harayama S. 1990; Growth-phase-dependent expression of the Pseudomonas putida TOL plasmid pWW0 catabolic genes. J Bacteriol 172:6651–6660
    [Google Scholar]
  25. Kukor J. J, Olsen R. H. 1996; Catechol 2,3-dioxygenases functional in oxygen-limited (hypoxic) environments. Appl Environ Microbiol 62:1728–1740
    [Google Scholar]
  26. Lange C, Wackett L. P, Minton K. W, Daly M. J. 1998; Engineering a recombinant Deinococcus radiodurans for organopollutant degradation in radioactive mixed waste environments. Nat Biotechnol 16:929–933 [CrossRef]
    [Google Scholar]
  27. Lipton M. S, Anderson G. A, Pasa-Tolić L. 18 other authors 2002; Global analysis of the Deinococcus radiodurans proteome using accurate mass tags. Proc Natl Acad Sci U S A 99:11049–11054 [CrossRef]
    [Google Scholar]
  28. Liu Y, Zhou J, Omelchenko M. V. 12 other authors 2003; Transcriptome dynamics of Deinococcus radiodurans recovering from ionizing radiation. Proc Natl Acad Sci U S A 100:4191–4196 [CrossRef]
    [Google Scholar]
  29. Lovley D. R, Coates J. D. 1997; Bioremediation of metal contamination. Curr Opin Biotechnol 8:285–289 [CrossRef]
    [Google Scholar]
  30. Macilwain C. 1996; Science seeks weapons clean-up role. Nature 383:375–379 [CrossRef]
    [Google Scholar]
  31. Makarova K. S, Aravind L, Wolf Y. I, Tatusov R. L, Minton K. W, Koonin E. V, Daly M. J. 2001; Genome of the extremely radiation-resistant bacterium Deinococcus radiodurans viewed from the perspective of comparative genomics. Microbiol Mol Biol Rev 65:44–79 [CrossRef]
    [Google Scholar]
  32. McCullough J, Hazen T. C, Benson S. M, Blaine-Metting F, Palmisano A. C. 2003 Bioremediation of Metals and Radionuclides, 2nd edn.. Germantown, MD: US Department of Energy, Office of Biological and Environmental Research;
    [Google Scholar]
  33. Omelchenko M. V, Wolf Y. I, Gaidamakova E. K, Matrosova V. Y, Valisenko A, Zhai M, Daly M. J, Makarova K. S. 2005; Comparative genomics of Thermus thermophilus and Deinococcus radiodurans : divergent routes of adaptation to thermophily and radiation resistance. BMC Evol Biol 5:57–79 [CrossRef]
    [Google Scholar]
  34. Riley R. G, Zachara J. M, Wobber F. J. 1992 Chemical Contaminants on DOE Lands and Selection of Contaminant Mixtures for Subsurface Science Research Washington, DC: US Department of Energy, Office of Energy Research, Subsurface Science Program;
    [Google Scholar]
  35. Ripp S, Sayler G. S. 2002; Field release of genetically engineered microorganisms (GEM). The Encyclopedia of Environmental Microbiology pp  1278–1287 New York: Wiley;
    [Google Scholar]
  36. Saier M. H. Jr 2005; Beneficial bacteria and bioremediation. J Mol Microbiol Biotechnol 9:63–64 [CrossRef]
    [Google Scholar]
  37. Smith R. L. 1995 Manual of Environmental Microbiology pp  577–585 Washington, DC: American Society for Microbiology;
    [Google Scholar]
  38. Strong L. C, McTavish H, Sadowsky M. J, Wackett L. P. 2000; Field-scale remediation of atrazine-contaminated soil using recombinant Escherichia coli over-expressing atrazine chlorohydrolase. Environ Microbiol 2:91–98 [CrossRef]
    [Google Scholar]
  39. Sugden K. D, Campo C. K, Martin B. D. 2001; Direct oxidation of guanine and 7,8-dihydro-8-oxoguanine in DNA by a high-valent chromium complex: a possible mechanism for chromate genotoxicity. Chem Res Toxicol 14:1315–1322 [CrossRef]
    [Google Scholar]
  40. Swift R. J, Carter S. F, Widdowson D. A, Mason J. R, Leak D. J. 2001; Expression of benzene dioxygenase from Pseudomonas putida ML2 in cis-1,2-cyclohexanediol-degrading pseudomonads. Appl Microbiol Biotechnol 55:721–726 [CrossRef]
    [Google Scholar]
  41. Timmis K. N, Steffan R. J, Unterman R. 1994; Designing microorganisms for the treatment of toxic wastes. Annu Rev Microbiol 48:525–557 [CrossRef]
    [Google Scholar]
  42. Venkateswaran A, McFarlan S. C, Ghosal D, Minton K. W, Vasilenko A, Makarova K. S, Wackett L. P, Daly M. J. 2000; Physiologic determinants of radiation resistance in Deinococcus radiodurans . Appl Environ Microbiol 66:2620–2626 [CrossRef]
    [Google Scholar]
  43. Wackett L. P, Sadowsky M. J, Newman L. M, Hur H.-G, Li S. 1994; Metabolism of polyhalogenated compounds by a genetically engineered bacterium. Nature 368:627–629 [CrossRef]
    [Google Scholar]
  44. Watts K. T, Lee P. C, Schmidt-Dannert C. 2004; Exploring recombinant flavonoid biosynthesis in metabolically engineered Escherichia coli . Chembiochem 5:500–507 [CrossRef]
    [Google Scholar]
  45. Werner F. T, Walters J. E, Keefer G. B. 1997; Bioventing pilot test results at the low point drain area, Offutt AFB, Nebraska. Ann NY Acad Sci 829:313–325 [CrossRef]
    [Google Scholar]
  46. White O. J, Eisen A, Heidelberg J. F. 28 other authors 1999; Complete genome sequencing of the radioresistant bacterium Deinococcus radiodurans R1. Science 286:1571–1577 [CrossRef]
    [Google Scholar]
  47. Yamaguchi M, Fujisawa H. 1980; Purification and characterization of an oxygenase component in benzoate 1,2-dioxygenase system from Pseudomonas arvilla C-1. J Biol Chem 255:5058–5063
    [Google Scholar]
  48. Zylstra G. J, Gibson D. T. 1989; Toluene degradation by Pseudomonas putida F1. Nucleotide sequence of the todC1C2BADE genes and their expression in Escherichia coli . J Biol Chem 264:14940–14946
    [Google Scholar]
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