Abstract
The potential of trichloroethylene (TCE) to induce andnon-aromatic growth substrates to support TCE degradationin five strains (Pseudomonas mendocina KR1,Ralstonia pickettii PKO1, Pseudomonas putida F1,Burkholderia cepacia G4, B. cepacia PR1) oftoluene-oxidizing bacteria was examined. LB broth andacetate did not support TCE degradation in any of thewild-type strains. In contrast, fructose supported thehighest specific levels of TCE oxidation observed ineach of the strains tested, except B. cepacia G4. Wediscuss the potential mechanisms and implications ofthis observation. In particular, cells of P. mendocinaKR1 degraded significant amounts of TCE during cellgrowth on non-aromatic substrates. Apparently, TCEdegradation was not completely constrained by anygiven factor in this microorganism, as was observedwith P. putida F1 (TCE was an extremely poorsubstrate) or B. cepacia G4 (lack of oxygenaseinduction by TCE). Our results indicate that multiplephysiological traits are required to enable useful TCEdegradation by toluene-oxidizing bacteria in the absenceof aromatic cosubstrates. These traits include oxygenaseinduction, effective TCE turnover, and some level ofresistance to TCE mediated toxicity.
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References
Alvarez-Cohen L & McCarty PL (1991) Effects of toxicity, aeration, and reductant supply on trichloroethylene transformation by a mixed methanotrophic culture. Appl. Environ. Microbiol. 57: 228–235
Ampe F, Leonard D & Lindley ND (1998) Repression of phenol catabolism by organic acids in Ralstonia eutropha. Appl. Environ. Microbiol. 64: 1–6
Arp DJ (1995) Understanding the diversity of trichloroethylene cooxidations. Curr. Opin. Biotechnol. 6: 352–358
Carmona M, Rodriguez MJ, Martinez-Costa O & de Lorenzo V (2000) In vivo and in vitro effects of (p)ppGpp on the σ54 promoter Pu of the TOL plasmid of Pseudomonas putida. J. Bacteriol. 182: 4711–4718
Cases I & de Lorenzo V (2000) Genetic evidence of distinct physiological regulation mechanisms in the σ54 Pu promoter of Pseudomonas putida. J. Bacteriol. 182: 956–960
Cases I, Perez-Martin J & de Lorenzo V (1999) The IIANtr (PtsN) protein of Pseudomonas putida mediates the C source inhibition of the σ54-dependent Pu promoter of the TOL plasmid. J. Biol. Chem. 274: 15562–15568
Dahlen EP & Rittmann BE (2002a) A detailed analysis of the mechanisms controlling the acceleration of 2,4-DCP monooxygenation in the two-tank suspended growth process. Biodegradation 13: 117–130
Dahlen EP & Rittmann BE (2002b) Two-tank suspended growth process for accelerating the detoxification kinetics of hydrocarbons requiring initial monooxygenation reactions. Biodegradation 13: 101–116
Ensley BD (1991) Biochemical diversity of trichloroethylene metabolism. Annu. Rev. Microbiol. 45: 283–299
Folsom BR, Chapman PJ & Pritchard PH (1990) Phenol and trichloroethylene degradation by Pseudomonas cepacia G4: kinetics and interactions between substrates. Appl. Environ. Microbiol. 56: 1279–1285
Fox BG, Borneman JG, Wackett LP & Lipscomb JD (1990) Haloalkene oxidation by the soluble methane monooxygenase from Methylosinus trichosporium OB3b: mechanistic and environmental implications. Biochemistry 29: 6419–6427
Gornall AG, Bardawill CJ & David MM (1949) Determination of serum proteins by means of the Biuret reaction. J. Biol. Chem. 177: 751–766
Gossett JM (1987) Measurement of Henry's law constants for C1 and C2 chlorinated hydrocarbons. Environ. Sci. Technol. 21: 202–208
Heald S & Jenkins RO (1994) Trichloroethylene removal and oxidation toxicity mediated by toluene dioxygenase of Pseudomonas putida. Appl. Environ. Microbiol. 60: 4634–4637
Holtel A, Marques S, Mohler I, Jakubzik U & Timmis KN (1994) Carbon source-dependent inhibition of xyl operon during expression of the Pseudomonas putida TOL plasmid. J. Bacteriol. 176: 1773–1776
Hyman MR, Russell SA, Ely RL, Williamson KJ & Arp DJ (1995) Inhibition, inactivation, and recovery of ammonia-oxidizing activity in cometabolism of trichloroethylene by Nitrosomonas europaea. Appl. Environ. Microbiol. 61: 1480–1487
Landa AS, Sipkema EM, Weijma J, Beenackers AA, Dolfing J & Janssen DB (1994) Cometabolic degradation of trichloroethylene by Pseudomonas cepacia G4 in a chemostat with toluene as the primary substrate. Appl. Environ. Microbiol. 60: 3368–3374
Lange CC, Wackett LP, Minton KW & Daly MJ (1998) Engineering a recombinant Deinococcus radiodurans for organopollutant degradation in radioactive mixed waste environments. Nat. Biotechnol. 16: 929–933
Leahy JG, Byrne AM & Olsen RH (1996) Comparison of factors influencing trichloroethylene degradation by toluene-oxidizing bacteria. Appl. Environ. Microbiol. 62: 825–833
Li S & Wackett LP (1992) Trichloroethylene oxidation by toluene dioxygenase. Biochem. Biophys. Res. Commun. 185: 443–451
Mars AE, Houwing J, Dolfing J & Janssen DB (1996) Degradation of toluene and trichloroethylene by Burkholderia cepacia G4 in growth-limited fed-batch culture. Appl. Environ. Microbiol. 1996: 886–891
McClay K, Streger SH & Steffan RJ (1995) Induction of toluene oxidation activity in Pseudomonas mendocina KR1 and Pseudomonas sp. strain ENVPC5 by chlorinated solvents and alkanes. Appl. Environ. Microbiol. 61: 3479–3481
Newman LM & Wackett LP (1997) Trichloroethylene oxidation by purified toluene 2-monooxygenase: products, kinetics, and turnover-dependent inactivation. J. Bacteriol. 179: 90–96
Olsen RH, Kukor JJ & Kaphammer B (1994) A novel toluene-3-monooxygenase pathway cloned from Pseudomonas pickettii PKO1. J. Bacteriol. 176: 3749–3756
Santos PM, Blatny JM, DiBartolo I, Valla S & Zennaro E (2000) Physiological analysis of the expression of the styrene degradation gene cluster in Pseudomonas fluorescens. Appl. Environ. Microbiol. 66: 1305–1310
Shields MS, Montgomery SO, Cuskey SM, Chapman PJ & Pritchard PH (1991) Mutants of Pseudomonas cepacia G4 defective in catabolism of aromatic compounds and trichloroethylene. Appl. Environ. Microbiol. 57: 1935–1941
Shields MS & Reagin MJ (1992) Selection of a Pseudomonas cepacia strain constitutive for the degradation of trichloroethylene. Appl. Environ. Microbiol. 58: 3977–3983
Shingleton JT, Applegate BM, Nagel AC, Bienkowski PR & Sayler GS (1998) Induction of the tod operon by trichloroethylene in Pseudomonas putida TVA8. Appl. Environ. Microbiol. 64: 5049–5052
Strand SE, Bjelland MD & Stensel HD (1990) Kinetics of chlorinated hydrocarbon degradation by suspended cultures of methaneoxidizing bacteria. Res. J. Wat. Poll. Control Fed. 62: 124–129
Studts JM, Mitchell KH, Pikus JD, McClay K, Steffan RJ & Fox BG (2000) Optimized expression and purification of toluene 4-monooxygenase hydroxylase. Protein Expr. Purif. 20: 58–65
Sze CC & Shingler V (1999) The alarmone (p)ppGpp mediates physiological-responsive control at the σ54-dependent Po promoter. Mol. Microbiol. 31: 1217–1228
Tover A, Ojangu EL & Kivisaar M (2001) Growth medium composition-determined regulatory mechanisms are superimposed on CatR-mediated transcription from the pheBA and catBCA promoters in Pseudomonas putida. Microbiology-(UK) 147: 2149–2156
van Hylckama Vlieg JET, De Koning W & Janssen DB (1997) Effect of chlorinated ethene conversion on viability and activity of Methylosinus trichosporium OB3b. Appl. Environ. Microbiol. 63: 4961–4964
Verdoni N, Aon M & Lebeault JM (1992) Metabolic and energetic control of Pseudomonas mendocina growth during transitions from aerobic to oxygen-limited conditions in chemostat cultures. Appl. Environ. Microbiol. 58: 3150–3156
Wackett LP & Gibson DT (1988) Degradation of trichloroethylene by toluene dioxygenase in whole-cell studies with Pseudomonas putida F1. Appl. Environ. Microbiol. 54: 1703–1708
Wackett LP & Householder SR (1989) Toxicity of trichloroethylene to Pseudomonas putida F1 is mediated by toluene dioxygenase. Appl. Environ. Microbiol. 55: 2727–2725
Winter RB, Yen KM & Ensley BD (1989) Efficient degradation of trichloroethylene by a recombinant Escherichia coli. Bio/Technology 7: 282–285
Yeager CM, Bottomley PJ & Arp DJ (2001) Cytotoxicity associated with trichloroethylene oxidation in Burkholderia cepacia G4. Appl. Environ. Microbiol. 67: 2107–2115
Yeager CM, Bottomley PJ, Arp DJ & Hyman MR (1999) Inactivation of toluene 2-monooxygenase in Burkholderia cepacia G4 by alkynes. Appl. Environ. Microbiol. 65: 632–639
Yuste L, Canosa I & Rojo F (1998) Carbon-source-dependent expression of the PalkB promoter from the Pseudomonas oleovorans alkane degradation pathway. J. Bacteriol. 180: 5218–5226
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Yeager, C.M., Arthur, K.M., Bottomley, P.J. et al. Trichloroethylene Degradation by Toluene-Oxidizing Bacteria Grown on Non-aromatic Substrates. Biodegradation 15, 19–28 (2004). https://doi.org/10.1023/B:BIOD.0000009947.09125.35
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DOI: https://doi.org/10.1023/B:BIOD.0000009947.09125.35