Abstract
The degradation of trichloroethylene (TCE) by toluene-oxidizing bacteria has been extensively studied, and yet the influence of environmental conditions and physiological characteristics of individual strains has received little attention. To consider these effects, the levels of TCE degradation by strains distinguishable on the basis of toluene and nitrate metabolism were compared under aerobic or hypoxic conditions in the presence and absence of nitrate and an exogenous electron donor, lactate. Under aerobic conditions with toluene-induced cells, strains expressing toluene dioxygenases (Pseudomonas putida F1, Pseudomonas sp. strain JS150, Pseudomonas fluorescens CFS215, and Pseudomonas sp. strain W31) degraded TCE at low rates, with less than 12% of the TCE removed in 18 h. In contrast, strains expressing toluene monooxygenases (Burkholderia cepacia G4, Burkholderia pickettii PKO1, and Pseudomonas mendocina KR1) degraded 36 to 67% of the TCE over the same period. Under hypoxic conditions (1.7 mg of dissolved oxygen per liter) or when lactate was added as an electron donor, the extent of TCE degradation by toluene-induced cells was generally lower. In the presence of lactate, degradation of TCE by denitrifying strain PKO1 was enhanced by nitrate under conditions in which dissimilatory nitrate reduction was observed. The results of experiments performed with strains F1, G4, PKO1, and KR1 suggested that TCE or an oxidation product induces toluene degradation and that TCE induces its own degradation in the monooxygenase strains. The role of TCE as an inducer of toluene oxygenase activity in PKO1 was confirmed by performing a promoter probe analysis, in which we found that TCE activates transcription from the PKO1 3-monooxygenase operon promoter.
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- Byrne A. M., Kukor J. J., Olsen R. H. Sequence analysis of the gene cluster encoding toluene-3-monooxygenase from Pseudomonas pickettii PKO1. Gene. 1995 Feb 27;154(1):65–70. doi: 10.1016/0378-1119(94)00844-i. [DOI] [PubMed] [Google Scholar]
- COHEN-BAZIRE G., SISTROM W. R., STANIER R. Y. Kinetic studies of pigment synthesis by non-sulfur purple bacteria. J Cell Physiol. 1957 Feb;49(1):25–68. doi: 10.1002/jcp.1030490104. [DOI] [PubMed] [Google Scholar]
- Dabrock B., Kesseler M., Averhoff B., Gottschalk G. Identification and characterization of a transmissible linear plasmid from Rhodococcus erythropolis BD2 that encodes isopropylbenzene and trichloroethene catabolism. Appl Environ Microbiol. 1994 Mar;60(3):853–860. doi: 10.1128/aem.60.3.853-860.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ensley B. D. Biochemical diversity of trichloroethylene metabolism. Annu Rev Microbiol. 1991;45:283–299. doi: 10.1146/annurev.mi.45.100191.001435. [DOI] [PubMed] [Google Scholar]
- Fan S., Scow K. M. Biodegradation of trichloroethylene and toluene by indigenous microbial populations in soil. Appl Environ Microbiol. 1993 Jun;59(6):1911–1918. doi: 10.1128/aem.59.6.1911-1918.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Folsom B. R., Chapman P. J., Pritchard P. H. Phenol and trichloroethylene degradation by Pseudomonas cepacia G4: kinetics and interactions between substrates. Appl Environ Microbiol. 1990 May;56(5):1279–1285. doi: 10.1128/aem.56.5.1279-1285.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gersberg R. M., Dawsey W. J., Bradley M. D. Biodegradation of monoaromatic hydrocarbons in groundwater under denitrifying conditions. Bull Environ Contam Toxicol. 1991 Aug;47(2):230–237. doi: 10.1007/BF01688645. [DOI] [PubMed] [Google Scholar]
- Ghiorse W. C., Wilson J. T. Microbial ecology of the terrestrial subsurface. Adv Appl Microbiol. 1988;33:107–172. doi: 10.1016/s0065-2164(08)70206-5. [DOI] [PubMed] [Google Scholar]
- Gibson D. T., Hensley M., Yoshioka H., Mabry T. J. Formation of (+)-cis-2,3-dihydroxy-1-methylcyclohexa-4,6-diene from toluene by Pseudomonas putida. Biochemistry. 1970 Mar 31;9(7):1626–1630. doi: 10.1021/bi00809a023. [DOI] [PubMed] [Google Scholar]
- Haigler B. E., Pettigrew C. A., Spain J. C. Biodegradation of mixtures of substituted benzenes by Pseudomonas sp. strain JS150. Appl Environ Microbiol. 1992 Jul;58(7):2237–2244. doi: 10.1128/aem.58.7.2237-2244.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Haigler B. E., Spain J. C. Biotransformation of nitrobenzene by bacteria containing toluene degradative pathways. Appl Environ Microbiol. 1991 Nov;57(11):3156–3162. doi: 10.1128/aem.57.11.3156-3162.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heald S., Jenkins R. O. Trichloroethylene removal and oxidation toxicity mediated by toluene dioxygenase of Pseudomonas putida. Appl Environ Microbiol. 1994 Dec;60(12):4634–4637. doi: 10.1128/aem.60.12.4634-4637.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hopkins G. D., Semprini L., McCarty P. L. Microcosm and in situ field studies of enhanced biotransformation of trichloroethylene by phenol-utilizing microorganisms. Appl Environ Microbiol. 1993 Jul;59(7):2277–2285. doi: 10.1128/aem.59.7.2277-2285.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hutchins S. R. Biodegradation of monoaromatic hydrocarbons by aquifer microorganisms using oxygen, nitrate, or nitrous oxide as the terminal electron acceptor. Appl Environ Microbiol. 1991 Aug;57(8):2403–2407. doi: 10.1128/aem.57.8.2403-2407.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johnson G. R., Olsen R. H. Nucleotide sequence analysis of genes encoding a toluene/benzene-2-monooxygenase from Pseudomonas sp. strain JS150. Appl Environ Microbiol. 1995 Sep;61(9):3336–3346. doi: 10.1128/aem.61.9.3336-3346.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Krumme M. L., Timmis K. N., Dwyer D. F. Degradation of trichloroethylene by Pseudomonas cepacia G4 and the constitutive mutant strain G4 5223 PR1 in aquifer microcosms. Appl Environ Microbiol. 1993 Aug;59(8):2746–2749. doi: 10.1128/aem.59.8.2746-2749.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Li S., Wackett L. P. Trichloroethylene oxidation by toluene dioxygenase. Biochem Biophys Res Commun. 1992 May 29;185(1):443–451. doi: 10.1016/s0006-291x(05)81005-8. [DOI] [PubMed] [Google Scholar]
- McClay K., Streger S. H., Steffan R. J. Induction of toluene oxidation activity in Pseudomonas mendocina KR1 and Pseudomonas sp. strain ENVPC5 by chlorinated solvents and alkanes. Appl Environ Microbiol. 1995 Sep;61(9):3479–3481. doi: 10.1128/aem.61.9.3479-3481.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mikesell M. D., Kukor J. J., Olsen R. H. Metabolic diversity of aromatic hydrocarbon-degrading bacteria from a petroleum-contaminated aquifer. Biodegradation. 1993;4(4):249–259. doi: 10.1007/BF00695973. [DOI] [PubMed] [Google Scholar]
- Mu D. Y., Scow K. M. Effect of trichloroethylene (TCE) and toluene concentrations on TCE and toluene biodegradation and the population density of TCE and toluene degraders in soil. Appl Environ Microbiol. 1994 Jul;60(7):2661–2665. doi: 10.1128/aem.60.7.2661-2665.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nelson M. J., Montgomery S. O., Mahaffey W. R., Pritchard P. H. Biodegradation of trichloroethylene and involvement of an aromatic biodegradative pathway. Appl Environ Microbiol. 1987 May;53(5):949–954. doi: 10.1128/aem.53.5.949-954.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nelson M. J., Montgomery S. O., Pritchard P. H. Trichloroethylene metabolism by microorganisms that degrade aromatic compounds. Appl Environ Microbiol. 1988 Feb;54(2):604–606. doi: 10.1128/aem.54.2.604-606.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Olsen R. H., Hansen J. Evolution and utility of a Pseudomonas aeruginosa drug resistance factor. J Bacteriol. 1976 Mar;125(3):837–844. doi: 10.1128/jb.125.3.837-844.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Olsen R. H., Kukor J. J., Kaphammer B. A novel toluene-3-monooxygenase pathway cloned from Pseudomonas pickettii PKO1. J Bacteriol. 1994 Jun;176(12):3749–3756. doi: 10.1128/jb.176.12.3749-3756.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Olsen R. H., Mikesell M. D., Kukor J. J. Enumeration and characterization of BTEX-degrading bacteria from hypoxic environments functional with mixed electron acceptors. Res Microbiol. 1994 Jan;145(1):47–49. doi: 10.1016/0923-2508(94)90068-x. [DOI] [PubMed] [Google Scholar]
- Page W. J., Sadoff H. L. Physiological factors affecting transformation of Azotobacter vinelandii. J Bacteriol. 1976 Mar;125(3):1080–1087. doi: 10.1128/jb.125.3.1080-1087.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rothmel R. K., Shinabarger D. L., Parsek M. R., Aldrich T. L., Chakrabarty A. M. Functional analysis of the Pseudomonas putida regulatory protein CatR: transcriptional studies and determination of the CatR DNA-binding site by hydroxyl-radical footprinting. J Bacteriol. 1991 Aug;173(15):4717–4724. doi: 10.1128/jb.173.15.4717-4724.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shields M. S., Montgomery S. O., Chapman P. J., Cuskey S. M., Pritchard P. H. Novel pathway of toluene catabolism in the trichloroethylene-degrading bacterium g4. Appl Environ Microbiol. 1989 Jun;55(6):1624–1629. doi: 10.1128/aem.55.6.1624-1629.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shields M. S., Montgomery S. O., Cuskey S. M., Chapman P. J., Pritchard P. H. Mutants of Pseudomonas cepacia G4 defective in catabolism of aromatic compounds and trichloroethylene. Appl Environ Microbiol. 1991 Jul;57(7):1935–1941. doi: 10.1128/aem.57.7.1935-1941.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shields M. S., Reagin M. J. Selection of a Pseudomonas cepacia strain constitutive for the degradation of trichloroethylene. Appl Environ Microbiol. 1992 Dec;58(12):3977–3983. doi: 10.1128/aem.58.12.3977-3983.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stanier R. Y., Palleroni N. J., Doudoroff M. The aerobic pseudomonads: a taxonomic study. J Gen Microbiol. 1966 May;43(2):159–271. doi: 10.1099/00221287-43-2-159. [DOI] [PubMed] [Google Scholar]
- Verdoni N., Aon M. A., Lebeault J. M. Metabolic and energetic control of Pseudomonas mendocina growth during transitions from aerobic to oxygen-limited conditions in chemostat cultures. Appl Environ Microbiol. 1992 Sep;58(9):3150–3156. doi: 10.1128/aem.58.9.3150-3156.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Verdoni N., Aon M. A., Lebeault J. M., Thomas D. Proton motive force, energy recycling by end product excretion, and metabolic uncoupling during anaerobic growth of Pseudomonas mendocina. J Bacteriol. 1990 Dec;172(12):6673–6681. doi: 10.1128/jb.172.12.6673-6681.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wackett L. P., Gibson D. T. Degradation of trichloroethylene by toluene dioxygenase in whole-cell studies with Pseudomonas putida F1. Appl Environ Microbiol. 1988 Jul;54(7):1703–1708. doi: 10.1128/aem.54.7.1703-1708.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wackett L. P., Householder S. R. Toxicity of Trichloroethylene to Pseudomonas putida F1 Is Mediated by Toluene Dioxygenase. Appl Environ Microbiol. 1989 Oct;55(10):2723–2725. doi: 10.1128/aem.55.10.2723-2725.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Whited G. M., Gibson D. T. Toluene-4-monooxygenase, a three-component enzyme system that catalyzes the oxidation of toluene to p-cresol in Pseudomonas mendocina KR1. J Bacteriol. 1991 May;173(9):3010–3016. doi: 10.1128/jb.173.9.3010-3016.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yeh W. K., Gibson D. T., Liu T. N. Toluene dioxygenase: a multicomponent enzyme system. Biochem Biophys Res Commun. 1977 Sep 9;78(1):401–410. doi: 10.1016/0006-291x(77)91268-2. [DOI] [PubMed] [Google Scholar]
- Zylstra G. J., Wackett L. P., Gibson D. T. Trichloroethylene degradation by Escherichia coli containing the cloned Pseudomonas putida F1 toluene dioxygenase genes. Appl Environ Microbiol. 1989 Dec;55(12):3162–3166. doi: 10.1128/aem.55.12.3162-3166.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]