Abstract
Subsurface bacteria commonly exist in a starvation state with only periodic exposure to utilizable sources of carbon and energy. In this study, the effect of carbon starvation on aerobic toluene degradation was quantitatively evaluated with a selection of bacteria representing all the known toluene oxygenase enzyme pathways. For all the investigated strains, the rate of toluene biodegradation decreased exponentially with starvation time. First-order deactivation rate constants for TMO-expressing bacteria were approximately an order of magnitude greater than those for other oxygenase-expressing bacteria. When growth conditions (the type of growth substrate and the type and concentration of toluene oxygenase inducer) were varied in the cultures prior to the deactivation experiments, the rate of deactivation was not significantly affected, suggesting that the rate of deactivation is independent of previous substrate/inducer conditions. Because TMO-expressing bacteria are known to efficiently detoxify TCE in subsurface environments, these findings have significant implications for in situ TCE bioremediation, specifically for environments experiencing variable growth-substrate exposure conditions.
Similar content being viewed by others
Abbreviations
- AMO:
-
ammonia monooxygenase
- BM:
-
basal salt medium
- CFU:
-
colony forming unit
- MMO:
-
methane monooxygenase
- TCE:
-
trichloroethylene
- TDO:
-
toluene dioxygenase
- TMO:
-
toluene monooxygenase
- T4MO:
-
toluene-4-monooxygenase
- TNA:
-
tryptone nutrient agar
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
Arciero D, Vannelli T, Logan M, Hooper AB, (1989) Degradation of trichloroethylene by the ammonia-oxidizing bacterium Nitrosomonas europea Biochem. Biophys. Res. Commun. 159: 640–643
Costura RK, Alvarez PJJ, (2000) Expression and longevity of toluene dioxygenase in Pseudomonas putida F1 induced at different dissolved oxygen concentrations Water Res. 34: 3014–3018
Duetz WA, De Jong C, Williams PA, Van Andel JG, (1994) Competition in chemostat culture between Pseudomonas strains that use different pathways for the degradation of toluene Appl. Environ. Microbiol. 60: 2858–2863
Duetz WA, van Andel JG, (1991) Stability of TOL plasmid pWWO in Pseudomonas putida mt-2 under non-selective conditions in continuous culture J. Gen. Microbiol. 137: 1369–1374
Ensign SA, Hyman MR, Arp DJ, (1992) Cometabolic degradation of chlorinated alkenes by alkene monooxygenase in a propylene-grown Xanthobacter strain Appl. Environ. Microbiol. 58:3038–3046
Fishman AF, Tao Y, Wood TK, (2004) Toluene 3-monooxygenase of Ralstonia pickettii PKO1 is a para-hydroxylating enzyme J. Bacteriol. 186:3117–3123
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
Ghiorse WC, Wilson JJ, (1988) Microbial ecology of the terrestrial subsurface Adv. Appl. Microbiol. 33: 107–172
Gibson DT, Hensley M, Yoshioka H, Mabry TJ, (1970) Formation of (+)-cis-2,3-dihydroxy-1-methylcyclohexa-4,6-diene from toluene by Pseudomonas putida Biochemistry 7: 2653–2662
Heald S, Jenkins RO, 1994. Trichloroethylene removal and oxidation toxicity mediated by toluene dioxygenase of Pseudomonas putida Appl. Environ. Microbiol. 60: 4634–4637
Henry SM, Grbic-Galic D, (1991) Influence of endogenous and exogenous electron donors and trichloroethylene oxidation toxicity on trichloroethylene oxidation by methanotrophic cultures from a groundwater aquifer Appl. Environ. Microbiol. 57: 236–244
Hopkins GD, McCarty PL, (1995) Field evaluation of in situ aerobic cometabolism of trichloroethylene and three dichloroethylene isomers using phenol and toluene as the primary substrates Environ. Sci. Technol. 29: 1628–1637
Jenkins RO, Heald SC, (1996) Stability of toluene oxidation by Pseudomonas putida under nutrient deprivation Appl. Microbiol. Biotechnol. 46: 388–392
Jones RD, Morita RY, (1985) Survival of a marine ammonia oxidizer under energy-source deprivation Mar. Ecol. Prog. Ser. 26: 175–179
Lang M, Roberts PV, Semprini L, (1997). Model simulations in support of field scale design and operation of bioremediation based on cometabolic degradation Ground Water 35: 565–573
Leahy JG, Byrne AM, Olsen RH, (1996) Comparison of factors influencing trichloroethylene degradation by toluene-oxidizing bacteria Appl. Environ. Microbiol. 62: 825–833
Leahy JG, Olsen RH, (1997) Kinetics of toluene degradation by toluene-oxidizing bacteria as a function of oxygen concentration, and the effect of nitrate FEMS Microbiol. Ecol. 23: 23–30
Lontoh S, Semrau JD, (1998) Methane and trichloroethylene degradation by Methylosinus trichosporium OB3b expressing particulate methane monooxygenase Appl. Environ. Microbiol. 64: 1106–1114
Malachowsky KJ, Phelps TJ, Teboli AB, Minnikin DE, White DC, (1994) Aerobic mineralization of trichloroethylene, vinyl chloride, and aromatic compounds by Rhodococcus species Appl. Environ. Microbiol. 60: 542–548
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. 62: 886–891
Massol-Deyá A, Weller R, Rios-Hernandez L, Zhou JZ, Hickey RF, Tiedje JM, (1997) Succession and convergence of biofilm communities in fixed film reactors treating aromatic hydrocarbons in groundwater Appl. Environ. Microbiol. 63: 270–276
McCarty PL, Goltz MN, Hopkins GD, Dolan ME, Allan JP, Kawakami BT, Carrothers TJ, (1998) Full-scale evaluation of in situ cometabolic degradation of TCE in groundwater through toluene injection Environ. Sci. Technol. 32: 88–100
Morita RY, (1993) Bioavailability of energy and the starvation state. In Kjelleberg S, (Ed.), Starvation in Bacteria, Plenum Press, New York/London pp. 1833–1847
Olsen RH, Hansen J, (1976) Evolution and utility of a Pseudomonas aeruginosa drug resistance factor J. Bacteriol. 125: 837–844
Olsen RH, Kukor JJ, Kaphammer B, (1994) A novel toluene-3-monooxygenase pathway cloned from Pseudomonas pickettii PKO1 J. Bacteriol. 176: 3749–3756
Park J, (2001) Influence of Substrate Exposure History on Biodegradation in Porous Media by Ralstonia pickettii PKO1. Doctoral dissertation. The University of Michigan, Ann Arbor, MI
Park J, Kukor JJ, Abriola LM, (2002) TCE concentration dependence of TCE inducibility, cometabolism and toxicity in Ralstonia pickettii PKO1 Appl. Environ. Microbiol. 68: 5231–5240
Park J, Chen Y-M, Kukor JJ, Abriola LM, (2001) Influence of substrate exposure history on biodegradation in a porous medium J. Contam. Hydrol. 51: 233–256
Roslev P, King GM, (1994) Survival and recovery of methanotrophic bacteria starved under oxic and anoxic conditions Appl. Environ. Microbiol. 60: 2602–2608
Shields MS, Montgomery SO, Chapman PJ, Cuskey SM, Pritchard PH, (1989) Novel pathway of toluene catabolism in the trichloroethylene-degrading bacterium G4 Appl. Environ. Microbiol. 55:1624–1629
Shields MS, Reagin MJ, (1992) Selection of a Pseudomonas cepacia strain constitutive for the degradation of trichloroethylene Appl. Environ. Microbiol. 58: 3977–3983
Shields MS, Reagin MJ, Gerger RR, Campbell R, Somerville C, (1995) TOM, a new aromatic degradative plasmid from Burkholderia (Pseudomonas) cepacia G4 Appl. Environ. Microbiol. 61: 1352–1356
Vroblesky DA, Champelle FH, (1994) Temporal and spatial changes of terminal electron-accepting processes in a petroleum hydrocarbon-contaminated aquifer and the significance for contaminant biodegradation Water Resour. Res. 30: 1564–1570
Wackett LP, Hershberger CD, (2001) Biocatalysis and Biodegradation: Microbial Transformation of Organic Compounds. ASM Press, Washington D.C
Whited GM, Gibson DT, (1991) Toluene-4-monooxygenase, a three-component enzyme system that catalyzes the oxidation of toluene to p-cresol in Pseudomonas mendocina KR1 J. Bacteriol. 173: 3010–3016
Williams PA, Taylor SD, Gibb LE, (1988) Loss of the toluene-xylene catabolic genes of TOL plasmid pWWO during growth of Pseudomonas putida on benzoate is due to a selective growth advantage of ‘cured’ segregants J. Gen. Microbiol. 134: 2039–2048
Worsey MJ, Williams PA, (1975) Metabolism of toluene and xylenes by Pseudomonas putida (arvilla) mt-2: evidence of a new function of the TOL plasmid J. Bacteriol. 124: 7–13
Wright A, Olsen RH, (1994) Self-mobilization and organization of the genes encoding the toluene metabolic pathway of Pseudomonas mendocina KR1 Appl. Environ. Microbiol. 60: 235–242
Zylstra GJ, McCombie WR, Gibson DT, Finette BA, (1988) Toluene degradation by Pseudomonas putida F1: genetic organization of the tod operon Appl. Environ. Microbiol. 54: 1498–1503
Zylstra GJ, Wackett LP, Gibson DT, (1989) Trichloroethylene degradation by Escherichia coli containing the cloned Pseudomonas putida F1 toluene dioxygenase genes Appl. Environ. Microbiol. 55: 3162–3166
Acknowledgements
We are grateful to Malcolm S. Shields, University of South Florida, for providing Burkholderia cepacia strains G4 and G4-PR131, and to Fredrick D. Bost, Rutgers University, for useful discussion. This research was supported by the National Institute of Environmental Health Sciences Superfund Basic Research Program (Grant P42-ES-04911). The content of this report does not necessarily represent the views of the agency.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Johnson, D.R., Park, J., Kukor, J.J. et al. Effect of carbon starvation on toluene degradation activity by toluene monooxygenase-expressing bacteria. Biodegradation 17, 437–445 (2006). https://doi.org/10.1007/s10532-005-9014-x
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10532-005-9014-x