Advertisement

Biodegradation

, Volume 17, Issue 5, pp 437–445 | Cite as

Effect of carbon starvation on toluene degradation activity by toluene monooxygenase-expressing bacteria

  • David R. Johnson
  • Joonhong Park
  • Jerome J. Kukor
  • Linda M. Abriola
Article

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.

Keywords

aromatic oxygenase carbon starvation TCE co-metabolism toluene oxidizing bacteria 

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

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

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.

References

  1. 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: 228–235PubMedGoogle Scholar
  2. Arciero D, Vannelli T, Logan M, Hooper AB, (1989) Degradation of trichloroethylene by the ammonia-oxidizing bacterium Nitrosomonas europea Biochem. Biophys. Res. Commun. 159: 640–643CrossRefPubMedGoogle Scholar
  3. Costura RK, Alvarez PJJ, (2000) Expression and longevity of toluene dioxygenase in Pseudomonas putida F1 induced at different dissolved oxygen concentrations Water Res. 34: 3014–3018CrossRefGoogle Scholar
  4. 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: 2858–2863PubMedGoogle Scholar
  5. 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: 1369–1374PubMedGoogle Scholar
  6. Ensign SA, Hyman MR, Arp DJ, (1992) Cometabolic degradation of chlorinated alkenes by alkene monooxygenase in a propylene-grown Xanthobacter strain Appl. Environ. Microbiol. 58:3038–3046PubMedGoogle Scholar
  7. Fishman AF, Tao Y, Wood TK, (2004) Toluene 3-monooxygenase of Ralstonia pickettii PKO1 is a para-hydroxylating enzyme J. Bacteriol. 186:3117–3123CrossRefPubMedGoogle Scholar
  8. Folsom BR, Chapman PJ, Pritchard PH, (1990) Phenol and trichloroethylene degradation by Pseudomonas cepacia G4: kinetics and interactions between substrates Appl. Environ. Microbiol. 56: 1279–1285PubMedGoogle Scholar
  9. 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: 6419–6427CrossRefPubMedGoogle Scholar
  10. Ghiorse WC, Wilson JJ, (1988) Microbial ecology of the terrestrial subsurface Adv. Appl. Microbiol. 33: 107–172PubMedCrossRefGoogle Scholar
  11. 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: 2653–2662CrossRefGoogle Scholar
  12. Heald S, Jenkins RO, 1994. Trichloroethylene removal and oxidation toxicity mediated by toluene dioxygenase of Pseudomonas putida Appl. Environ. Microbiol. 60: 4634–4637PubMedGoogle Scholar
  13. 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: 236–244PubMedGoogle Scholar
  14. 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: 1628–1637CrossRefGoogle Scholar
  15. Jenkins RO, Heald SC, (1996) Stability of toluene oxidation by Pseudomonas putida under nutrient deprivation Appl. Microbiol. Biotechnol. 46: 388–392CrossRefGoogle Scholar
  16. Jones RD, Morita RY, (1985) Survival of a marine ammonia oxidizer under energy-source deprivation Mar. Ecol. Prog. Ser. 26: 175–179CrossRefGoogle Scholar
  17. 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: 565–573CrossRefGoogle Scholar
  18. Leahy JG, Byrne AM, Olsen RH, (1996) Comparison of factors influencing trichloroethylene degradation by toluene-oxidizing bacteria Appl. Environ. Microbiol. 62: 825–833 PubMedGoogle Scholar
  19. 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: 23–30CrossRefGoogle Scholar
  20. Lontoh S, Semrau JD, (1998) Methane and trichloroethylene degradation by Methylosinus trichosporium OB3b expressing particulate methane monooxygenase Appl. Environ. Microbiol. 64: 1106–1114PubMedGoogle Scholar
  21. 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: 542–548PubMedGoogle Scholar
  22. 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: 886–891PubMedGoogle Scholar
  23. 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: 270–276PubMedGoogle Scholar
  24. 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: 88–100CrossRefGoogle Scholar
  25. Morita RY, (1993) Bioavailability of energy and the starvation state. In Kjelleberg S, (Ed.), Starvation in Bacteria, Plenum Press, New York/London pp. 1833–1847Google Scholar
  26. Olsen RH, Hansen J, (1976) Evolution and utility of a Pseudomonas aeruginosa drug resistance factor J. Bacteriol. 125: 837–844PubMedGoogle Scholar
  27. Olsen RH, Kukor JJ, Kaphammer B, (1994) A novel toluene-3-monooxygenase pathway cloned from Pseudomonas pickettii PKO1 J. Bacteriol. 176: 3749–3756PubMedGoogle Scholar
  28. 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, MIGoogle Scholar
  29. Park J, Kukor JJ, Abriola LM, (2002) TCE concentration dependence of TCE inducibility, cometabolism and toxicity in Ralstonia pickettii PKO1 Appl. Environ. Microbiol. 68: 5231–5240CrossRefPubMedGoogle Scholar
  30. 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: 233–256CrossRefPubMedGoogle Scholar
  31. Roslev P, King GM, (1994) Survival and recovery of methanotrophic bacteria starved under oxic and anoxic conditions Appl. Environ. Microbiol. 60: 2602–2608PubMedGoogle Scholar
  32. 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. 55:1624–1629PubMedGoogle Scholar
  33. Shields MS, Reagin MJ, (1992) Selection of a Pseudomonas cepacia strain constitutive for the degradation of trichloroethylene Appl. Environ. Microbiol. 58: 3977–3983PubMedGoogle Scholar
  34. 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: 1352–1356PubMedGoogle Scholar
  35. 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: 1564–1570CrossRefGoogle Scholar
  36. Wackett LP, Hershberger CD, (2001) Biocatalysis and Biodegradation: Microbial Transformation of Organic Compounds. ASM Press, Washington D.CGoogle Scholar
  37. 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: 3010–3016PubMedGoogle Scholar
  38. 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: 2039–2048PubMedGoogle Scholar
  39. 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: 7–13PubMedGoogle Scholar
  40. 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: 235–242PubMedGoogle Scholar
  41. 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: 1498–1503PubMedGoogle Scholar
  42. 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: 3162–3166PubMedGoogle Scholar

Copyright information

© Springer Science+Business Medaia Inc. 2006

Authors and Affiliations

  • David R. Johnson
    • 1
  • Joonhong Park
    • 2
  • Jerome J. Kukor
    • 3
    • 4
  • Linda M. Abriola
    • 1
    • 5
  1. 1.Department of Civil and Environmental EngineeringUniversity of Michigan Ann ArborUSA
  2. 2.School of Civil and Environmental EngineeringYonsei UniversitySeoulRepublic of Korea
  3. 3.Biotechnology Center for Agriculture and the EnvironmentRutgers UniversityNew BrunswickUSA
  4. 4.Department of Environmental Sciences, Cooks CollegeRutgers UniversityNew BrunswickUSA
  5. 5.Department of Civil and Environmental EngineeringTufts UniversityMedfordUSA

Personalised recommendations