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Trichloroethylene degradation by butane-oxidizing bacteria causes a spectrum of toxic effects

  • Applied Microbial and Cell Physiology
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Abstract

The physiological consequences of trichloroethylene (TCE) transformation by three butane oxidizers were examined. Pseudomonas butanovora, Mycobacterium vaccae, and Nocardioides sp. CF8 utilize distinctly different butane monooxygenases (BMOs) to initiate degradation of the recalcitrant TCE molecule. Although the primary toxic event resulting from TCE cometabolism by these three strains was loss of BMO activity, species differences were observed. P. butanovora and Nocardioides sp. CF8 maintained only 4% residual BMO activity following exposure to 165 μM TCE for 90 min and 180 min, respectively. In contrast, M. vaccae maintained 34% residual activity even after exposure to 165 μM TCE for 300 min. Culture viability was reduced 83% in P. butanovora, but was unaffected in the other two species. Transformation of 530 nmol of TCE by P. butanovora (1.0 mg total protein) did not affect the viability of BMO-deficient P. butanovora cells, whereas transformation of 482 nmol of TCE by toluene-grown Burkholderia cepacia G4 caused 87% of BMO-deficient P. butanovora cells to lose viability. Together, these results contrast with those previously reported for other bacteria carrying out TCE cometabolism and demonstrate the range of cellular toxicities associated with TCE cometabolism.

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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

    Article  CAS  Google Scholar 

  • Arp DJ (1999) Butane metabolism by butane-grown ‘Pseudomonas butanovora’. Microbiology 145:1173–1180

    Article  CAS  Google Scholar 

  • Arp DJ, Yeager CM, Hyman MR (2001) Molecular and cellular fundamentals of aerobic cometabolism of trichloroethylene. Biodegradation 12:81–103

    Article  CAS  Google Scholar 

  • Brzostowicz P, Walters DM, Thomas SM, Nagarajan V, Rouviere PE (2003) mRNA differential display in a microbial enrichment culture: simultaneous identification of three cyclohexanone monooxygenases from three species. Appl Environ Microbiol 69:334–342

    Article  CAS  Google Scholar 

  • Chu KH, Alvarez-Cohen L (1998) Effect of nitrogen source on growth and TCE degradation by methane-oxidizing bacteria. Appl Environ Microbiol 64:3451–3457

    Article  CAS  Google Scholar 

  • Chu KH, Alvarez-Cohen L (1999) Evaluation of toxic effects of aeration and trichloroethylene oxidation on methanotrophic bacteria grown with different nitrogen sources. Appl Environ Microbiol 65:766–772

    Article  CAS  Google Scholar 

  • Coleman NV, Mattes TE, Gossett JM, Spain JC (2002) Biodegradation of cis-dichloroethene as the sole carbon source by a β-proteobacterium. Appl Environ Microbiol 68:2726–2730

    Article  CAS  Google Scholar 

  • Gornall AG, Bardawill CJ, David MM (1949) Determination of serum proteins by means of the Biuret reaction. J Biol Chem 177:751–766

    CAS  PubMed  Google Scholar 

  • Gossett JM (1987) Measurement of Henry’s law constants for C1 and C2 chlorinated hydrocarbons. Environ Sci Technol 21:202–208

    Article  CAS  Google Scholar 

  • Hamamura N, Arp DJ (2000) Isolation and characterization of alkane-utilizing Nocardioides sp. strain CF8. FEMS Microbiol Lett 186:21–26

    Article  CAS  Google Scholar 

  • Hamamura N, Page C, Long T, Semprini L, Arp DJ (1997) Chloroform cometabolism by butane-grown CF8, Pseudomonas butanovora, and Mycobacterium vaccae JOB5 and methane-grown Methylosinus trichosporium OB3b. Appl Environ Microbiol 63:3607–3613

    Article  CAS  Google Scholar 

  • Hamamura N, Storfa RT, Semprini L, Arp DJ (1999) Diversity in butane monooxygenases among butane-grown bacteria. Appl Environ Microbiol 65:4586–4593

    Article  CAS  Google Scholar 

  • Hamamura N, Yeager CM, Arp DJ (2001) Two distinct monooxygenases for alkane oxidation in Nocardioides sp. strain CF8. Appl Environ Microbiol 67:4992–4998

    Article  CAS  Google Scholar 

  • Kim Y, Semprini L, Arp DJ (1997) Aerobic cometabolism of chloroform, 1,1,1-trichloroethane, and other chlorinated aliphatic hydrocarbons by butane-utilizing microorganisms. In: Alleman BC, Lecson A (eds) In-Situ and On-Site Bioremediation 4(3). Battelle Press, Columbus, CH, pp 247–252

    Google Scholar 

  • Kim Y, Arp DJ, Semprini L (2000) Chlorinated solvent cometabolism by butane-grown mixed culture. J Environ Eng 126:934–942

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Newman LM, Wackett LP (1997) Trichloroethylene oxidation by purified toluene 2-monooxygenase: products, kinetics, and turnover-dependent inactivation. J Bacteriol 179:90–96

    Article  CAS  Google Scholar 

  • Pardi J, Sayavedra-Soto LA, Semprini L (2001) Bioaugmentation of butane-utilizing microorganisms to promote cometabolism of 1,1,1-trichloroethane in groundwater microcosms. Biodegradation 12:11–22

    Article  Google Scholar 

  • Rasche ME, Hyman MR, Arp DJ (1991) Factors limiting aliphatic chlorocarbon degradation by Nitrosomonas europaea: cometabolic inactivation of ammonia monooxygenase and substrate specificity. Appl Environ Microbiol 57:2986–2994

    Article  CAS  Google Scholar 

  • Silverman RB (1988) Mechanism-based inactivation: chemistry and enzymology. CRC, Boca Raton

    Google Scholar 

  • Sluis MK, Sayavedra-Soto LA, Arp DJ (2002) Molecular analysis of the soluble butane monooxygenase from ‘Pseudomonas butanovora’. Microbiology 148:3617–3629

    Article  CAS  Google Scholar 

  • Vangnai AS, Arp DJ, Sayavedra-Soto LA (2002) Two distinct alcohol dehydrogenases participate in butane metabolism by Pseudomonas butanovora. J Bacteriol 184:1916–1924

    Article  CAS  Google Scholar 

  • Hylckama Vlieg JET van, Koning W de, Janssen DB (1996) Transformation kinetics of chlorinated ethenes by Methylosinus trichosporium OB3b and detection of unstable epoxides by on-line gas chromatography. Appl Environ Microbiol 62:3304–3312

    Article  Google Scholar 

  • Hylckama Vlieg JET van, Koning W de, Janssen LP (1997) Effect of chlorinated ethene conversion on viability and activity of Methylosinus trichosporium OB3b. Appl Environ Microbiol 63:4961–4964

    Article  Google Scholar 

  • Wackett LP, Brusseau GA, Householder SR, Hanson RS (1989) Survey of microbial oxygenases: trichloroethylene degradation by propane-oxidizing bacteria. Appl Environ Microbiol 55:2960–2964

    Article  CAS  Google Scholar 

  • Wiegant WW, Bont JAM de (1980) A new route for ethylene glycol metabolism in Mycobacterium E44. J Gen Microbiol 120:325–331

    CAS  Google Scholar 

  • Yeager CM, Bottomley PJ, Arp DJ (2001) Cytotoxicity associated with trichloroethylene oxidation in Burkholderia cepacia G4. Appl Environ Microbiol 67:2107–2115

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the office of Research and Development, United States Environmental Protection Agency, under Agreement R-828772 through the Western Region Hazardous Substance Research Center.

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Authors and Affiliations

  1. Molecular and Cellular Biology Program, Oregon State University, ALS 3021, Corvallis, OR 97331-2902, USA

    Kimberly H. Halsey

  2. Department of Botany and Plant Pathology, Oregon State University, Cordley 2082, Corvallis, OR 97331-2902, USA

    Luis A. Sayavedra-Soto & Daniel J. Arp

  3. Department of Microbiology, Oregon State University, Nash 220, Corvallis, OR 97331-2902, USA

    Peter J. Bottomley

Authors
  1. Kimberly H. Halsey
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  2. Luis A. Sayavedra-Soto
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  3. Peter J. Bottomley
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  4. Daniel J. Arp
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Correspondence to Daniel J. Arp.

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Halsey, K.H., Sayavedra-Soto, L.A., Bottomley, P.J. et al. Trichloroethylene degradation by butane-oxidizing bacteria causes a spectrum of toxic effects. Appl Microbiol Biotechnol 68, 794–801 (2005). https://doi.org/10.1007/s00253-005-1944-z

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  • DOI: https://doi.org/10.1007/s00253-005-1944-z

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