Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Anaerobic benzene oxidation coupled to nitrate reduction in pure culture by two strains of Dechloromonas

Abstract

Benzene contamination is a significant problem. It is used in a wide range of manufacturing processes and is a primary component of petroleum-based fuels. Benzene is a hydrocarbon that is soluble, mobile, toxic and stable, especially in ground and surface waters. It is poorly biodegraded in the absence of oxygen. However, anaerobic benzene biodegradation has been documented under various conditions. Although benzene biomineralization has been demonstrated with nitrate1, Fe(III)2,3,4,5, sulphate6,7 or CO28,9 as alternative electron acceptors, these studies were based on sediments or microbial enrichments. Until now there were no organisms in pure culture that degraded benzene anaerobically. Here we report two Dechloromonas strains, RCB and JJ, that can completely mineralize various mono-aromatic compounds including benzene to CO2 in the absence of O2 with nitrate as the electron acceptor. This is the first example, to our knowledge, of an organism of any type that can oxidize benzene anaerobically, and we demonstrate the potential applicability of these organisms to the treatment of contaminated environments.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2: Growth of strain RCB (mean of triplicate determinations) with AHDS (5 mM) as the electron donor and chlorate (10 mM) as the electron acceptor.
Figure 3: Phylogenetic tree of the 16S rDNA sequences of strains RCB and JJ and their closest relatives resulting from a heuristic search with parsimony analysis.
Figure 4: Anaerobic oxidation of benzene by strains JJ and RCB (mean of triplicate determinations).
Figure 5: Degradation of [14C]benzene in anoxic sediments amended with nitrate (10 mM) in the presence and absence of strain RCB (mean of triplicate determinations).

Similar content being viewed by others

References

  1. Burland, S. M. & Edwards, E. A. Anaerobic benzene biodegradation linked to nitrate reduction. Appl. Environ. Microbiol. 65, 529–533 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Lovley, D. R., Woodward, J. C. & Chapelle, F. H. Stimulated anoxic biodegradation of aromatic hydrocarbons using Fe(III) ligands. Nature 370, 128–131 (1994).

    Article  ADS  CAS  PubMed  Google Scholar 

  3. Lovley, D. R., Woodward, J. C. & Chapelle, F. H. Rapid anaerobic benzene degradation with a variety of chelated Fe(III) forms. Appl. Environ. Microbiol. 62, 288–291 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Anderson, R. T. & Lovley, D. R. Naphthalene and benzene degradation under Fe(III)-reducing conditions in petroleum-contaminated aquifers. Bioremed. J. 3, 121–135 (1999).

    Article  CAS  Google Scholar 

  5. Anderson, R. T., Rooney-Varga, J., Gaw, C. V. & Lovley, D. R. Anaerobic benzene oxidation in the Fe(III) reduction zone of petroleum-contaminated aquifers. Environ. Sci. Technol. 32, 1222–1229 (1998).

    Article  ADS  CAS  Google Scholar 

  6. Lovley, D. R., Coates, J. D., Woodward, J. C. & Phillips, E. J. P. Benzene oxidation coupled to sulfate reduction. Appl. Environ. Microbiol. 61, 953–958 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Weiner, J. & Lovley, D. R. Anaerobic benzene degradation in petroleum-contaminated sediments after inoculation with a benzene-oxidizing enrichment. Appl. Environ. Microbiol. 64, 775–778 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Grbic-Galic, D. & Vogel, T. Transformation of toluene and benzene by mixed methanogenic cultures. Appl. Environ. Microbiol. 53, 254–260 (1987).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Weiner, J. & Lovley, D. R. Rapid benzene degradation in methanogenic sediments from a petroleum-contaminated aquifer. Appl. Environ. Microbiol. 64, 1937–1939 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Anderson, R. T. & Lovley, D. R. Ecology and biogeochemistry of in situ groundwater bioremediation. Adv. Microb. Ecol. 15, 289–350 (1997).

    Article  CAS  Google Scholar 

  11. Ridgeway, H. F., Safarik, J., Phipps, D., Carl, P. & Clark, D. Identification and catabolic activity of well-derived gasoline-degrading bacteria and a contaminated aquifer. Appl. Environ. Microbiol. 56, 3565–3575 (1990).

    Google Scholar 

  12. Christensen, T., Kjeldsen, P., Albrechtsen, H. & Heron, G. Attenuation of pollutants in landfill leachate polluted aquifers. Crit. Rev. Environ. Sci. Technol. 24, 119–202 (1994).

    Article  CAS  Google Scholar 

  13. Lovley, D. R. Potential for anaerobic bioremediation of BTEX in petroleum-contaminated aquifers. J. Ind. Microbiol. 18, 75–81 (1997).

    Article  CAS  Google Scholar 

  14. Coates, J. D., Anderson, R. T. & Lovley, D. R. Anaerobic oxidation of polycyclic aromatic hydrocarbons under sulfate-reducing conditions. Appl. Environ. Microbiol. 62, 1099–1101 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Coates, J. D., Woodward, J., Allen, J., Philp, P. & Lovley, D. R. Anaerobic degradation of polycyclic aromatic hydrocarbons and alkanes in petroleum-contaminated marine harbor sediments. Appl. Environ. Microbiol. 63, 3589–3593 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Coates, J. D., Anderson, R. T. & Lovley, D. R. Anaerobic hydrocarbon degradation in petroleum-contaminated harbor sediments under sulfate-reducing and artificially imposed iron-reducing conditions. Environ. Sci. Technol. 30, 2784–2789 (1996).

    Article  ADS  CAS  Google Scholar 

  17. Galushko, A., Minz, D., Schink, B. & Widdel, F. Anaerobic degradation of naphthalene by a pure culture of a novel type of marine sulfate-reducing bacterium. Environ. Microbiol. 1, 415–420 (1999).

    Article  CAS  PubMed  Google Scholar 

  18. Rabus, R., Nordhaus, R., Ludwig, W. & Widdel, F. Complete oxidation of toluene under strictly anoxic conditions by a new sulfate-reducing bacterium. Appl. Environ. Microbiol. 59, 1444–1451 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Lovley, D. R. & Lonergan, D. J. Anaerobic oxidation of toluene, phenol, and p-cresol by the dissimilatory iron-reducing organism, GS-15. Appl. Environ. Microbiol. 56, 1858–1864 (1990).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Coates, J. D., Phillips, E. J. P., Lonergan, D. J., Jenter, H. & Lovley, D. R. Isolation of Geobacter species from a variety of sedimentary environments. Appl. Environ. Microbiol. 62, 1531–1536 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Vogel, T. M. & Grbic-Galic, D. Incorporation of oxygen from water into toluene and benzene during anaerobic fermentative transformation. Appl. Environ. Microbiol. 52, 200–202 (1986).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Rooney-Varga, J. N., Anderson, R. T. & Fraga, J. L. Microbial communities associated with anaerobic benzene degradation in a petroleum-contaminated aquifer. Appl. Environ. Microbiol. 65, 3056–3063 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Bruce, R. A., Achenbach, L. A. & Coates, J. D. Reduction of (per)chlorate by a novel organism isolated from a paper mill waste. Environ. Microbiol. 1, 319–331 (1999).

    Article  CAS  PubMed  Google Scholar 

  24. Coates, J. D. et al. The ubiquity and diversity of dissimilatory (per)chlorate-reducing bacteria. Appl. Environ. Microbiol. 65, 5234–5241 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Coates, J. D., Bruce, R. A., Patrick, J. A. & Achenbach, L. A. Hydrocarbon bioremediative potential of (per)chlorate-reducing bacteria. Bioremed. J. 3, 323–334 (1999).

    Article  CAS  Google Scholar 

  26. Lovley, D. R., Fraga, J. L., Coates, J. D. & Blunt-Harris, E. L. Humics as an electron donor for anaerobic respiration. Environ. Microbiol. 1, 89–98 (1999).

    Article  CAS  PubMed  Google Scholar 

  27. Achenbach, L. A., Bruce, R. A., Michaelidou, U. & Coates, J. D. Dechloromonas agitata N. N. gen., sp. nov. and Dechlorosoma suillum N. N. gen., sp. nov. two novel environmentally dominant (per)chlorate-reducing bacteria and their phylogenetic position. Int. J. Syst. Evol. Microbiol. 51, 527–533 (2001).

    Article  CAS  PubMed  Google Scholar 

  28. Achenbach, L. A. & Coates, J. D. Disparity between bacterial phylogeny and physiology. ASM News 66, 714–716 (2000).

    Google Scholar 

  29. Anderson, R. T. & Lovley, D. R. Anaerobic bioremediation of benzene under sulfate-reducing conditions in a petroleum contaminated aquifer. Environ. Sci. Technol. 34, 2261–2266 (2000).

    Article  ADS  CAS  Google Scholar 

  30. Coates, J. D., Bruce, R. A. & Haddock, J. D. Anoxic bioremediation of hydrocarbons. Nature 396, 730 (1998).

    Article  ADS  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported in part by funding to J.D.C. by the US Office of Naval Research. Funding to J.D.C. and L.A.A. was also from the US Department of Defense SERDP Program.

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Coates, J., Chakraborty, R., Lack, J. et al. Anaerobic benzene oxidation coupled to nitrate reduction in pure culture by two strains of Dechloromonas. Nature 411, 1039–1043 (2001). https://doi.org/10.1038/35082545

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35082545

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing