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Identification and analysis of a bottleneck in PCB biodegradation

Nature Structural Biology volume 9, pages 934–939 (2002)Cite this article

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Abstract

The microbial degradation of polychlorinated biphenyls (PCBs) provides the potential to destroy these widespread, toxic and persistent environmental pollutants. For example, the four-step upper bph pathway transforms some of the more than 100 different PCBs found in commercial mixtures and is being engineered for more effective PCB degradation. In the critical third step of this pathway, 2,3-dihydroxybiphenyl (DHB) 1,2-dioxygenase (DHBD; EC 1.13.11.39) catalyzes aromatic ring cleavage. Here we demonstrate that ortho-chlorinated PCB metabolites strongly inhibit DHBD, promote its suicide inactivation and interfere with the degradation of other compounds. For example, kcatapp for 2′,6′-diCl DHB was reduced by a factor of ∼7,000 relative to DHB, and it bound with sufficient affinity to competitively inhibit DHB cleavage at nanomolar concentrations. Crystal structures of two complexes of DHBD with ortho-chlorinated metabolites at 1.7 Å resolution reveal an explanation for these phenomena, which have important implications for bioremediation strategies.

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Figure 1: DHBD-catalyzed ring-cleavage reaction and its inhibition
Figure 2: Illustrations of ortho-chlorinated DHBs bound to the active site of DHBD.

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  • 11 November 2002

    Appended PDF with errata, figure legend updated

Notes

  1. *Note: Due to a mistake that occurred during production of this manuscript, the units for two values reported in the legend of Fig. 1 were incorrect. The correct unit for KiAapp in the legend for Fig. 1b is mM (KiAapp = 2.7 ±0.6 mM), whereas the concentration range of 2-Cl DHB for Fig. 1b insert is µM (0–50 µM). This mistake has been corrected in the HTML version and will appear correctly in print. The PDF for the AOP version of this paper has been appended.

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Acknowledgements

This research was supported by a Strategic grant from the Natural Sciences and Engineering Research Council of Canada (NSERC) and an award from the U.S. National Institutes of Health (NIH). Use of the Argonne National Laboratory Structural Biology Center beamlines at the Advanced Photon Source was supported by the U. S. Department of Energy, Office of Biological and Environmental Research. F.H.V. was the recipient of an NSERC postgraduate scholarship. D.B.N. was supported in part by an NIH institutional training award. S. He, G. Labbé and W. Minor are thanked for their expert assistance.

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Author notes

  1. Shaodong Dai, Frédéric H. Vaillancourt and Victor Snieckus: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Biological Sciences, Markey Center for Structural Biology, Purdue University, West Lafayette, 47907-1392, Indiana, USA

    Shaodong Dai, David B. Neau & Jeffrey T. Bolin

  2. Departments of Microbiology and Biochemistry, University of British Columbia, Vancouver, V6T 1Z3, British Columbia, Canada

    Frédéric H. Vaillancourt & Lindsay D. Eltis

  3. Department of Biochemistry, Pavillon Marchand, Université Laval, Quebec City, G1K 7P4, Quebec, Canada

    Frédéric H. Vaillancourt, Halim Maaroufi, Nathalie M. Drouin & Lindsay D. Eltis

  4. Department of Chemistry, Queen's University, Kingston, K7L 3N6, Ontario, Canada

    Victor Snieckus

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Correspondence to Jeffrey T. Bolin or Lindsay D. Eltis.

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Dai, S., Vaillancourt, F., Maaroufi, H. et al. Identification and analysis of a bottleneck in PCB biodegradation. Nat Struct Mol Biol 9, 934–939 (2002). https://doi.org/10.1038/nsb866

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