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Applied and Environmental Microbiology, January 2006, p. 585-595, Vol. 72, No. 1
0099-2240/06/$08.00+0     doi:10.1128/AEM.72.1.585-595.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Genetic and Genomic Insights into the Role of Benzoate-Catabolic Pathway Redundancy in Burkholderia xenovorans LB400

Center for Microbial Ecology,¹ Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan 48824,² Department of Microbiology and Immunology, University of British Columbia, Vancouver, British Columbia V6T 1Z3, Canada,³ Laboratory of Microbial Ecology and Technology, Ghent University, Ghent, Belgium⁴

Received 10 August 2005/ Accepted 18 October 2005

Transcriptomic and proteomic analyses of Burkholderia xenovorans LB400, a potent polychlorinated biphenyl (PCB) degrader, have implicated growth substrate- and phase-dependent expression of three benzoate-catabolizing pathways: a catechol ortho cleavage (ben-cat) pathway and two benzoyl-coenzyme A pathways, encoded by gene clusters on the large chromosome (box_C) and the megaplasmid (box_M). To elucidate the significance of this apparent redundancy, we constructed mutants with deletions of the ben-cat pathway (the benABCD::kan mutant), the box_C pathway (the boxAB_C::kan mutant), and both pathways (the benABCD boxAB_C::kan mutant). All three mutants oxidized benzoate in resting-cell assays. However, the benABCD::kan and benABCD boxAB_C::kan mutants grew at reduced rates on benzoate and displayed increased lag phases. By contrast, growth on succinate, on 4-hydroxybenzoate, and on biphenyl was unaffected. Microarray and proteomic analyses revealed that cells of the benABCD::kan mutant growing on benzoate expressed both box pathways. Overall, these results indicate that all three pathways catabolize benzoate. Deletion of benABCD abolished the ability of LB400 to grow using 3-chlorobenzoate. None of the benzoate pathways could degrade 2- or 4-chlorobenzoate, indicating that the pathway redundancy does not directly contribute to LB400's PCB-degrading capacities. Finally, an extensive sigmaE-regulated oxidative stress response not present in wild-type LB400 grown on benzoate was detected in these deletion mutants, supporting our earlier suggestion that the box pathways are preferentially active under reduced oxygen tension. Our data further substantiate the expansive network of tightly interconnected and complexly regulated aromatic degradation pathways in LB400.

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