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J. Biol. Chem., Vol. 281, Issue 17, 11981-11991, April 28, 2006

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Transcriptional Tradeoff between Metabolic and Stress-response Programs in Pseudomonas putida KT2440 Cells Exposed to Toluene^*

Patricia Domínguez-Cuevas, José-Eduardo González-Pastor, Silvia Marqués, Juan-Luis Ramos¹, and Víctor de Lorenzo^¶

From the Department of Biochemistry and Molecular and Cellular Biology of Plants, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, Profesor Albareda, 1, E-18008 Granada, Spain, Instituto Nacional de Tecnica AeroespacialConsejo Superior de Investigaciones Científicas, Centro de Astrobiología, Torrejón de Ardoz, E-28850 Madrid, Spain, and ^¶Department of Microbiology, Centro Nacional de Biotecnología-Consejo Superior de Investigaciones Científicas, Cantoblanco, E-28049 Madrid, Spain

When Pseudomonas putida KT2440 cells encounter toluene in the growth medium, they perceive it simultaneously as a potential nutrient to be metabolized, as a membrane-damaging toxic drug to be extruded, and as a macromolecule-disrupting agent from which to protect proteins. Each of these inputs requires a dedicated transcriptional response that involves a large number of genes. We used DNA array technology to decipher the interplay between these responses in P. putida KT2440 subjected to a short challenge (15 min) with toluene. We then compared the results with those in cells exposed to o-xylene (a non-biodegradable toluene counterpart) and 3-methylbenzoate (a specific substrate of the lower TOL pathway of the P. putida pWW0 plasmid). The resulting expression profiles suggest that the bulk of the available transcriptional machinery is reassigned to endure general stress, whereas only a small share of the available machinery is redirected to the degradation of the aromatic compounds. Specifically, both toluene and o-xylene induce the TOL pathways and a dedicated but not always productive metabolic program. Similarly, 3-methylbenzoate induces the expression not only of the lower meta pathway but also of the non-productive and potentially deleterious genes for the metabolism of (nonsubstituted) benzoate. In addition, toluene (and to a lesser extent o-xylene) inhibit motility functions as an unequivocal response to aromatic toxicity. We argue that toluene is sensed by P. putida KT2440 as a stressor rather than as a nutrient and that the inhibition by the aromatic compounds of many functions we tested is the tradeoff for activating stress tolerance genes at a minimal cost in terms of energy.

Received for publication, September 7, 2005 , and in revised form, January 24, 2006.

^* This work was supported by European Commission Grant QLK3-CT-2002-1923 and Plan Nacional de Biotecnología Grant GEN2001-4698-CO5-03 (to J.-L. R.) and by grants from the 5th and 6th Framework Programmes of the European Union (to V. d. L.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Tables 1-11.

¹ To whom correspondence should be addressed. Tel.: 34-958-181608 or -181600 (ext. 326); Fax: 34-958-135740; E-mail: jlramos{at}eez.csic.es.

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