Transcriptional tradeoff between metabolic and stress-response programs in Pseudomonas putida KT2440 cells exposed to toluene.
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.
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.
Patricia
P
Domínguez-Cuevas
José-Eduardo
JE
González-Pastor
Silvia
S
Marqués
Juan-Luis
JL
Ramos
Víctor
V
de Lorenzo
D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism; D001565:Benzoates / Q000494:pharmacology; D002465:Cell Movement / Q000187:drug effects; D020869:Gene Expression Profiling; D015964:Gene Expression Regulation, Bacterial; D020411:Oligonucleotide Array Sequence Analysis; D016958:Pseudomonas putida / Q000187:drug effects / Q000235:genetics / Q000378:metabolism; D015398:Signal Transduction; D012997:Solvents / Q000494:pharmacology*; D014050:Toluene / Q000494:pharmacology*; D014158:Transcription, Genetic / Q000187:drug effects*; D014992:Xylenes / Q000494:pharmacology
D001426:Bacterial Proteins; D001565:Benzoates; D012997:Solvents; D014992:Xylenes; D014050:Toluene; C026114:2-xylene