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Bacteria use two‐component signal transduction pathways to sense both extracellular and intracellular environment and to coordinate cellular events according to changing conditions. Adaptation can be either physiological or genetical. Here, we present evidence that a genome reorganization process such as transposition can be controlled by certain environmental cues  sensed  by  a  two‐component  signal  transduction system. We demonstrate that transposition‐dependent accumulation of phenol‐utilizing mutants is severely decreased in Pseudomonas putida defective in a two‐component system colRS. Translocation of Tn4652 is decreased both in colR‐ and colS‐defective strains, indicating that signal transduction from a histidine kinase ColS to a response regulator ColR is necessary for the activation of Tn4652 in bacteria starving on phenol. However, overexpression of ColR in a colS‐defective …