Regulatory noise in prokaryotic promoters: how bacteria learn to respond to novel environmental signals.

Various features of the regulation of pathways for biodegradation of recalcitrant compounds by Pseudomonas provide insights into the mechanisms by which operons evolve to acquire conditionally active promoters that permit the corresponding genes to be transcribed only when required. The "regulatory noise hypothesis' proposes that transcriptional control systems develop responsiveness to new signals due to the leakiness and lack of specificity of preexisting promoters and regulators. When needed, these may become more specific through suppression of undesirable signals and further fine-tuning of the recruited proteins to interact with distinct chemicals. This hypothesis is supported by the sophisticated regulation of sigma 54-dependent promoters of the TOL (toluene biodegradation) operons, which can be activated to various degrees by heterologous proteins. Such "illegitimate' activation is suppressed by bent DNA structures, either static or protein induced, between promoter core elements. Therefore, not only the regulators but also the DNA sequences participate in the process that gives rise to novel specificities.